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Vision Research 48 (2008) 2070–2089

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Vision Research

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Neuronal mechanisms of visual stability

Robert H. Wurtz *

Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bldg. 49, RM 2A50, Bethesda, MD 20892-4435, USA

a r t i c l e i n f o

Article history:Received 4 February 2008Received in revised form 22 March 2008

Keywords:Stable visionSaccadesCorollary dischargeEfference copyVisual maskingTranssaccadic memoryProprioception

0042-6989/$ - see front matter Published by Elsevierdoi:10.1016/j.visres.2008.03.021

* Fax: +1 301 402 0511.E-mail addresses: [email protected], wurtzr@nei

a b s t r a c t

Human vision is stable and continuous in spite of the incessant interruptions produced by saccadic eyemovements. These rapid eye movements serve vision by directing the high resolution fovea rapidly fromone part of the visual scene to another. They should detract from vision because they generate two majorproblems: displacement of the retinal image with each saccade and blurring of the image during the sac-cade. This review considers the substantial advances in understanding the neuronal mechanisms under-lying this visual stability derived primarily from neuronal recording and inactivation studies in themonkey, an excellent model for systems in the human brain. For the first problem, saccadic displacement,two neuronal candidates are salient. First are the neurons in frontal and parietal cortex with shiftingreceptive fields that provide anticipatory activity with each saccade and are driven by a corollary dis-charge. These could provide the mechanism for a retinotopic hypothesis of visual stability and possiblyfor a transsaccadic memory hypothesis, The second neuronal mechanism is provided by neurons whosevisual response is modulated by eye position (gain field neurons) or are largely independent of eye posi-tion (real position neurons), and these neurons could provide the basis for a spatiotopic hypothesis. Forthe second problem, saccadic suppression, visual masking and corollary discharge are well establishedmechanisms, and possible neuronal correlates have been identified for each.

Published by Elsevier Ltd.

1. Introduction

We think of our visual perception as a unified continuous pan-orama of the world, present at all times and seamless in its conti-nuity. Only when we consider how we acquire this visualknowledge do we appreciate that the underlying mechanisms arenot nearly as seamless as our perception. The biggest challengesarise from the occurrence of rapid or saccadic eye movements thathave been widely recognized following the illustrations of the fre-quency of these movements by Alfred Yarbus (1967). He used thethen newly developed techniques for recording eye movements torecord the shifts of the eye while a subject looked at a visual scene.What he found was hundreds of saccades that rapidly move thefine grained receptors of the fovea from point to point in the visualscene.

Consider the consequences of these movements for vision. If welook at a series of schematic saccades (Fig. 1A) we see that this vi-sual motor sequence has two phases: fixation at a particular loca-tion (blue dots in Fig. 1A) when virtually all vision occurs, and therapidly moving saccades (blue lines in Fig. 1A) when virtually novision occurs. As a consequence of this, the visual system receivesa series of high resolution snapshots centered on different points inthe scene (Fig. 1B). But the problem becomes even more challeng-

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ing. The snapshots transmitted up the optic nerve with successivefixations are all centered on the fovea. There is no information inthis transmission about where in the scene this snapshot is located(Fig. 1C). Finally, interspersed amongst the snapshots are theblurred images of the wide field motion produced by the rapidlymoving eye during the saccade (indicated by the white patchesin Fig. 1C).

How our sense of visual stability survives such disruptions ofthe visual input has been the subject of speculation at least sincethe 1600s and of behavioral investigation for over a hundredyears. Only since techniques became available to record neuronalactivity in the brains of awake animals able to move their eyes,however, has it been possible to look at the brain mechanismsunderlying this stable visual perception. This review attemptsto summarize the major findings that the study of awake ani-mals has permitted and to address the two major questionsemphasized in Fig. 1: the displacement of the retinal imageresulting from the saccade and the suppression of the blur andmotion during the saccade.

A substantial literature has accumulated on visual stability atboth behavioral and neuronal levels, and this has required someselection for this review. First, I will concentrate on the prob-lems of stability generated by saccadic eye movements whichmeans neglecting the equally important questions of stabilityarising from such eye movements as smooth pursuit or thosemade during our movement through the environment. Second,

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Extra} Extraretinal}

(Reafference) Retinal}WholeVisualField Moves

Proprioception(inflow)

Corollary Discharge(outflow)

Fig. 2. Three signals available for producing visual stability: Visual field motion(reafference), Proprioception (extraretinal inflow), Corollary Discharge (CD, ext-raretinal outflow).

Fig. 1. The two problems saccades produce for the visual system. (A) Schematicsaccades (blue lines) and fixations (blue dots) used to illustrate the consequences ofthe saccades for vision. The painting is titled An Unexpected Visitor by Ilya Repin,and was made famous in vision research by Alfred Yarbus who used it as one of theillustrations he had his subjects look at while he recorded their eye movements. (B)The snapshots at the location of each fixation. Shading is intended to indicate re-duction of acuity as the distance from the fovea increases. (C) The transmission inthe optic nerve of the snapshots from three fixations without any information aboutlocation but with the interspersed blurs from the intervening saccades.

R.H. Wurtz / Vision Research 48 (2008) 2070–2089 2071

I will concentrate on the neuronal correlates of stability becausethe goal is to identify possible underlying mechanisms of stabil-ity to which EEG and fMRI make minimal contributions. Third,while it is essential to start each topic by specifying the behaviorto be explained, I will concentrate on those behavioral attributesfor which I see some evidence of at least a potential neuronalmechanism. Finally, the neuronal evidence will be from monkeysunless otherwise indicated because of the similarity of the visualand oculomotor system of old world monkeys and humans andbecause the monkeys can be trained to perform tasks that allow

systematic investigation of the relation between neurons andbehavior.

2. Signals that contribute to visual stability

In order to evaluate the neuronal mechanisms of visual stability,we need to know when changes in the image on the retina resultfrom real world movement and when from eye movement. Onlythree signals and the interactions between them are used to makethis distinction (Fig. 2). The first signal is visual reafference fromthe retina; when the eye moves it generates visual motion and dis-placement signals that can indicate eye movement. The second sig-nal is an extraretinal one; when the eye muscles contract,proprioceptors are activated, and these indicate the eye has moved.This proprioception is an inflow signal from the periphery into thebrain just as is visual input. The third signal is also an extraretinalone. It is a corollary or copy of the command to move the eyes. It isreferred to as an outflow signal because it copies what flows out toactivate the eye muscles. That’s it. All the mechanisms consideredin this review are derived from these three signals and their inter-actions. But their contributions are not equal, and we first separatethe major ones from the minor ones.

2.1. Visual reafference

With each eye movement, the whole visual field moves, and thisoptic flow can be taken as indication of self motion rather than mo-tion in the environment. This visual input is referred to as ‘‘reaffer-ence” (von Holst & Mittelstaedt, 1950) in recognition of its self-generated nature in contrast to the ‘‘exafference” that results frommotion in the real world in front of a stationary eye. With saccades,such full field motion is usually blurred because of their rapiditybut a visual cue remains because the whole field is displaced. Forslower eye movements such as with movement of the subjectthrough the environment such optic flow can be critical. This ‘‘op-tic array” was regarded as the central factor for stability by Gibson(1966), but for saccades the contribution is probably minimal asindicated by the evidence presented below related to corollarydischarge.

2.2. Proprioception

Eye position information from eye muscle proprioceptors couldflow into the brain after the eye moves and interact with the visualinput to produce visual stability. The preponderance of evidenceavailable, however, is that proprioception does not make a sub-stantial contribution to perceptual stability.

A critical test has been to artificially change the position of theeye by electrically stimulating the brain while the monkey was

2072 R.H. Wurtz / Vision Research 48 (2008) 2070–2089

preparing a saccade to a visual target. After the stimulation, thesaccade had to be made to the same visual target, but from anew position. If proprioception provides position information,every time stimulation changed the initial eye position, proprio-ceptive feedback should have indicated that new position, andthe subsequent visually guided saccade should have compensatedfor the change in position. When the eyes were moved by stimulat-ing the motor neurons, compensation did not occur, so that propri-oception could not have conveyed sufficient information about thenew eye position (Mays, Sparks, & Porter, 1987; Schiller & Sandell,1983; Sparks & Mays, 1983). In contrast, when the eyes weremoved by stimulating several synapses above the motor neurons,in the superior colliculus (SC), the saccade did compensate forthe new initial eye position. The simplest interpretation is thatstimulation at higher levels produced not only proprioceptionbut an internal signal, and it was this internal signal that providedinformation on eye position, not proprioception.

A second set of experiments has relied on cutting the proprio-ceptive afferents from the eye. When the nerves were cut, (Guthrie,Porter, & Sparks, 1983), compensation still occurred after SCevoked saccades which indicated again that proprioception wasnot required. In a subsequent set of experiments, Lewis, Zee, Hay-man, and Tamargo (2001) found that saccadic accuracy was notsignificantly altered after a monkey’s proprioceptive afferents werecut. Thus, assuming all the afferents were cut, these experimentsalso indicate that proprioception does not provide an adequateeye position signal for saccades.

Finally, the nature of the eye proprioceptive signal itself hasbeen revealed by the recent discovery by Wang, Zhang, Cohen,and Goldberg (2007) that such an input reaches the face regionof somatosensory cortex (area 3a). They found long latencies forthese proprioceptive signals, frequently about 100 ms (personalcommunication, M.E. Goldberg and Wang et al., 2007), which prob-ably is too late to influence the next saccade.

In net, there is now no good evidence that proprioception isused to provide an extraretinal position signal that could be usedto correct for the effect of eye movement after each saccade. In-stead, the proprioceptive information might be providing the longterm calibration of saccades that are actually made as opposed tothe ones that are planned, particularly in cases where visual infor-mation is not available (Lewis et al., 2001; Wang et al., 2007). Itmight well be that rapid information is provided by a corollaryor copy for each saccade while longer term information is providedby proprioception (Lewis et al., 2001; Steinbach, 1987) includingcases in which static eye deviation leads to misperception of direc-tion (Gauthier, Nommay, & Vercher, 1990).

2.3. Corollary discharge (CD)

The other source of extraretinal information is from a corollaryor copy of the command to move the eye. The basic concept is thatat the same time that instructions are issued for the muscles toproduce a movement, a copy or corollary of those instructions issent to other regions of the brain to inform them of the impendingmovement. The term efference copy was coined by von Holst andMittelstaedt (1950) and the term corollary discharge was coinedin the same year by Sperry (1950)—1950 was a big year for theconcept. In the Sperry experiments, he surgically rotated the eyesof fish by 180 degrees and found as others had that the fish swamin circles. After exploring alternatives, he reached the conclusionthat ‘‘. . .any excitation pattern that normally results in a move-ment that will cause a displacement of the visual image on the ret-ina may have a corollary discharge into the visual centers tocompensate for the retinal displacement.” Thus as the fish nor-mally moved forward a corollary discharge indicated forward mo-tion and this compensated for the backward image motion on the

retina. As the fish with the rotated eye moved forward, the corol-lary stayed the same, but the image motion direction conveyedto the brain was now also forward and this combined with the cor-ollary. The corollary now did not compensate for the retinal motionbut accentuated it, leading to the circling. In the von Holst andMiddlestadt experiments (1950), the test was on the optokineticresponse of a fly to rotation of vertical stripes in front of it, withsimilar logic and interpretation.

While the concepts of efference copy and corollary dischargeare essentially identical, in this review I will use corollary dis-charge (CD). First, the term efference copy implies a copy of theoutput close to the muscles, while the neuronal mechanisms rele-vant to visual stability are at higher levels of the brain includingthe cerebral cortex. Second, the term copy implies that the signalis an exact replica of what is sent to generate the movement, butcorollary need have no such exact identity. Finally the efferencecopy term has been closely associated with the cancellationhypothesis, in which the reafferent input and the efferent copyoutput match, and there is little evidence for such cancellation inthe saccadic system (for discussion see Sommer & Wurtz, 2008).

Whatever the name, the concept is not new, and its history ischronicled in excellent summaries (Bridgeman, 2007; Bridgeman,Van der Heijden, & Velichkovsky, 1994; Grusser, 1995). A few sali-ent points from these reviews illustrate how central the concepthas been for visual stability. Descartes in his Treatise on Man in-ferred what must be the mechanistic difference between the stabil-ity of the visual scene when he moved his eye as opposed to itsinstability when he deflected his eye ball by pushing on it. Evenearlier a Dutch scientist Aquilonius in 1613 made the same pointand concluded that ‘‘an internal faculty of the soul perceives themovement of the eye”. In the 19th century those who consideredthe issue reads like a visual science who’s who: Bell, Purkinje,Mach, and von Helmholtz.

Helmholtz referred to the concept as the ‘‘effort of will”, andmarshaled the evidence in favor of his view. Among the lines ofevidence, three are as significant now as they were then (see Bridg-eman, Hendry, & Stark, 1975; von Helmholtz, 1925). First was thepreviously recognized apparent motion of the visual world whenthe eye is moved passively by pushing on the eyeball. The per-ceived motion was taken to result from the movement of the eyewithout CD. More recent experiments that measured the passiveeye movements (Bridgeman & Stark, 1991; Ilg, Bridgeman, & Hoff-mann, 1989; Stark & Bridgeman, 1983) showed that the perceivedmotion of the visual world resulted from a subject’s attempt whilefixating to counter the external push to rotate the eye rather thanthe rotation of the eye itself. The CD accompanying the attemptedbut blocked eye movement was therefore taken as the source ofthe perceived motion.

Second was the apparent displacement of the visual worldwhen a saccade is attempted but the eye muscles are paralyzed.Considerable controversy followed this observation, because sev-eral subsequent experimenters failed to obtain such a simple find-ing (see Stevens et al. 1976 for a more complete discussion). Thisuncertainty might well have been related to residual eye move-ment due to partial paralysis in some experiments. This ambiguitywas resolved by heroic experiments in which the whole subject,John Stevens, was paralyzed (Stevens et al., 1976). Under suchcomplete paralysis, with each attempted saccade the visual fieldwas displaced in the direction of the intended saccade. There wasalso a greatly increased sense of effort in trying to make the sac-cade, and there was fading of the image over time. These experi-ments also carefully delineated the perception of motion, thesweeping motion of objects in the visual field, from the perceptionof displacement, the sudden shift of an object from one position toanother position. A perception of motion was absent with com-plete paralysis, but was reported with partial paralysis, presum-


ably due to residual eye movements. Thus, with complete paralysisand the delineation of motion and displacement, the conclusions ofHelmholtz were reinstated.

Subsequent paralysis experiments (Matin et al., 1982) went on toshow that in the presence of visual input, perception was controlledby vision rather than any extraretinal input. This ‘‘visual capture”provided a critical perspective on the relative role of CD: when bothvisual and CD information are available, vision prevails.

The third observation was based on images that are fixed on theretina, afterimages. They remain stable when the eye is moved pas-sively in the dark, but they are displaced with saccades (Bridg-eman, 2007). The perception of displacement of an image frozenon the retina must be provided by an extraretinal signal, presum-ably CD.

2.4. Conclusion

Of the three signals available to distinguish eye movement fromworld movement, CD is the critical one for saccadic eye move-ments. The contribution of the other extraretinal signal, proprio-ception, seems unlikely to be significant on a saccade by saccadebasis but rather may be important for longer term calibration.The signature visual input from eye movement, full field motion,may be of less use with the rapid sweep of saccades than withslower pursuit movements or the optic flow with observermovement.

CD will therefore be a central focus of this review, but only withrespect to visual stability since two recent reviews have consideredthe neural basis of the CD more generally (Sommer & Wurtz, 2008).In addition previous reviews and commentaries provide substan-tial details and evaluation of the CD mechanism (Bridgeman,1995, 2007; Bridgeman et al., 1994).

Fig. 3. The logic of shifting receptive fields and remapping. (A) Receptive Field andFuture Field at the time of the saccade. (B) Future field has become the new Rec-eptive Field after the saccade. See text for explanation.

3. Saccadic displacement

3.1. Multiple hypotheses

Conceptually, the most challenging problem is the perception ofvisual stability in spite of the displacement of the image on the ret-ina with each saccade (as illustrated in Fig. 1). How this problem issolved by the brain has been the topic of speculation involvingmany hypotheses with many variations. We will consider twobroad categories of hypotheses and the possible neuronal corre-lates for each. The first hypotheses posit that we maintain only amap of what is currently on the retina, and that this retinotopicmap is simply updated with each saccade. Included here arehypotheses that require updating only of regions to which atten-tion is directed, particularly the small region of the map near thefovea. Possible neuronal mechanisms for this are neurons with ashifting receptive field (RF) in parietal and frontal cortex. The sec-ond group of hypotheses assume that there is a spatiotopic mapwithin the brain and that each successive retinal image updatesthis higher order map. The neuronal evidence for this rests onthe discovery of gain field neurons, whose visual responses aremodulated by the position of the eye in the orbit, and real positionneurons, whose responses are independent of orbital position.

3.2. Visual stability and visually guided movement

Before considering these hypotheses, it is essential to recognizethat maintaining perceptual stability and generating movementoccur simultaneously, and neuronal activity may be related toone and not to the other. A case of separation between perceptionand movement that illustrates the issue is failure to see the dis-placement of a saccade target when the displacement occurs dur-

ing the saccade (Bridgeman et al., 1975). Displacements up to onethird the size of the saccade go undetected. Even though such a dis-placement is not perceived, however, the displaced target can stillbe accurately located when used as a saccade target (Bridgeman,Lewis, Heit, & Nagle, 1979; McLaughlin, 1967). The displacementinformation for the saccade is independent of that for perception.The extent to which neuronal activity is devoted to perceptionrather than to the control of movement is a recurring issue with re-spect to the neuronal correlates of visual stability.

4. Displacement: Retinotopic maps

In this hypothesis, there is no higher order spatial map in thebrain but instead the representation of the visual world always re-mains in retinotopic coordinates. At a neuronal level, we would ex-pect to find a mechanism for updating a retinotopic map, and ascomplicated as it initially may seem, this updating probably hasaccumulated the largest body of neuronal evidence.

4.1. The concept of shifting receptive fields

The landmark experiment of Duhamel, Colby, and Goldberg(1992) showed that neurons in the parietal cortex had the remark-able property that the location of their visual sensitivity shifted inanticipation of the upcoming saccade. This anticipatory change hasbeen referred to as remapping or spatial updating (which empha-sizes the conceptual significance) or as shifting receptive fields(which just describes the neuronal activity).

The concept is best explained by returning to the same illustra-tions used to show the problems generated by saccades but nowwith the aim of understanding how the problem of displacementmight be resolved (Fig. 3). If the subject is looking at one point inthe figure (Fig. 3A, blue dot on the face on the left) and we recordfrom a neuron in the brain, it will be sensitive to visual stimuli

RFprobe

FFprobe

Probe onset(during fixation)

Probe onset(just before saccade)

Noprobe

Fig. 4. An example FEF neuron with a shifting RF. The visual response is aligned onthe visual probe flashed during fixation (left column) and just before the saccade(right column). Probes were in the RF (top row), in the Future Field (FF, middle row),or absent as a control in the bottom row. The visual response shifts from the RF(magenta, left) to the FF (magenta, right) just before the saccade. Each trace is themean and SEM; vertical scale is 110 sp/s; horizontal tick marks, 100 ms. Modifiedfrom Sommer and Wurtz (2006).


falling in one part of the visual field, the RF (Fig. 3A, darkenedcircle). Such localized RFs are what we expect of visual neuronsfrom the retina onward. The cortical neurons considered here,however, have an added property: as the monkey prepares to makethe saccade, the sensitivity at the site the RF will occupy after thesaccade becomes more sensitive even before the saccade occurs.Thus for a time the neuron can respond to stimuli in its currentRF (not surprising) and in its future field (FF in Fig. 3A)—very sur-prising. These neurons must have information about the amplitudeand direction of the impending saccade because the FF sensitivityis located at the site where the RF will be after a saccade. The loca-tion of the FF must depend on a CD of the impending saccade sincehere the FF activity precedes the saccade just as the CD does. Afterthe saccade, the FF becomes the RF of the neuron (Fig. 3B). Thecycle then begins again with preparation to make the next saccade.

So what does this have to do with visual stability? In its sim-plest form, the idea is that it is the increased sensitivity at the FFbefore the saccade that highlights the same object before the sac-cade that will fall on the RF after the saccade. When there is con-gruity between what is there before and after saccade, the eyemust have moved from one fixation point to another. There wouldthen be two successive increases of activity, one reflecting the in-creased sensitivity to the object in the FF, and one as the eye bringsthe RF onto the object. In contrast, if there is just a single increasein visual activity, an object must have appeared in the environ-ment, and it was that appearance that activated the neuron ratherthan a saccade.

While the sequence of events shown in Fig. 3 illustrates theanticipatory events that might be associated with saccades, recentpsychophysical experiments by Melcher (2005,2007) provide evi-dence for such anticipatory changes. In one experiment, for exam-ple, subjects adapted to a tilted grating pattern overlying thefixation point, and then were tested for a tilt after effect as theycontinued to fixate. On subsequent adaptation trials, instead ofcontinuing to fixate, the subjects made saccades to a target. Withsaccades, the adaptation increased by 60% at the new target whileat the same time it decreased by 80% at the current fixation point.Both these changes occurred before the saccade began. Thus thesechanges in adaptation show experimentally essentially what isshown conceptually in Fig. 3. More generally, both the conceptand the experiment emphasize that ‘‘postsaccadic perception doesnot begin anew but rather takes into account previous visual expe-rience” (Melcher, 2007).

4.2. Neurons with shifting receptive fields

Neurons that show evidence of shifting RFs have been studiedin LIP where they were initially discovered (Batista, Buneo, Snyder,& Andersen, 1999; Colby, Duhamel, & Goldberg, 1996; Duhamelet al., 1992; Heiser & Colby, 2006; Kusunoki & Goldberg, 2003),and have subsequently been found in the visual-motor area offrontal cortex, FEF (Sommer & Wurtz, 2006; Umeno & Goldberg,1997, 2001). The shifting RFs have also been seen in earlier extras-triate visual areas (Nakamura & Colby, 2002; Tolias et al., 2001),and the SC (Walker, FitzGibbon, & Goldberg, 1994). There is alsofMRI evidence for them in the human brain (Medendorp, Goltz, Vi-lis, & Crawford, 2003; Merriam, Genovese, & Colby, 2003, 2007).

Fig. 4 shows an example of a shifting RF of a frontal eye field(FEF) neuron. The basic strategy is to probe the sensitivity of theRF and FF locations at varying times before and after the saccadewith brief light flashes. While the monkey fixated, the neuron re-sponded only to probes flashed in the RF (Fig. 4 top row), but justbefore the saccade, it responded to probes flashed in the FF (Fig. 4middle row). After the saccade the probe was only effective in thearea of the FF which, because of the saccade, was now the RF. Theincreased sensitivity at the FF was not activity simply related to the

saccade because when there was no probe, there was no increasedactivity (Fig. 4 bottom row). The shifting RF is a change in sensitiv-ity in the FF that is only revealed when probed with a stimulus.

The shifting RFs neurons become understandable if they receivenot only visual input, but also a CD input that provides the vectorof the impending saccade that would point to the new fixationlocation. The RFs with a fixed retinotopic relation to the currentfixation point would have the same relation to the target of thesaccade (which becomes the new fixation point after the saccade).While identified visual pathways to frontal cortex are numerous(Salin & Bullier, 1995), pathways carrying a corollary dischargeare not, so the next issue is identifying such a CD pathway.

4.3. A CD to cerebral cortex

The fundamental problem in identifying a CD in the primatebrain is two fold. First it is necessary to understand the brain cir-cuits for pre-motor processing in order to identify the level fromwhich the CD is drawn. Second, the CD has to be identified as sep-arate from the signal that actually produces the movement. In themonkey both of these requirements have been met.

The outline of the circuit for the generation of saccades is prob-ably better understood than that for any other coordinated move-ment circuit in the primate brain in part because the saccade is arelatively simple movement (Robinson, 1964, 1968) and in part be-cause of the substantial number of studies devoted to it since the1960s. Fig. 5A shows an outline of this circuit extending from theretina to the eye muscles. In outline, the visual input arrives at stri-ate or V1 cortex through a retinal-lateral geniculate pathway, andthen is distributed to extrastriate areas. From there the visualinformation reaches two critical cortical regions: the posteriorparietal cortex (particularly the lateral intraparietal region, LIP)and the dorsal frontal cortex (particularly the frontal eye field,FEF). From these two regions pathways descend to the superiorcolliculus (SC) on the roof of the midbrain. The SC in turn projectsto the midbrain and pontine reticular formation, which project tothe oculomotor nuclei that innervate each of the six eye muscles.Other descending pathways (including one from FEF through thebasal ganglia to SC) and a second visual input pathway (from retina

SuperiorColliculusMD

Thalamus

FrontalEye Field

MovementCommand

CorollaryDischarge

SensorimotorProcessing

VisualProcessing

MovementCommand

CorollaryDischarge

SensorimotorProcessing

VisualProcessing

LGNLGN

V1V1

SuperiorColliculus

Midbrain& Pons

Posterior ParietalCortex

FrontalCortex

Fig. 5. Brain circuits for visually guided saccades (A) and saccade based corollarydischarge (CD, B). See text for description.


to SC superficial layers and then through pulvinar to visual cortex)are not shown, nor are the pathways through the cerebellum. Thepoint, however, is that while this is just a sketch of our admittedlyincomplete knowledge of these pathways, it is complete enough tounderstand the type of signal conveyed by neurons at multiple lev-els within the brain.

Which brings us to the second question: locating a CD thatbranches off from this descending motor pathway. For a saccadicCD, we obviously look for neurons whose discharge is correlatedwith saccade generation and this activity is found first in cortex(FEF and to some extent LIP), then prominently in the intermediatelayers of the SC, and then in the pontine and midbrain areas towhich it projects. One pathway that is particularly intriguing(Fig. 5B, right) extends from the intermediate SC layers to the med-ial dorsal nucleus (MD) of the thalamus to the FEF (Lynch, Hoover,et al., 1994). Saccadic information in these SC layers is still orga-nized in a retinotopic map so that the saccade related informationfrom SC would be in the same coordinate system as the target ofthe pathway, the FEF. To more specifically relate this pathway toa CD function, the outline of a CD circuit is indicated on the leftin Fig. 5B. The sensorimotor area in which the CD originates wouldbe the SC, the visual processing area would be the FEF, and the con-nection between them would be the SC–MD–FEF pathway.

The issue is whether this pathway actually conveys a CD signal.In contrast to invertebrates, where transmission of a CD can be re-lated to a specific neuron type (Poulet & Hedwig, 2006), the CD inthe primate is embedded in a complex of pathways. In addition, ifwe isolate a neuron in a putative CD pathway, how do we know itcarries a CD signal or is just part of a loop in the movement gener-ation circuit? To address this problem, Sommer and Wurtz (2002)relied upon previous experience in studying CD particularly ininvertebrates and identified four criteria that they argued wouldqualify the candidate neurons as those carrying a CD. These points

have been discussed in detail in a recent review by Sommer andWurtz (2008), and only the conclusions need be stated here. Theypointed out that the neurons in the MD relay in the pathway tocortex had the characteristics expected of CD neurons in that theydischarged before saccades and only before saccades of givenamplitude and direction, reflecting their SC origins. The MD neu-rons were not in the pathway that led to saccades because inacti-vation did not disrupt either visually or memory guided saccades.But MD inactivation did disrupt the monkey’s ability to do a doublestep saccade task that requires a CD for its performance (Hallett &Lightstone, 1976). Thus the neuronal activity in the SC–MD–FEFpathway did meet the criteria for CD for saccades (Sommer &Wurtz, 2008). But as has already been discussed, a CD could be re-lated to control of movement and not be used for perception. Thenext question is whether this CD contributes to shifting RFs andpossibly to the stability of perception.

4.4. Does the CD to cortex drive the shifting RFs?

We now have identified two factors that might contribute to vi-sual stability. The first is the shifting RFs that could contribute toremapping of the visual field with each saccade and that dependupon a CD to do so. The second is a CD signal that reaches theFEF as just described. Does the identified CD fit the requirementsof the shifting RFs?

To answer this question it was necessary to establish that shift-ing RFs have the characteristics we would expect if the shifts re-sulted from the CD in the SC–MD–FEF pathway and then to see ifthe CD is necessary to drive shifts.

4.4.1. Is the CD appropriate for driving RF shifts?First, do the shifting RFs have the expected spatial configura-

tion? Neuronal CD activity in MD (as in SC activity) indicates thevector of the upcoming saccade: the discharge increases beforesaccades of given amplitude and direction. Therefore we would ex-pect the RF shifts in FEF to act as if they resulted from such a vectorinput: they should jump from one location to another (Fig. 6A top)rather than just expand and then contract around the FF. If therewere such a slide or expansion, there would be activity betweenthe RF and the FF whereas with the jump there would not be. Therewas no indication of activity between the RF and the FF (Fig. 6Abottom) and thus no indication of a slide (Sommer & Wurtz,2006). The shift behaves spatially as if it received input from theCD vector that jumps the activity from the RF to the FF.

The second expected characteristic is a temporal one: is thetime of the RF shifts consistent with the timing of the CD? TheCD activity in MD is synchronized with saccade onset (Sommer &Wurtz, 2004) and if this CD is driving the shift of activity in FF, thisshift should also be synchronized with the saccade onset. The in-crease in the activity with the shift for the example neuron inFig. 6B top shows a highly significant correlation with saccade on-set (p < 0.01, Sommer & Wurtz, 2006), as expected if the CD drivesthe shift. For the same reason, the increased activity with the shiftshould not be at the latency of the neuron’s visual response. Toshow this, the results for the same example neuron are alignedon the visual probe rather than the saccade in Fig. 6B bottom.The visual latency to a stimulus flashed in the RF of the neuronwas 80 ms (black arrow) which occurs long before the activityassociated with the shift (bold orange trace of average firing rate).Therefore the shift is synchronized with the saccade, and it is moreappropriate to refer to it as visual activity (it requires a visual stim-ulus) rather than as a visual response (it has no brisk onset or fixedlatency).

The range of onset times for FF activity extended from about100 ms before the saccade to about 200 ms after it, with a meanonset at 24 ms after the saccade had started (Sommer & Wurtz,

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Fig. 7. Necessity of CD input from MD thalamus for shifting RFs in FEF. (A) Exampleof a shifting RF impaired by MD inactivation. During inactivation (orange traces) theactivity in the future field decreased by 78%. (B) The deficit in the population ofneurons. Reductions in activity were seen only in the FF, not the RF, and only forcontralateral, not ipsilateral, saccades. **Significant changes at p < 0.0001 level. Fr-om Sommer and Wurtz (2006).

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Fig. 6. The spatial (A) and temporal (B) characteristics for shifting RFs are consis-tent with an input from the CD passing through MD thalamus. (A) The shifting RFswould be expected to jump from the RF to the FF with no significant change inactivity at the midpoint if the shift resulted from the vector input of a CD. Anexample FEF neuron shows this lack of midpoint activity consistent with the shiftbeing driven by a CD. From Sommer and Wurtz (2008). (B) The timing of the shiftingRF should be synchronized with the saccade as is the CD. In the upper record theactivity of an example FEF neuron aligned on saccade onset shows that the incre-ased activity with the shift is synchronized with saccade initiation. In the lowerrecord, the same neuronal responses are aligned on visual probe onset, and showthat the increase in activity with the shift occurs long after the visual latency (blackarrow). The green dots show the time of saccade onset in each trial. From Sommerand Wurtz (2006).


2006). The mean onset time of the CD activity in MD was 72 ms be-fore the saccade. The mean onset time of the CD activity in MD pre-ceded the mean for shifting activity in FEF by 96 ms so that the CDis early enough to drive the shifts. Such a long delay between theCD and the shift indicates that the shift is not the action at a singleor even only a few synapses, but must instead result from activityin a multisynaptic network which remains to be explored.

With the timing of the shifts now specified, it is worth clarifyingthe assertion that the shifting RF activity provides an ‘‘anticipa-tory” signal before the saccade. If the mean time of the shift is24 ms after the saccade has started for FEF neurons, and the rangeof shift times extends into the period after most saccades haveended, is it appropriate to refer to the shifts as being anticipatory?No, if anticipatory refers to the onset saccade. Yes, if it refers to thetime of the reafferent visual input produced by the saccade reachesthe FEF neuron. After a stimulus falls on the RF as a result of thesaccade, there is a visual latency for the response in the neuron.So even if the shifting RF activity occurs after the saccade it willstill activate the neuron before the reafferent visual stimulation

in most cases. So the shift is anticipatory because its visual activitystill occurs before the visual response generated as a result of thesaccade. Of course regardless of the time at which the visual activ-ity occurs, the flash that generates the activity is always before thesaccade.

4.4.2. Is the CD necessary for driving RF shifts?While the shifting RFs in FEF have spatial and temporal charac-

teristics consistent with input from the identified CD, this onlydemonstrates a correlation between the shifting RFs and the CD.The critical question is whether the CD is necessary to producethe shift. Inactivation of the region of identified relay neurons inMD, while measuring the shifting RFs in an FEF neuron, makes itpossible to test this necessity. Fig. 7A shows an example of oneof these experiments (Sommer & Wurtz, 2006). Black traces inFig. 7A show activity before inactivation; orange traces are activityafter inactivation. The neuron had a strong visual response in theRF during fixation (left upper panel) and a strong shift to the FF justbefore the saccade (right lower panel). During inactivation, the FFresponse was greatly reduced. The response in the RF response

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Fig. 8. Saccadic mislocalization (A) and a possible correlate in shifting RFs (B). (A)Mislocalization of the position of a bar briefly presented around the time of a ho-rizontal saccade from �10� to +10� (black stepped line-0 refers to screen center).The apparent position judged by the subject (ordinate) is plotted against the displaytimes relative to the onset of a saccade (abscissa). The bar was presented at one ofthree positions on the screen (�20�, 0�, 20�, indicated by the arrows). The result wasthat subjects systematically mislocated the bar. Bars presented at �20� or 0� weremislocalized in the direction of the saccade at about the same time as the onset of asaccade. Bars presented at +20� were mislocated in the opposite direction (againstthe direction of the saccade). The combination produced an effective compressionof visual space. Adapted, with permission, from Ross et al. (2001). (B) Spread in shiftonset times given by four example FEF neurons. The orange trace is from the neuronin Fig. 6B. Shift magnitudes are normalized to each other for comparison of timing.From Sommer and Wurtz (2008).


was unchanged showing that the neuron still had its sensitivity tovisual stimuli. The monkey also could still make the saccade to thetarget confirming that the MD inactivation did not block saccadegeneration. But the connection between the FEF visual processingand the CD was impaired because now the FEF neuron lost muchof its advance information about the impending saccade. This inturn led to the impaired RF shift. The deficit was present in 7 ofthe 8 neurons in which the experiment was completed, and washighly significant in the pooled results (Fig. 7B) with the shift re-duced by on average about 50%. The activity of the MD neuronswas related to saccades to the contralateral visual field, and sotoo was the deficit in the shifting RFs; the deficit was related tocontralateral saccades leaving ipsilateral saccades unimpaired.The combination of these correlation and inactivation experimentsprovides firm evidence that the identified CD from the SC is criticalfor RF shifts in FEF neurons.

The working assumption is that the functions of a CD inputestablished for FEF also apply to the shifting receptive fields foundin LIP (Colby & Goldberg, 1999) and even in earlier cortical areas(Nakamura & Colby, 2002). One possibility is that there are addi-tional pathways conveying a CD directly to parietal cortex but atthis point none has been identified. Another possibility is thatthe CD reaches parietal cortex transcortically via the extensivefunctional projections between the two structures (Chafee & Gold-man-Rakic, 1998; Chafee & Goldman-Rakic, 2000). One clue as towhether there is a direct CD to parietal cortex or an input throughFEF might be obtained by a detailed comparison of the shifts in thetwo areas but that has not yet been done. Such a comparison mightalso provide insight into the relative roles of frontal and parietalcortex in visual stability.

What must be true for both frontal and parietal neurons withshifting RFs is that they do not receive input from just one localizedregion of the retinotopic map as do neurons in the early visualareas. Because the FEF neurons responded to visual stimuli in boththe RF and the FF, these neurons must have connections to boththose retinotopic areas. Since a saccade can be made to any regionof the visual field, the FF can fall in any part of the field, and so theneuron must be connected to every part of the retinotopic map.This requires a tremendous increase in the connections to eachof the shifting RF neurons, and a model simulation by Quaia, Opt-ican, and Goldberg (1998) shows how these multiple connectionscould be changed at the time of the saccade.

4.5. Temporal distribution of shifts: Saccadic compression

Stimuli presented at the time of the saccade are mislocalized,and this may be related to the underlying mechanism of shiftingreceptive fields. Matin and his collaborators (Matin, Matin, &Pearce, 1969; Matin, Matin, & Pola, 1970; Matin & Pearce, 1965)flashed spots of light just before a saccade and found that the stim-uli were mislocalized. A substantial number of subsequent experi-ments have verified this (Morrone, Ross, & Burr, 1997; Ross,Morrone, & Burr, 1997), and also have demonstrated mislocaliza-tion of a flash after the saccade. As illustrated in Fig. 8A, the mislo-calization is in the direction of the saccade or opposite to thedirection depending on flash location and timing. This has been de-scribed as a compression of the visual field at the time of thesaccade.

Ross, Morrone, Goldberg, and Burr (2001) suggested that thiscompression might be related to relative activity in the RF andthe FF of the shifting neurons. For example, for the FEF neuron inFig. 4, the activity declined in the RF field as it increased in theFF, and this was the case in 1/3 of the neurons, with the remaining2/3 showing continuing activity in the RF as the activity developedin the FF. LIP also has a mixture of shifting RF types (Colby & Gold-berg, 1999; Colby et al., 1996; Kusunoki & Goldberg, 2003). Neu-

rons with activities in both the RF and FF might effectivelyindicate that a flashed stimulus fell between the RF and FF loca-tions, which would put the implied location closer to the saccadeendpoint than it actually was, and this could lead to the apparentcompression. A second source of the compression might be relatedto the timing of the shift in different neurons. Recall that in the FEFexperiments a brief flash (as in Fig. 4) led to increased activity inthe FF. The time at which the shift became evident, however, var-ied from neuron to neuron as illustrated for four FEF neurons inFig. 8B. The distribution of the shift onset times across the sampleof FEF neurons ranged from about 100 ms before to 200 ms afterthe saccade onset (Sommer & Wurtz, 2008). This distribution pro-longs the period over which the shifting occurs, and it may be inpart this prolongation of the updating that contributes to themislocalization of brief flashes occurring while the process is stillunderway.

More generally, the long time course over which the shiftingof the RFs occurs implies that any consequent updating of a


retinotopic map also might be spread over time. If so, this longtime for shifting completion might underlie the behaviorally basedconclusion that the shift in visual stability is a sluggish system assummarized in a recent critique by Bridgeman (2007). By this logic,the mislocalization at the time of the saccade is a flaw in thesystem rather than a feature. Such a slow updating might be toler-ated by the system because there is no necessity for a temporallyperfect shift; the flaws are covered up by the suppression consid-ered later (Matin et al., 1969).

4.6. Conclusion: Shifting fields for updating a retinotopic map

Shifting RFs could provide the neuronal basis for visual stabilityin the presence of saccades: they provide a potential link betweenthe concept of updating a retinotopic map with each saccade andthe CD that would be necessary to accomplish that updating. Wemight at this point say that we have three legs of a four leggedstool supporting the retinotopic hypothesis of visual stability.The first leg is the demonstration that neurons in FEF, LIP and otherareas show shifting receptive fields that could contribute to updat-ing or remapping of the visual field with each saccade. The secondleg is the identification of a CD from the SC–MD–FEF pathway thatreaches these neurons. The third leg is the demonstration that theCD is necessary for the shift to occur in FEF. Before we try to sup-port a hypothesis of visual stability on this stool, we need a fourthleg: we need to demonstrate that the shifting RFs actually underlieperceptual stability. Up to this point such a demonstration hasbeen largely beyond testing even in monkeys because any inactiva-tion at the site of the shifting RFs either in FEF or LIP would disruptthe visual processing as well as the shifting RF mechanisms. Withthe identification of the MD relay in the CD pathway, however, itshould be possible to inactivate MD, reduce the CD to cortex, andreduce the FEF shift. With the shift reduced, the perception of sta-bility should be reduced. The challenge then becomes one of show-ing that a monkey with reduced shifts has reduced ability todistinguish object displacement due its own movement from thatin the environment. A successful experiment would provide the fi-nal leg of the visual stability stool by relating an internal input (CD)to the modulation of visual processing (shifting RFs) to the percep-tion of visual stability with saccades.

5. Displacement: Transsaccadic memory and attention

The function of CD was put into a different light by MacKay(1972) who argued that a CD should be regarded as a questionasked as a movement is generated. The answer is given by the vi-sual input resulting from the movement, and it is evaluated in lightof the question. He hypothesized that the world is assumed to bestable unless the answer with a given movement gave evidenceto the contrary. One way of looking at the neuronal shifting recep-tive fields illustrated in Fig. 3 is that they provide that mechanism:the CD-generated future field (FF) is the question and the visual re-sponse in the new RF after the saccade is the answer. Prophetically,MacKay also expected to find such activity at a point where visualand movement activity were both represented as is the case infrontal and parietal cortex. Mackay’s approach might also be re-garded as a forerunner of the optimal inference approach basedon Bayes’ theorem that has been used to explain visual perceptionat the time of saccades (Binda, Bruno, Burr, & Morrone, 2007; Nie-meier, Crawford, & Tweed, 2003).

5.1. Transsaccadic memory

A recent hypothesis uses the assumption of stability across sac-cades to explain the perception of visual stability, and implementsthe idea by using transsaccadic memory to determine whether the

assumption is correct. Deubel and his collaborators (Deubel, 2004;Deubel, Bridgeman, & Schneider, 2004; Deubel, Schneider, & Bridg-eman, 2002) proposed the following steps. First, the features of thesaccadic target and of objects immediately surrounding the targetare stored in memory. This transsaccadic memory serves as the ref-erence for determining whether the target object and its surroundafter the saccade are the same as before the saccade. After the sac-cade, if the objects around what is now the fixation point matchthose in memory, the assumption of a stable world is correct. Ifthe match fails, the assumption of visual stability is abandoned,and it is assumed the target moved.

A key observation of Deubel et al. (Deubel, Bridgeman, &Schneider, 1998; Deubel, Schneider, & Bridgeman, 1996) providedthe impetus for this hypothesis. After verifying that even relativelylarge displacements of the saccade target made during the saccadewere not detected (the suppression of displacement consideredpreviously, Bridgeman et al., 1975), they were able to make thesedisplacements obvious with a simple manipulation. If the dis-placed target was blanked out and not restored until at least50 ms after the end of the saccade, the displacement was easily de-tected. When target blanking was entirely within the saccade, dis-placement was not detected. There is something special about thepresence of the target immediately after the saccade which hadbeen emphasized previously (Wolf, Hauske, & Lupp, 1980). Thisled to the transsaccadic hypothesis that makes the fundamentalassumption that if the target remains in the same position beforeand after the saccade, it and the visual world are stable. Thisassumption is rejected by the total absence of the target right afterthe saccade as in this experiment and with large displacementsbrought about by real world displacements during the saccade.

A specific neuronal basis for this transsaccadic memory hypoth-esis is lacking, but two neuronal observations are relevant. The firstis derived from an area that is probably on the pathway to objectvision, V4. Moore, Tolias, and Schiller (1998) showed that the vi-sual response of V4 neurons to an optimally oriented stimuluswas enhanced just before a saccade was made to the RF of the neu-ron. It was not enhanced when the saccade was not to the RF. Theysuggested that the enhanced activity just before the saccade pro-vided reactivation of the response to the visual stimulus beforethe saccade. This reactivation would facilitate comparison to thepost-saccadic stimulus, and this is what is needed for the trans-saccadic hypothesis.

A second neuronal finding relevant to the transsaccadic mem-ory hypothesis is the activity related to the shifting RFs alreadyconsidered in detail above. The activity at the future field couldbe regarded as representing a transsaccadic memory. As shownconceptually in Fig. 3, the activity at the FF indicates the stimulusfalling there before the saccade which can then be compared towhat falls on the RF after the saccade. This appears to be exactlythe mechanism required for the transsaccadic memory. Theseshifting RF neurons, however, are not specifically coding for objectsas required by the transsaccadic hypothesis, but if the object mem-ory could be conveyed by the retinotopic based RFs of frontal orparietal neurons, these neurons could provide the required trans-saccadic memory. Alternatively, the same shifting field mechanismmight be present in cortical areas devoted to object vision.

5.2. Attention restricts the displacement problem

A critical point of the transsaccadic memory hypothesis is that itis only the region close to the saccade target (the future fixationpoint) for which a transsaccadic memory is relevant; the comparisonis made for objects only at or near this point. The rationale for thisrestriction results from a series of experiments showing increasedefficiency of visual processing for visual stimuli located around thetarget of the upcoming saccade (Deubel & Schneider, 1996; Hoffman


& Subramaniam, 1995; Kowler, Anderson, Dosher, & Blaser, 1995).For example, discrimination of one letter among a cluster of lettersis best when that letter is the target of the saccade (Deubel & Schnei-der, 1996). Furthermore in these experiments, it was not possible todirect attention to one location and make a saccade to an adjacentlocation, which was taken as an indication of the close coupling be-tween this spatial attention and saccades. In the transsaccadic mem-ory hypothesis, therefore, only the objects close to the saccade targetare selected for memory across the saccade.

More generally, the coupling of visual spatial attention and sac-cades has implications for any hypothesis that incorporates updat-ing of a retinotopic map. Each time a saccade occurs there is anaccompanying shift of visual attention as indicated by the saccadeand attention experiments just recounted. The importance ofattention for limiting perception to selected locations is furtheremphasized by the phenomenon referred to as change blindnessor inattentional blindness (for reviews see Mack & Rock, 1998;Rensink, 2002; Rensink, O’Regan & Clark, 1997; Simons, 2000),and comparable effects have been demonstrated in monkeys (Cav-anaugh & Wurtz, 2004). In a change blindness experiment, a sub-stantial change in the visual scene is not reported by an observerwhen the sudden onset transient associated with the change iseliminated. Changes occurring in the visual scene during saccadiceye movements also go unnoticed (O’Regan and Noe, 2001). Butif the observer’s attention is directed to the region of the visualfield with the change, the change is seen instantly. The implicationof these experiments is that we probably do not maintain a percep-tual image or memory of the entire visual scene but only that partto which we pay attention. The consequence of this for a retinop-ically based hypothesis for visual stability is that it need not ac-count for a remapping of the whole visual field but just that partof the field to which attention is directed at the time of the saccade.In fact in the experiments described on shifting fields, attentionmay have a particularly salient role because the experiment isdone with flashing lights that attract attention simply by their on-set. If there is no such attention, LIP neurons show no RF shift(Gottlieb, Kusunoki, & Goldberg, 1998). The shifting RFs may onlybe required in the region to which attention is directed, but the ex-tent to which this is true is unknown.

5.3. Conclusion: Transsaccadic memory and updated retinotopic maps

The simplifying assumption that there is stability across sac-cades unless there is evidence to the contrary (MacKay, 1972)has been applied to a hypothesis using object matching across sac-cades to verify or reject that assumption (Deubel et al., 2002).

An intriguing feature of this transsaccadic memory hypothesisis that the neuronal mechanism required for the memory is con-ceptually similar to that considered for updating a retinotopicmap. The activity in the future field (FF) before the saccade is avail-able for comparison to the RF after the saccade. In the remappinghypothesis, the FF activity is used to update a retinotopic map;in the transsaccadic hypothesis the FF activity is used to test thematch to the RF after the saccade. At the neuronal level thesetwo hypotheses would be difficult to distinguish. Both might alsoapply primarily to the region around the saccade target becausethere is substantial evidence that only those regions attended toat the time of the saccade are relevant to perception. The shiftsare still retinotopic, but the retinotopic area is not the full fieldbut just the limited area to which attention is directed.

6. Displacement: Spatiotopic maps

A logically attractive hypothesis is that by the time visual inputreaches the brain regions related to visual perception, the repre-sentation of the visual world is not in the retinotopic coordinates

of the eye, but rather in coordinates of visual space. That is, visualperception is based on a spatiotopic map that supersedes the reti-notopic map. As the eye moves, the information with each fixationis incorporated into this higher order spatial map. This hypothesisis appealing because it fits with our personal visual experience: thespatial map is what we are aware of, not the series of snapshots de-picted in Fig. 1. At the neuronal level this hypothesis predicts that aspatiotopic visual map should be found at some point in the visualsystem.

The distinguishing feature of a neuron lying in a spatial map isthat as the eye moves the RF of the neuron remains activated by astimulus that remains at one point in the visual field. Neurons onthe spatiotopic map are related to different points in space and ta-ken together form a map of space. (For simplicity I refer to eyemovements, but head and body movement have the same require-ments). At this point no spatiotopic map has been identified in themonkey brain. Neurons have been identified, however, that re-spond to a visual stimulus but have a response modulated or gatedby eye position. The hypothesis is that these neurons form the in-put to a map or are themselves part of a distributed map that cannot be identified at the single neuron level.

6.1. Gain fields and real position neurons

Neurons in area V1 fall into a clearly delineated retinotopic mapand neither large saccades (Bridgeman, 1973) nor micro-saccades(Gur & Snodderly, 1987, 1997) disrupt that spatial map (for inter-pretive review see Bridgeman, 1999).

In striking contrast, clear modulation of the visual response byeye position was first reported for neurons in posterior parietalcortex by Andersen and Mountcastle (1983). The magnitude ofthe visual response changed systematically with eye position(Fig. 9A). These neurons were still retinopically organized, butthe gain of their visual response was modulated up or down asthe eye was directed to different regions of the visual field. Subse-quent experiments (Andersen, Essick, & Siegel, 1985) have pro-vided further information on these gain fields (for a review seeAndersen, 1989).

The basic mapping in other extrastriate areas also appears to belargely retinotopic with a major change being the progressive in-crease in RF size in successive visual areas which provides a possi-ble mechanism for increased space constancy (Kjaer, Gawne, Hertz,& Richmond, 1997; Salinas & Abbott, 1997). But extrastriate areasalso show modulation of visual responses as demonstrated by Gal-letti and Battaglini (1989); nearly half of the neurons in V3A aremodulated by eye position. Such modulation subsequently hasbeen found in a number of areas along the dorsal visual pathway(for a summary see Galletti & Fattori, 2002) as well as in FEF(Cassanello & Ferrera, 2007), supplementary eye field (Schlag,Schlag-Rey, & Pigarev, 1992), and dorsolateral prefrontal cortex(Funahashi & Takeda, 2002).

It has been suggested that these gain field neurons might them-selves represent a distributed spatiotopic map that is not revealedby the activity of any individual neuron (Andersen et al., 1985; Gal-letti & Battaglini, 1989). Several models have shown how spatialinformation could be represented if the gain field neurons wereenvisioned as one of the steps in producing a spatiotopic map (Gal-letti & Fattori, 2002; Zipser & Andersen, 1988). For example, in thenetwork model of Zipser and Andersen (1988), ‘‘neurons” in themiddle layer were found to have gain fields similar to those of pari-etal neurons. This of course does not demonstrate the presence of aspatiotopic map, but it does show that such information in a dis-tributed map is conceptually possible.

Other neurons have been identified that do respond to stimuliin one region of visual space rather than one point on the retina.These spatiotopic ‘‘real position” neurons were first found in

Fig. 9. Possible inputs to a spatial map. (A) An example gain field neuron from posterior parietal cortex. On the left drawing of the screen in front of the monkey, when themonkey looked at the central fixation point (o), the RF was mapped out and was found to be in the lower right quadrant (dashed circle). On the right, the response of theneuron aligned on stimulus onset is shown for fixation at the center of the screen by the record at 0, 0. Then the monkey fixated at one of the other eight positions on thescreen (left drawing) each separated by 20�. At each fixation position the stimulus was moved so that it fell on the RF. Even though the stimulus fell on the same retinotopicposition, the gain of the visual response changed systematically as the monkey’s eye position changed. These responses are shown on the right. The strongest response waswith fixation in the upper left, the weakest with fixation in the lower right. Modified from Andersen et al. (1985). (B) An example real position neuron from area V6A. Thestimulus was always in the lower right quadrant (dashed line), and +s indicate the five fixation points on an 80� wide screen. The visual response was nearly the sameregardless of the fixation point. Modified from Galletti and Fattori (2002).


parietal cortex (Galletti, Battaglini, & Fattori, 1993), and Fig. 9Bshows an example; the response of the neuron remains strongwhen the visual stimulus remains in one part of the field evenwhen fixation is moved to different points in the visual field.Neurons that ranged from retinotopic to clearly spatiotopic havebeen found in V6A (Galletti et al., 1993) and in the ventral intrapa-rietal area (Duhamel, Bremmer, BenHamed, & Graf, 1997), and ingeneral real position neurons have been found in areas that overlapthose where the gain field neurons are found (Galletti & Fattori,2002). Thus, these real position neurons directly represent a loca-tion in visual space, and a map built up of these real position neu-rons could represent visual space. Furthermore, multiple gain fieldneurons could provide the input necessary to produce real positionneurons as proposed by Galletti, Battaglini, and Fattori (1995).

While there is not enough evidence to say that these real spaceneurons form a spatiotopic map, they have characteristics that areprobably sufficient for them to represent elements of such a mapwhich in turn could be the basis of our perception of visual stabil-ity. There is also the possibility that these neurons (as is also the

case for those with shifting RFs) are unrelated to visual stabilitybut instead are part of the transformation leading to movement.For example some neurons in posterior parietal cortex are activebefore saccades while others are active before reaching (Snyder,Batista, & Andersen, 1997) suggesting a dedication to movementrather than general visual processing. Similarly the gain field neu-rons in several regions of parietal cortex could contribute to thecoordinate conversions preceding the necessary coordination ofeye and hand movements (Andersen, Snyder, Bradley, & Xing,1997; Galletti, Kutz, Gamberini, Breveglieri, & Fattori, 2003; Sny-der, Grieve, Brotchie, & Andersen, 1998) rather than producingthe spatiotopic reference necessary for visual stability.

6.2. Conclusion: Updating maps

Recording neurons in the monkey brain during saccades hasprovided neuronal evidence for the updating of either retinotopicor spatiotopic maps as the mechanism underlying stable visualperception. In the retinotopic hypothesis, the visual world remains


represented in a retinotopic map centered on the fovea. With eachsaccade, there is a brief transition period in which the map is up-dated by anticipatory activity in the visual field area where the fu-ture receptive field will be located. After the saccade the map isstill a retinotopic one. In the spatiotopic hypothesis, there is a spa-tially based map of the visual world that is updated with each sac-cade. Or alternatively, in one version of the spatiotopic hypothesis,positions are calculated anew with each new fixation (a calibrationhypothesis, Bridgeman et al., 1994). In either case both before andafter the saccade the map is in spatial coordinates. In spite of thesedifferences between the retinotopic and spatiotopic hypotheses,there are a few striking similarities in their neuronal requirements.Both require a mechanism for updating a map with each saccade.The mechanisms of the updating might be different for the twotypes of maps, but both require it. Furthermore, both require vastlyincreased connections over the simple one to one connection for aretinotopic map. Because both types of map require an updatingwith each saccade, and this updating can come from any part ofa retinotopic map, neurons in both maps must have connectionsto all parts of the entire retinotopic map. How this could be accom-plished has been specified by several models and hypotheses (Gal-letti et al., 1995; Quaia et al., 1998; Salinas & Sejnowski, 2001;Trehub, 1991).

I do not think that the current evidence for the two hypothe-ses is equal but rather that there are two reasons to favor theretinotopic hypothesis. The first is that the neuronal evidencefor the contribution of the shifting RFs to updating a retinotopicmap has become substantial and coherent. The studies on shiftingRFs have established a possible mechanism for shifting the visualsensitivity on the retinotopic map, and the CD required for driv-ing such a shift has been identified. This detailed knowledge inturn allows a test of the relation of the shifts to the perceptionof visual stability. In contrast, a spatiotopic map, distributed ornot, has yet to be identified, the signal that contributes the eyeposition signal is not established, and a test is not obvious. Sec-ond, at a behavioral level, there is growing evidence from exper-iments on change blindness that there may be no spatial map inthe brain, but rather a transient retinotopic map with each newfixation. If there were a spatiotopic map independent of the cur-rent retinal image, why are such changes missed? The spatiotopicmap should be representing the whole field all of the time. Incontrast, if there were a retinotopic map that changes with eachsaccade, such omissions are readily understandable. In net, theevidence from change blindness argues against a spatial map,an argument that is independent of the issue of visual stability.Future evidence, particularly at the neuronal level, may changethis conclusion on the preeminence of updated retinotopic mapsfor visual stability, but for now these maps are the core of aworking hypothesis—with emphasis on working.

7. Saccadic suppression

Saccades move the eye rapidly with peak speeds of about 500�/sfor a 20� saccade in humans (Westheimer, 1954) and substantiallyfaster (800�/s) in monkeys (Fuchs, 1967). This high speed of thesaccade sweeps the image of the visual scene across the retina pro-ducing a blur. Yet we are usually unaware of this blur. This lack ofvision during saccades is referred to as saccadic suppression or, toemphasize the lack of awareness of sweep, as saccadic omission(Campbell & Wurtz, 1978). There is also a more specific suppres-sion of motion detection (Burr, Holt, Johnstone, & Ross, 1982)and displacement detection (Bridgeman et al., 1975). Anyonewho has looked at an amateur home video appreciates how criticalit is to eliminate these disturbing interruptions, be the recordingdevice a camera or the eye.

The first reports of suppression were from the eminently prac-tical experiments of Erdman and Dodge in 1898 who found thatduring reading, letters presented during saccades were not seenand that all reading occurred during the fixations between sac-cades (for a concise summary and references for this early historysee Volkmann, 1986). The conclusion was that we are functionallyblind during saccades, but there was no consensus on the source.Holt argued that during saccades the visual input was ‘‘blankedout” producing a ‘‘central anesthesia”. In contrast, Dodge believedthe lack of vision was due to both a central factor and to the inter-action of the clear images outside the saccade with the blurredimages during it. Interest in these turn of the century issues re-vived with the ability to accurately record saccades in the 1960s,and these experiments are summarized in excellent reviews(Bridgeman, 1986; Matin, 1974; Volkmann, 1986).

A half century of experimentation has established that there aretwo sources of saccadic suppression: an extraretinal CD and a vi-sual masking mechanism. While there is strong behavioral andneuronal evidence for both mechanisms, it seems likely that innormal high contrast environments visual masking is the dominantmechanism with the contribution of the CD being more modest.

8. Suppression by CD

8.1. Behavioral evidence

When saccades are made across normal visual scenes, the speedof the eye movement usually produces a brief blurred image, and itwas natural to assume that nothing was needed to account for thesuppression of such minimal stimulation. Establishing a role for anextraretinal input for suppression was the first success of quantita-tive measurements of saccadic suppression in the 1960’s. In theseexperiments blur was eliminated by using flashed stimuli duringsaccades made in the dark or against a uniform background. Detec-tion during saccades required flashes about three times as bright asthose during fixation (Volkmann, 1962). This was a threshold ele-vation of about 0.5 log units which was small compared to thebrightness of stimuli that might be experienced during a saccadegiven the many log unit sensitivity range of the visual system.The use of a brief flash also revealed that the suppression beganas long as 50 ms before the saccade (Latour, 1962). These two earlyobservations on threshold and timing showed that the suppressionresulted from an extraretinal signal which had to be a CD becauseits effect preceded any proprioceptive input from eye musclecontraction.

Detection of motion is also suppressed during saccades as indi-cated by the observation that a drifting grating moved suddenly re-quired a larger movement during a saccade than during fixation tobe detected (Burr et al., 1982). A larger change in motion of randomdot patterns also was required for detection during a saccade thanduring fixation (Bridgeman et al., 1975). We have already notedthat target displacement during a saccade is suppressed (Bridg-eman et al., 1975), and Shioiri and Cavanagh (1989) showed thatmotion detection occurred without any displacement by using mo-tion of random dot patterns that had no displacement. This reduc-tion in motion sensitivity is specific for saccades; Burr and Ross(1982) showed that during fixation there was no lack of sensitivityto high speed motion. As motion speed increased, the direction ofthe motion was simply discriminated at lower and lower spatialfrequencies.

One of the most striking changes during saccades is the selec-tive reduction of sensitivity to low spatial frequencies (Burr et al.,1982; Volkmann, Riggs, White, & Moore, 1978). In these experi-ments, horizontal saccades were made over horizontal gratingsso that blur was minimal, but reduced visibility of the lower spatialfrequencies persisted. This makes good functional sense because


the selective suppression of the lower spatial frequencies duringsaccades would take care of what the high speed of the retinal im-age had not eliminated. Burr, Morrone, and Ross (1994) showed inaddition that while saccades reduced the visibility of luminance-modulated gratings at low spatial frequencies, they did not reducethe perception of equiluminant color-modulated gratings at anyspatial frequency. They noted that the reduced sensitivity duringsaccades to motion, to low spatial frequencies, and specifically toluminance and not color dependent spatial frequencies were char-acteristics expected from a contribution of the magnocellular lay-ers of the lateral geniculate nucleus (LGN). They suggested thatthe saccadic suppression seen psychophysically could result fromsuppression of this segment of the LGN.

The identification of other factors contributing to suppressionare summarized by Volkmann (1986), but two other observationsin particular lend support to the conclusion that a fraction of sacc-adic suppression results from a CD. First, afterimages show sup-pression during saccades, and afterimages have the advantage ofno possible movement on the retina and no optical changes asso-ciated with a saccade. The suppression lasts longer with larger sac-cades (of consequently longer durations), but is evident even withthe saccades as small as 0.5 deg. (Kennard, Hartmann, Kraft, & Bos-hes, 1970). Second, suppression occurs during blinks which can ob-scure vision for up to 100–150 ms (longer than the 50 ms of mostsaccades), and the suppression has characteristics similar to thatduring saccades (Volkmann, 1986). The magnitude of suppressionto a full field flash is about 0.5 log unit threshold elevation (Volk-mann, Riggs, & Moore, 1980).

Thus, there is clearly a modest reduction in visual sensitivity(about 0.5 log unit) during saccades that results form a CD becauseit occurs in the absence of any possible visual interactions and be-gins before the saccade. There are also selective changes in sensi-tivity to motion, displacement, and low spatial frequency thatreflect the action of a CD. The combination of these sensitivitychanges are consistent with the LGN as the site of the saccadicsuppression.

8.2. Neuronal evidence

8.2.1. The LGN to visual cortex pathwayExtraretinal input to the LGN with eye movements has been

known since the discovery of pontine-geniculate-occipital(PGO) waves of rapid eye movement sleep (see for exampleBizzi, 1966). Multiple possible sources of such modulation havealso been identified (Singer, 1977). Whether these modulationscontribute to saccadic suppression has been studied more re-cently usually using full field visual stimulation and looking forchanges in LGN visual responses associated with saccades. Rep-pas, Usrey, and Reid (2002) found changes with saccades. Mag-nocellular LGN neurons showed the largest changes and thelargest proportion of neurons (90%) showing a change. The larg-est modulation, however, was not primarily a suppression, but abiphasic-small suppression and a later and larger enhancement.The suppression ends about 50 ms after saccade onset and re-duces the amplitude of the initial visual response. This shouldreduce at least the initial burst of visual input generated as a re-sult of the saccade. The cat LGN shows a similar suppression be-fore and facilitation after the saccade (Lee & Malpeli, 1998).Ramcharan, Gnadt, and Sherman (2001) in the monkey foundprimarily increased visual responses after the saccade also pri-marily in magnocellular neurons. Much earlier Buttner and Fuchs(1973) found little consistent modulation of response to full fieldstimuli with saccades and again most of what was found was anincrease of activity after the saccade. Other experiments havenot measured the suppression of specific visual input, but havelooked at the modulation of the background activity. Royal

et al. (Royal, Sary, Schall, & Casagrande, 2006) have summarizedprevious studies, and in their own studies have found reductionof background activity in all LGN layers beginning on averageover 100 ms before the saccade and extending about 50 ms afterthe saccade. If this background reduction was accompanied by asuppression of the visual response, it would last long enough toact on at least some of the visual input generated by a saccade.They also found that the most consistent and largest modulationwas an increase in background activity beginning about 100 msafter the saccade end. In net, while the more prominent modu-lations in several studies have been in the magnocellular layers,which is consistent with the expectations from psychophysicalexperiments (summarized by Ross, Burr, & Morrone, 1996), thesuppression of responses to visual stimulation have been bothshort in duration and limited in magnitude.

The neurons in primary visual cortex (V1) were the first to bechecked for suppression during saccades (Wurtz, 1968, 1969a,1969b)—indeed, it was the first question to be investigated in theawake monkey trained to fixate in order to provide controlled vi-sual stimulation to one area of the visual field. The response ofV1 to a light bar stimulus swept across the receptive field duringfixation was similar to that when the saccade swept the eye acrossthe same stationary stimulus. Similar qualitative experiments donesubsequently also generally did not observe suppression in V1(Fischer, Boch, & Bach, 1981) although a few neurons were re-ported to fail to respond during saccades (Battaglini, Galletti, Aicar-di, Squatrito, & Maioli, 1986, see summary in Galletti & Fattori,2003). The question of a central anesthesia was answered just asit had been answered by psychophysics: there is none. Subtlechanges in neuronal responses were not measured, so that changescomparable to the slight rise in threshold seen psychophysicallywould probably not have been detected.

Subsequent experiments on V1 quantified saccade related activ-ity that occurred during memory guided saccades but the changewas an increase not a suppression and it preceded saccades by100–200 ms rather than followed them (Super, van der Togt, Spe-kreijse, Lamme, & Zd, 2004). Background V1 neuronal activity ismodulated with spontaneous saccades in the dark, including somecases with suppression after the saccade (Kayama, Riso, Bartlett, &Doty, 1979), and there is ample evidence of subcortical input to V1(Doty & Ra, 1983). If this input led to suppression of the visual re-sponse, however, we would expect it to be substantial more fre-quently in the V1 visual responses.

While there seems to be little indication of a substantial sup-pressive mechanism in the LGN to V1 pathway, there is clear evi-dence of suppression in the extrastriate areas related to visualmotion, MT and MST. Thiele, Henning, Kubischik, and Hoffmann(2002) found that the directionally selective neurons in these areasdifferentiate between motion during fixation and during saccades.About two thirds of the neurons responded to stimuli moving atsaccadic velocities while the monkeys fixated but failed to respondwhen the monkey made saccades across the stationary stimulus(Fig. 10A). For some neurons, the preferred direction during sac-cades actually reversed and Thiele et al. suggested that this rever-sal might contribute to reducing any residual motion responsesgenerated by the saccade over a visual background. Ibbotson, Price,Crowder, Ono, and Mustari (2007) subsequently found that over80% of MT/MST neurons showed a reduced response to the motionproduced by saccades compared to the same motion duringfixation.

While neuronal correlates of pursuit eye movements have notbeen considered in this review, it is worth noting that as with sac-cades, during pursuit relatively few neurons in V1 have been foundthat show evidence of a CD (Dicke, Chakraborty, & Thier, 2008; Gal-letti, Squatrito, Battaglini, & Grazia Maioli, 1984; Ilg & Thier, 1996).In contrast, the fraction of neurons with such a CD input increases

Fig. 10. Saccadic suppression by CD. (A) Response of an MT neuron to a moving visual stimulus (lower record) but failure to do so during a saccadic eye movement (upperrecord). From Thiele et al. (2002). (B) Example SC superficial layer neuron that responds to a moving visual stimulus in front of the stationary eye but not during a saccade. Thevisual stimulus moved across the RF (left record) or was moved across the RF by a saccade (right record). Peak of ordinate is 250 sp/s; tick marks on the abscissa are 100 ms.From Robinson and Wurtz (1976). (C) An example SC superficial neuron demonstrated to have input from a corollary discharge. On the left and right is the suppression duringnormal saccades (in the light to maintain background discharge rate). In the center is the suppression that continues during retrobulbar block of both eyes. All of the recordsare triggered on the integrated burst of activity of the oculomotor nucleus (Oc. Nuc), that remained even when the EOG for horizontal and vertical components of the saccadewere eliminated by the block (center). Peak of ordinate is 20 sp/s; tick marks on the abscissa are 100 ms. From Richmond and Wurtz (1980).


substantially at the levels of MT, MST and posterior parietal cortex(Dicke et al., 2008; Erickson & Thier, 1991; Ilg, Schumann, & Thier,2004; Newsome, Wurtz, & Komatsu, 1988).

Given the limited suppression in LGN and V1, there is the pos-sibility that at least some of the suppression seen in MT results notfrom V1 input but from the now established pathway from SC topulvinar to MT. This would be consistent with the frequent failureto find suppression in V1 and success in finding it in areas anteriorto V1 (Fischer et al., 1981). A recent study determined the effect ofsaccades on phosphenes produced by transcranial magnetic stimu-

lation of occipital cortex and concluded that the suppression altersearly cortical visual processing (Thilo, Santoro, Walsh, & Blake-more, 2004). This would be consistent with the neuronal evidenceif the cortical stimulation affected primarily V2 rather than V1. Fi-nally an fMRI study in humans also showed correlates of suppres-sion at higher levels in the visual pathway, including the MTregion, but not at the level of V1 (Kleiser, Seitz, & Krekelberg,2004). It therefore becomes relevant to consider the modulationwith saccades in the other pathway to visual cortex, that leadingfrom SC to MT.


8.2.2. The SC–pulvinar–cortex pathwayThe major source of the visual input to cortex from the SC is via

the superficial layers, and in contrast to LGN and V1, neurons inthese layers show striking suppression with saccades. Of the SCneurons that responded to rapid stimulus motion, Robinson andWurtz (1976) found that roughly 2/3 failed to respond when thereceptive field was swept across a slit of light by a saccade(Fig. 10B). The SC neurons responded to all four orthogonal motiondirections during fixation, and saccades in all these directions pro-duced suppression. Suppression was effective for stimuli at leastone log unit above background for all neurons tested, and it lastedfrom saccade onset to about 125 ms after saccade end. Neuronsshowing a visual suppression during saccades frequently alsoshowed a suppression of background activity (Goldberg & Wurtz,1972; Robinson & Wurtz, 1976), and the duration of the two sup-pressions frequently matched. Thus the saccadic suppression of theSC neurons was robust, came at a time after the saccade when thevisual stimulation resulting from the saccade reached the neurons,and correlated with a suppression of the background activity.

One source for the suppression could simply be a response tothe visual background during the saccade, but the suppression oc-curred with saccades made in total darkness. This implied that anextraretinal signal was the source of the suppression, and becausethe neuronal suppression was after the saccade, this signal couldlogically be either proprioceptive input from the periphery or aCD generated internally. While there were a number of character-istics that suggested the source was not proprioception (Robinson& Wurtz, 1976), this possibility was tested explicitly by Richmondand Wurtz (1980) who reversibly paralyzed the eye muscles in or-der to eliminate muscle contraction and the resulting propriocep-tion (Fig. 10C). Eye movements were recorded to make certainthe eye did not move, and the monkey’s attempts to make saccadeswere monitored by recording the bursts of activity of extraocularmuscle motor neurons. The suppression of the background activitypersisted in spite of the lack of movement (10C, center), and be-cause the background suppression accompanied the visual stimu-lus suppression, it indicated the continued presence of theextraretinal signal in the absence of proprioception. The source ofthe neuronal suppression must have been a CD.

The source of the CD input remains unknown. Robinson andWurtz (1976) suggested that the source might be the FEF becauseneurons there discharge after saccades and with saccades in alldirections, and it had been suggested that these neurons mightrepresent a CD (Bizzi, 1968). Another source might be the saccaderelated neurons in the adjacent SC intermediate layers particularlybecause this connection has recently been demonstrated in the rat(Lee et al., 2007). The intermediate layer neurons connect only tosuperficial neurons directly above them so this connection wouldconvey activity for just the one saccadic direction represented inthe intermediate layers just below. To get the multidirectional sup-pression shown by the superficial layer neurons, other indirectconnections would be required. Regardless of the specific sourceof input, the neurons in the SC superficial layers show a strikingsuppression of the visual response, and the most likely source ofthis suppression is a corollary discharge.

The issue is whether this suppression of visual response in theSC during saccades contributes to visual perception. Since suppres-sion with saccades has been relatively minimal in LGN and V1compared to that in SC and MT, an intriguing possibility is thatthe perceptual suppression associated with saccades is derivedfrom the SC. The contribution of the SC suppression would be com-pelling if it were known that the SC neurons were selectively sen-sitive to low spatial frequencies and could thus provide theselectivity that Burr et al. (1994) envisioned for the LGN. Unfortu-nately the spatial frequency tuning for the SC visual neurons isunknown.

If SC superficial layer neurons are a potential source of percep-tual suppression during saccades, that suppression would probablyreach visual cortex via the projection from SC to the pulvinar nu-cleus of the thalamus. Robinson and collaborators (Robinson, McC-lurkin, Kertzman, & Petersen, 1991; Robinson & Petersen, 1985)showed that the suppression is clearly present in the pulvinar,and that it has properties similar to those seen in the superior col-liculus. Subsequently, Berman (2007) have identified relay neuronsin the pulvinar that convey visual information from SC to MT.These relay neurons are centered on the medial region of the infe-rior pulvinar (using the nomenclature of Stepniewska & Kaas,1997; Stepniewska, Ql, & Kaas, 2000). Some of these neuronsclearly showed the suppression of background activity during sac-cades (Berman and Wurtz, personal communication) so that thispathway now is known to provide an input to MT that is sup-pressed during saccades.

8.3. Conclusion: Finding a CD for saccadic suppression

Perception shows a suppression that results from a CD becauseit occurs in the absence of visual interactions and begins before thesaccade. The evidence that suppression begins in the magnocellu-lar layers of LGN and is conveyed to V1 cortex is limited. The neu-ronal suppression seems to be most prominent in visual areasbeyond V1, particularly in the motion areas, MT and MST. One ideaabout a possible added source of that suppression, though a novelone, is that it could be provided by the SC superficial layer neurons,which show a CD based suppression, and that could project up-ward via the pathway from SC through pulvinar to cortex. In thisscenario suppression may not be a function of the geniculocorticalpath but rather of a collicular cortical path. Regardless of this spec-ulation about pathway, neuronal correlates of saccadic suppressionthat probably depend on CD have been identified, and this fullyvalidates the psychophysical evidence for a CD based saccadicsuppression.

9. Suppression by visual masking

9.1. Behavioral evidence

A purely visual mechanism proposed to explain our lack ofawareness of the visual blur during a saccade is masking, the inter-action between stimuli presented one after the other. Forwardmasking refers to a masking stimulus blocking perception of a latertest stimulus, and backward masking refers to a masking stimulusblocking the perception of a test stimulus that came before it. Bothmasking types could act during saccades: the blur would be a lowcontrast test stimulus and the mask would be the high contrastimages before and after the saccade.

The first experiment to show how potent such a masking effectcould be was by Matin, Clymer, and Matin (1972) who showed firstthat a light bar limited to the duration of the saccade was seen as alonger and longer blur as the bar’s duration increased within thesaccade duration. But as soon as the duration extended about100 ms beyond the end of the saccade, only a bright bar was seen;the blur was gone. Campbell and Wurtz (1978) illustrated thismasking further by showing that a contoured visual image (a lab-oratory room) was blurred when illuminated just during thesaccade but became clear when the illumination extended 40–100 ms after the end of the saccade. The key point in both of theseexperiments is that with illumination extending beyond the end ofthe saccade, the perception was not a blur and then a clear image,but just the clear image. Masking had obliterated the blur or ‘‘grey-out” (Campbell & Wurtz, 1978). A clear image before the saccade ofmore than 100 ms produced a forward making effect (Campbell &Wurtz, 1978) which also eliminated perception of the blur. Subse-

Fig. 11. Saccadic suppression by visual masking. (A) Forward masking in a V1 ne-uron by a masking stimulus falling on the RF (line under each trace) on a subseq-uent brief RF stimulus (carrot under the trace). In the left column, the eye sweepsthe RF across a stationary RF stimulus, and on the right the RF stimulus is sweptacross a stationary RF during fixation. The top records show the visual response tothe RF stimulus only, the middle trace the reduced response to the RF stimuluswhen preceded by the mask, and the bottom trace to the mask only. Ordinate tickmarks are 100 sp/s; abscissa marks are 100 ms. From Judge et al. (1980). (B) For-ward and backward masking in a V1 neuron in an alert monkey. Black trace is theresponse of the neuron to the RF stimulus alone (Target Only). Pink trace shows theelimination of the on response by forward masking. Blue trace shows the elimin-ation of the transient after discharge by backward masking. From Macknik et al.(1998).


quent experiments (Corfield, Frosdick, & Campbell, 1978) showedthat the elimination of the blur was a purely visual effect. The typeof stimulus in the intra-saccadic interval made little difference(Chekaluk & Llewellyn, 1990). Reduced motion perception duringthe saccade was also shown to be a result of masking by Castetand Masson (2002), 2000). When their subjects viewed stationaryvertical gratings briefly presented during the saccade, they ap-peared to move in the direction opposite to the saccade, that is,in the direction of the grating motion on the retina. As the gratingduration extended beyond the duration of the saccade, the proba-bility of reporting this motion dropped precipitously even thoughthe same motion remained during the saccade.

The point is that masking contributes to saccadic suppression ina normal high contrast environment whereas the CD related to thesaccade itself is independent of the visual background during thesaccade (Diamond, Ross, & Morrone, 2000). On the relative roleof masking and corollary discharge in saccadic suppression thereis little reason to alter the conclusion reached by Volkmann(1986) in her review of 20 years ago: ‘‘Masking effects, therefore,undoubtedly play a primary role in threshold elevations whichaccompany saccades in lighted, contoured environments. It isequally clear, however, that saccadic suppression can be shownto exist under experimental conditions in which masking effectsare minimized . . ..” Visual masking has been extensively studied(for reviews see Breitmeyer, 1984; Bridgeman, 1971; Macknik,2006; Matin, 1975), and it may well be that one of the most impor-tant contributions that masking makes to visual perception is theelimination of the blur during saccades.

9.2. Neuronal correlates

The effectiveness of visual masking during saccades was firsttested in V1 of awake monkeys by Judge, Wurtz, and Richmond(1980). They first tested how frequently V1 neurons respondedto velocities comparable to those of a saccade by using an optimalstimulus: a slit moved across the RF along its long axis so that theintegration time of light in the RF was maximal. Even under theseoptimal conditions only about 50% of the supragranular neuronsresponded, while over 90% of the infragranular neurons responded.Because the anatomical connections of the supragranular layersare primarily to subsequent cortical visual areas (Van Essen,1983), these neurons would seem to be the most likely to contrib-ute to perception. Because no more than half of V1 neurons re-sponded to even optimal stimuli moving at saccade speeds, anymasking effect need only act on a fraction of V1 neurons, and onweak responses at that.

Masking was then studied primarily in the supragranular neu-rons by determining the interaction between a stimulus fallingon the RF before a saccade (comparable to the mask in human psy-chophysical experiments) and the slit stimulus swept across the RFby the saccade. The response of the V1 neuron to the slit during thesaccade was reduced by at least half in 95% of the neurons andeliminated in 35% of them. That this was independent of any CDaccompanying saccades was shown by a comparable interactionbetween a stationary mask and a moving stimulus while the mon-key remained fixating (Fig. 11A). The mask was most effectivewhen there was no interval between it and the RF stimulus whichwould be the case during a saccade.

When the masking stimulus fell on the RF after the saccade,there was a backward reduction of the response during the sweepin only a few neurons (Judge et al., 1980). Instead, the mask pro-duced a possible confounding merging of the responses to thetwo stimuli. A similar effect had been seen in the cat LGN by (Schil-ler, 1968). Finally, psychophysical experiments measured detec-tion of the stimuli with and without a masking stimulus andshowed approximately the same time course for humans as did

the neuronal responses in monkeys, with forward masking beingmore effective than backward masking.

Masking effects have subsequently been quantitatively studiedin V1 neurons by Macknik and Livingstone (1998) in order tounderstand visual masking rather than suppression during sac-cades. They found a forward masking effect similar to that in theprevious observations (Judge et al., 1980). Their masks were adja-cent to the target in the RF instead of in the RF, which is probablywhy their masking reduced responses to about 70% of the un-masked response whereas the reduction during saccades ap-proached 100% (Judge et al., 1980). A key addition in the Macknikand Livingstone experiments (1998) was that for backward


masking the effect resulted from the elimination of an off transientoccurring about 100 ms after RF stimulus offset (Fig. 11B). Furtherwork showed the importance of spatiotemporal edges in producingsuch masking effects (Macknik, Martinez-Conde, & Haglund, 2000),factors that must also contribute to the effectiveness of maskingduring saccades. Other experiments on stimulus interactions havedemonstrated that masking effects in V1 have substantial effectson visual responses including those responses generated bysaccades (Bridgeman, 1980; Gawne, Woods, & Fp, 2003; Richmond,Hertz, Gawne, & Uk, 1999), and such masking interactions haverecently been reviewed by Macknik (2006). Visual interactions alsoare clear in the responses of the SC superficial layer visual neurons(Bender & Davidson, 1986; Rizzolatti, Camarda, Grupp, & Pisa,1973; Rizzolatti, Camarda, Grupp, & Pisa, 1974; Wurtz, Richmond,& Judge, 1980).

Macknik et al. (1998) showed that an optimal combination offorward and backward masking produced an illusion of stimulusdisappearance (the Standing Wave of Invisibility). Since the inter-vals used in this illusion are in the range of those occurring withsaccadic eye movements it is an excellent illustration of the elim-ination of visual stimulation during saccades. It demonstrates thatthe stimulus is not so much suppressed as eliminated; it demon-strates the ‘‘saccadic omission” postulated earlier (Campbell &Wurtz, 1978).

9.3. Conclusion: Visual masking rules saccadic suppression

Visual masking is likely to be the major factor producing sacc-adic suppression in normal high contrast environments. Suppres-sion of V1 neuronal responses to the brief stimuli duringsaccades by stimuli before the saccades (forward masking) aloneappears to be substantial enough to provide the underlying mech-anism. Furthermore, demonstrations of combined forward andbackward masking show that masking can produce not only sup-pression but the perceptual omission of briefly presented stimuli.Such saccadic omission is what is required to avoid a disruptivepause between successive fixations.

10. Summary and conclusions

Understanding why our perception is stable in spite of saccadicinterruptions depends on resolving two problems: displacement ofthe image on the retina after each saccade and suppression of theblur during each saccade. As in many biological systems, there aremultiple solutions for each of these problems.

For saccadic suppression, the multiple mechanisms are wellestablished: visual masking and corollary discharge (CD). Eachmechanism can be dominant depending on visual conditions, withmasking being prominent in the normal high contrast environ-ments and CD in low contrast ones. Neuronal mechanisms for sup-pression by CD have been identified, but rather than acting on theLGN and V1, they seem to act beyond V1. The clearest cortical sup-pression has been demonstrated in MT, and it might result from in-put from SC superficial layer neurons where the suppressiondepends upon a CD input. Neuronal mechanisms for visual mask-ing that are adequate to eliminate the blur during a saccade havebeen identified in V1. Thus, while a number of critical details arestill missing, neuronal correlates for both the CD and the maskingmechanisms have been identified.

Saccadic displacement is the more central, more difficult, andmore interesting problem, both historically and presently. It ishardly surprising that the neuronal mechanism has not been iden-tified, and here we still do not know whether there are multipleneuronal mechanisms. There are two salient neuronal candidates.First are the neurons in frontal and parietal cortex with shifting

receptive fields that provide anticipatory activity with each sac-cade. These could provide support for the retinotopic hypothesisof visual stability based on updating a retinotopic map. The antic-ipatory shift in activity might also provide the memory for thetranssaccadic memory hypothesis of visual stability. The secondneuronal mechanism is provided by neurons whose visual re-sponse is modulated by eye position (gain field neurons) or largelyindependent of eye position (real position neurons). These neuronscould provide the basis for a higher order map for a spatiotopichypothesis of visual stability.

On the basis of the current evidence, I conclude that the shiftingreceptive fields provide the most attractive neuronal basis forunderstanding the mechanisms for visual stability. At the neuronallevel the shift provides a mechanism for shifting the visual sensi-tivity on a retinotopic map, the CD driving such a shift has beenidentified, and a test of the relation of this neuronal activity to per-ceptual stability is now possible. Furthermore, at a behavioral le-vel, the evidence from change blindness suggests that there is nospatial map in the brain but rather a transient retinotopic one witheach saccade. Thus, both the neuronal and the behavioral evidenceavailable now make the updating of a retinotopic map an attractivehypothesis. The shifting receptive fields also provide a possiblemechanism for a transsaccadic memory hypothesis of visual stabil-ity. Happily, even with the techniques now available, these specu-lative conclusions can be modified, rejected, or replaced by furtherexperimental evidence.

Finally, it is important to realize how far we have come inunderstanding what the neuronal mechanisms underlying visualstability might be. We have moved from general conceptions ofthe importance of a CD over several centuries, to fortifying the ideawith direct experimental evidence from flies and fish beginning inthe 1950s, to the more recent neuronal correlates of CD mecha-nisms in the primate brain. The initial search for neuronal corre-lates was for a mechanism that might underlie saccadicsuppression. Such a neuronal mechanism was thought to simplysuppress vision, to act relatively early in the visual processing se-quence, and to serve as a cudgel on any visual input followingany saccade. What has introduced a more profound understandingof how precisely a CD might function, however, is the understand-ing of its action in producing shifting receptive fields in parietaland frontal cortex. Starting with the discovery by Duhamel et al.(1992), studies of these neurons have revealed how a motor basedCD and visual processing can be seamlessly combined: the vectorof the upcoming saccade is used to heighten the sensitivity of neu-rons on a retinotopic map. All the information both before andafter the saccade remains in retinotopic coordinates, but thechanges on the map incorporate the motor information. This illus-trates an organization that was not envisioned on the basis of theCD concept, that expands our conception of possible ways in whicha CD can act, and that emphasizes how far our understanding ofpossible neuronal mechanisms underlying visual stability havecome—and how far they have to go.

Acknowledgments

I am grateful for assistance on the illustrations by M. Smith, forlibrary assistance by A. Griswold, and for critical comments fromthe readers of an earlier draft: R. Berman, D. Burr, T. Crapse, H. Deu-bel, and C. Galletti.

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