Feature Article Vernon B. Mountcastle

The Parietal System and Some HigherBrain Functions

Krieger Mind/Brain Institute and the Department ofNeuroscience, Johns Hopkins University, Baltimore, Maryland21218

A quarter century has passed since electrophysiological stud-ies of the homotypical cortex in waking monkeys began.These are made as monkey subjects emit behavioral acts suf-ficiently complex to qualify as those generated and controlledby the "higher" functions of the neocortex. The general ex-perimental plan is an extension to the study of higher func-tions of an approach proven successful in earlier studies ofthe neocortical mechanisms in sensation and perception, andthe control of movement. The early phase of exploratory ex-periments on the homotypical cortex has now given way tomore precise experiments, quantitative analysis, and modeltesting, and it is clear that we can look forward to a rapidacquisition of knowledge of these complex neocortical op-erations. If progress during the early phase was less rapid thanhad been hoped for, the reasons are easy to find. At the ex-perimental level the linkage between behavioral events andneural activity in homotypical cortical areas is always less pre-cise than in primary areas; in many cases it is conditional innature and influenced by central state functions of the brain,and interpretations are plagued by the ever difficult transitionfrom causation to causality. Interpretations are always besetby varying concept: command or re-afference, attention orneglect, active intention or passive reception, and so on? In-deed, the neurophysiologist who ventured into the homotyp-ical cortex in the 1970s entered a foreign country in whichnew and unlabeled neural events were encountered at everyturn, or rather, in nearly every microelectrode penetration!

This issue of Cerebral Cortex brings together a number ofdescriptions of these new studies of the homotypical cortex,restricted to a sample of the many now underway on theposterior parietal cortex. I preface them with an account ofmy own adventures into the parietal lobe, now long ago.

My Adventures in the Parietal Lobe

Edward Evarts and tbe Transition to tbeWaking Monkey ExperimentGiven a highball or two even the most reserved of scientistsmay be persuaded to reveal a tale of serendipity in research,often with some embellishments that add measurably to itstelling. I have observed this quite often among the highpriests of molecular biology, and even on rare occasionsamong my colleagues in neuroscience. I assert, however, thatthe following is a true account of my first adventures into theposterior parietal cortex of the waking monkey. Many livingwitnesses impose constraint.

It began on a bright Monday morning in April of 1968. Ihad spent the previous Friday visiting my friend the late Ed-ward Evarts, watching as he recorded the activity of neuronsin the motor cortex of a waking monkey as the latter exe-cuted motor tasks. I had left Bethesda somewhat despondent,for I saw difficulty in delivering mechanical stimuli in a pre-cise way to the glabrous skin of the hand of a waking monkey.

That Monday morning changed it all. I glanced down thehall from my laboratory in Baltimore to see none other than

that same Edward Evarts striding toward me, his facewreathed in that wonderful smile, with a large wooden boxon his shoulder. He had brought me all the gadgets requiredfor recording from the waking monkey. With that encourage-ment I could not do otherwise; I used his gifts for a year, andbegan a long series of adventures.

Technical Preparations, and Our First Study of tbeSomatic Sensory Cortex in tbe Waking MonkeyThe next two years were filled with technical and behavioraldevelopment, particularly with William H. Talbot, that geniusof the computer-controlled laboratory experiment (with anoriginal line, memory = 1000 bytes; and only later a PDP);with Robert H. LaMotte, whom I am convinced can read mon-keys' brains and train even the most cantankerous one to ex-ecute difficult tasks; and with an extraordinary engineer, JohnChubbuck. Thus, with improved methods we began to recordthe electrical signs of the activity of single neurons in thepostcentral somatic sensory cortex of monkeys as they exe-cuted sensory tasks, in this case the detection of a sine wavemechanical oscillation at the flutter frequency (10-40 Hz) su-perimposed upon a 0.5 mm step indentation of the glabrousskin of the hand. All went well, and by the summer of 1970we had established a correlation between the increasingprobability of correct detection with increasing stimulus am-plitude, and an increase in the cyclic entailment of the cor-tical neuronal activity at the stimulus frequency (see Figs. 1,2; Carli et al., 1971a,b). Alas! When we examined neuronalresponses to stimuli detected only 50% of the time, we foundno differences between those evoked by stimuli detected andthose missed! Where was the critical neural event uponwhich detection depended?

Transition to Study of tbe Posterior Parietal AreasThus, it was more in frustration than in a planned experi-mental foray that on 8 September 1970 in monkey BM 19we (Robert LaMotte, now at Yale University; Carlos Acuna,now at the University of Santiago de Compestella in Spain;and I) suddenly changed the locus of recording from thepostcentral somatic sensory area to the posterior parietalhomotypical cortex, first on that day to area 5, and a fewmonths later to area 7. What we observed in those explor-atory experiments determined my experimental life for fif-teen years: neurons that were active if and only if the animal"had a mind" to deal with the stimulus in a behaviorallymeaningful way! In area 5, there were neurons active whenthe animal projected his arm toward a target of interest, butnot during random arm movements; and neurons activewhen the animal worked with his fingers to extract a morselof food from a recess, but not during other hand actions likepinching (we called them "winkle neurons"). Quite differentsets of neurons appeared to drive the transport and graspingphases of reaching movements. Other sets of neurons wereactivated by joint rotation, more intensely during his activejoint rotations than when the joints were rotated passively

Cerebral Cortex Scp/Oct 1995:5:377-390; 1047-3211/95/W.OO

Rgnn 1. Results obtained in study ofthe postcentral somatic sensory cortexof a monkey as he worked in a flutterdetection task. Stimuli were delivered tothe glabrous skin of the hand in the ar-rangement shown in figure 1 A, Impulsereplicas of a cortical neuroa Each linewas obtained during a single trial; eachshort upstroke indicates the instant atwhich the neuron discharged an im-pulse. Peak-to-peak amplitudes of themechanical sinusoid imposed on a 500(jjn step indentation of the glabrous skinare shown to the right Trials at differentamplitudes were sequenced randomly.Trials are separated into those detected(W75) and those not detected (M/SSfS).B, Analysis of power in the neuronal sig-nals by Fourier shows growth of the firstharmonic pan passu with the increasingcertainty of correct detection. However,analysis of hits and misses at the 50%point of detection revealed no differ-ence. Data from Carli et aL (1971a).

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by us; still others by cutaneous stimulation, frequently fromlarge, bilateral receptive fields, often with directional selec-tivity. In area 7, there were neurons active during visualfixation of objects of interest, but not during casual fixations,and insensitive to visual stimuli; neurons active during vi-

sually evoked but not during spontaneous saccadic eyemovements; neurons active during smooth pursuit visualtracking; and neurons that responded to visual stimuli, perse, with unusual receptive fields and response properties.We called diem "light-sensitive" or "visual space" neurons,

378 The Parietal System and Some Higher Brain Functions • Mountcastle

Hgura 2. Apparatus used for the exper-iment the results of which are shown inFigure 1. Tactile stimulator shown to theleft poised over the glabrous skin of therestrained hand of the waking monkeysubject Microdrive and cathode followerare shown upper right Box surroundingthe head, shown cutaway, contained sig-nal lights indicating trial onset, and soon. Reprinted with permission, fromMountcastie et al. (1972).

leaving open for the time being the question of whetherthey played an active role in visual perceptions.

The major source of information about the putative func-tions of the parietal systems was in the descriptions of pa-tients with lesions of the parietal lobe (Critchley, 1953). I be-gan to attend the neurological ward rounds in the hospital,and soon my colleagues Guy McKhann and Richard Johnsonshowed me a patient who had sustained a vascular lesion ofhis right posterior parietal cortex, and who displayed all theclassical signs of optic ataxia and contralateral neglect. Heloudly complained of a foreign arm in his bed—it was hisown! I followed this patient's history, and observed his re-markable degree of recovery, such that one year later it wasnot easy to demonstrate either his neglect or his optic ataxia.This was of great interest to me in relation to the function ofdistributed systems. I obtained and reviewed all the case his-tories in the Johns Hopkins Hospital filed under the label"parietal lobe syndrome," and I reviewed the relatively sparseliterature on studies of the effects of parietal lobe lesions innonhuman primates, as well as that describing the connectiv-ity of these regions. These reviews provided a base for a scriesof studies of the parietal lobe system I then carried out witha succession of extraordinarily able collaborators, in temporalsequence: W. H. Talbot, R. H. LaMotte, C. Acuna, J. C. Lynch, H.Sakata, A. P Georgopoulos, T. T. C. Yin, B. C. Motter, C. J. Duffy,R. A. Andersen, M. A. Steinmetz, and A. K. Sestokas.

These exploratory experiments indicated how useless itwas to study the posterior parietal cortex in a qualitative way,or with the standard sensory stimuli available to us. JohnChubbuck designed the test apparatus shown in Figure 3.This provided a target light carried on a car moved at differ-ent speeds for selected arcs of the circle, all under programcontrol. We then studied the reach neurons of areas 5 and 7,as the monkey made arm projections at different angles forthe same distances, and tracked the moving target with eyeand hand. For the reach neurons we also combined the tactilestimulator of Figure 2 in the apparatus of Figure 3, and dis-covered that the activity of a typical reach neuron is inde-pendent of the sensory channel—somesthetic or visual—evoking the movement, in both a lighted and a darkened en-

vironment. This was at least for us compelling evidence thatin areas 5 and 7 we dealt with a higher order of corticalfunction than we had hitherto encountered, and that ourdeeply embedded concepts derived from studies of primarysensory areas were too simple for the new tasks. We managedsome preliminary reports in 1973 (Lynch et al., 1973a,b), butour first full-length report was delayed until 1975 (Mountcas-tie et al., 1975).

Several things became clear early in our studies: first, dratit is possible to study the higher functions of the brain innonhuman primates, but only if the complex properties ofthe homotypical cortex are matched by equally complex be-havioral tasks, and that quantitative studies under controlledconditions are essential; second, that although the propertiesof posterior parietal neurons do provide a limited positiveimage of the defects of the parietal lobe syndrome, the func-tions inferred are embedded in dynamic neuronal processesin widely distributed systems of the forebrain, in which theparietal lobe is but one of several essential nodes; third, whatis important for experimental design, that in any given ex-perimental arrangement one cannot study quantitatively all ofthe many classes of parietal neurons, perhaps at best only two.This makes especially acute the ubiquitous sampling problemthat dogs all electrophysiological studies of the cerebral cor-tex, and emphasizes that conclusions drawn from any smallsample of neurons are especially hazardous. This is, I believe,the explanation of why in so many cases different investiga-tors describe populations of parietal neurons with quite dif-ferent properties, even though recording from what are pu-tatively the same areas of cortex. These differences provideno grounds for polemic controversy.

Cerebral Cortical Mechanisms in the TransportPhase of Directed ReachingPsychophysical studies of reaching and grasping in humansand in nonhuman primates have documented the decompo-sition of reaching to a target into a transport phase of projec-tion of the arm and hand, and a grasping phase in which thehand adapts to the spatial contours of the target. Studies ofthis sort have been made in many laboratories, and with par-

Ccrebral Cortex Sep/Oct 1995, V 5 N 5 379

Figaro 1 Drawing of a Macaca arcto-ides working in the test apparatus usedin our first studies of the reach, handmanipulation, fixation, and tracking neu-rons of the posterior parietal cortex. Thehead-fixation apparatus, implanted mi-crodrive, cathode follower, and rewardtube are shown upper left The signalkey is seen through the cutaway of thecircular race. The animal has just re-leased the key with his left hand andprojected his arm and hand forward tocontact the light switch mounted on themoving carriage, upper right The car-riage could be moved from any presetposition in either direction at speeds of12 or 21 degrees/sec for preset distanc-es. All parameters were under PDP 11control. Drawing by Mrs. L Bodian, fromMourrtcasfJe el al. (1975), reprinted withpermission.

ticular elegance and insight by our colleagues in France, par-ticularly by Paillard (1982,1991),Jeannerod et al. (1988,1996),and Perinin and Vighetto (1988). These two phases have beenselectively damaged by lesions located in different parts ofthe parietal lobe in human subjects.

It was the perceptive insight of Georgopoulos that visuallyguided reaching movements of the arm could be studied inthe waking monkey experiment, both for the immediate prob-lem of the motor and premotor cortical activity controllingdirected reaches (Georgopoulos et al., 1982, 1986; Georgo-poulos, 1991; 1994), and for the more general problem of thesensory-motor interface, in this case the population codingsbetween the parietal and frontal lobe mechanisms involved.He used a directional vector to define the population signalin the motor cortex driving reaching movements, a methoddevised by K. O. Johnson, and it was Georgopoulos who ob-served neuronal activity directly correlated with a silent andunexpressed "mental" activity, mental rotation (Georgopouloset al., 1989). Since then research on the posterior parietal andmotor cortical mechanisms in reaching has reached a level ofsophistication rarely matched by any other body of neuro-physiological studies of the neocortex in waking monkeys.

The problem of the neural mechanisms in reaching to vi-sual targets opened for study several major themes in thephysiology of the neocortex. How are precise signals for ac-tion generated in a population of imprecise neural elements?How are the neural signals for different parts of a complexaction—like the transport and grasping phases of reaching—processed in parallel in different parts of a widely distributedsystem, yet finally converge (but never to a single point) todrive a smoothly phased temporal evolution of the action?How are different neural operations composed in differentframes of reference, yet coordinate transforms between themachieved? Understanding of these matters is still incomplete,but the major problems are all in play in the experimentalarena, and discoveries flow in rapid succession from manylaboratories. This area of research has been characterized byan unusual convergence of psychophysical, anatomical, neu-rophysiological, and modeling methods and concepts that ac-counts in large part, I believe, for the rapid progress that hasbeen made (for reviews, see Jeannerod, 1988; Paillard, 1991).

Some aspects of the role of the posterior parietal corticalareas in reaching to visual targets are described in three ar-ticles, two in this issue of Cerebral Cortex.

In an article in a forthcoming issue of Cerebral Cortex,Caminiti et al. (1996) will provide a review of a host of newstudies of the neural connections between several recentlydefined areas of the posterior parietal cortex. The results de-scribed resolve a long-standing problem in understanding thecortical mechanisms in visually guided reaching. That is, thatwhile projections are known to link area 5 to the dorsal pre-motor area of the frontal lobe, and also directly to the motorcortex itself, no connections had hitherto been shown to linkthe visual mechanisms of the inferior to the motor mecha-nisms of the superior parietal lobule. The new studies madewith tracing methods have now revealed strong projectionsfrom the prestriate and posterior parietal visual areas to amore medial parietal area, PO, which projects forward uponthe region of area 5 lining the anterior bank in the medialportion of the intraparietal sulcus. This provides the link fromthe visual to the somesthetic and motor mechanisms involvedin visually guided reaching. It is of special importance, for amajor class of visual neurons of area 7a is optimally suited byvirtue of its motion and directional sensitivities to guide themovement of the arm through the periphery of the visualfield during the transport phase of visually guided reaching(Motter and Mountcastle, 1981).

The cortex of area 7a lining the posterior bank of the in-traparietal sulcus in its more medial extent contains a signif-icantly large population of reach neurons. These resemblethose of area 5, described above, but differ in that they aremore likely to be active with reaches of either arm (Mount-castle et al., 1975). MacKay (1992) has studied these cells andobserved that when "bilateral" reach neurons have a direc-tional preference, that direction is similar for the two.

Lacquaniti et al. (pp 391-409 in this issue) present a newand penetrating analysis of a population of reach neurons inarea 5 studied in Caminiti's laboratory, in the three-work-spacearrangement shown in their Figure 1. They show that thedirectional vector tuning is much less precise for the parietalpopulation than it is for neurons of the motor and premotorareas of the frontal lobe. For example, only 22% of parietal

The Parietal System and Some Higher Brain Functions • Mountcastie

reach neurons fit the directional vector model for all three ofthe cubed work spaces, versus the 75% of motor cortical neu-rons that do so. Moreover, when a parietal neuron is direc-tionally tuned in at least two of the work spaces, the preferreddirections for individual neurons change in an idiosyncraticway from one space to the next, with average but disorgan-ized rotations of 50°. This contrasts with the motor cortexpopulation, where the preferred directions change in a uni-form and systematic way from one work space to the adjacentone, to a degree determined by the angular rotation of theshoulder required by the change.

Lacquaniti et al. base their analysis upon the results of psy-chophysical studies indicating that the transformation fromsensory signals to motor commands for reaching movementsis specified in a body-centered coordinate system. They thendemonstrate that the activity of area 5 reach neurons is mon-otonicly tuned in a way encoding the start position of thehand, its movement through successive way points in space,and its final location at the target, all in a body-centered frameof reference probably centered on the shoulder. Several mod-els were tested, and the spherical angular one centered at theshoulder achieved the best prediction of the experimentalobservations. A finding of considerable interest is a strongtendency for die individual spatial coordinates (whether an-gular or Cartesian) to be encoded in separate subpopulationsof parietal reach neurons. This is a particularly concise ex-ample of parallel processing, for the total movement is sig-naled in quasi-separate populations, and I conjecture thatthese three never converge to any summing or nodal points,but engage directly the premotor/motor cortical mechanismsof the frontal lobe. This emphasizes the need for further studyof the population-to-population interface in the sensory mo-tor transformation.

All current and past studies of area 5 leave unresolved thequestion of its relative position and role in the distributednetwork controlling projection movements of the arm andhand to visual targets. Although the responses of area 5 reachneurons to passive stimulation of the contralateral arm arevery weak, nevertheless 80% of those analyzed by Lacquanitiet al. were responsive at some level to such stimuli. Are weto conclude diat the area 5 activity is largely produced bysensory re-afference from peripheral receptors during move-ment, and used in some matching operation for correction ofdie actual to the intended movement? Unhappily, no separateanalyses have ever been made of die 20% (or more) of area5 reach neurons insensitive to sensory stimulation, nor ofdiose (are they die same?) shown by earlier studies of severalinvestigators to remain active during visually evoked reachingmovements after section of the dorsal roots.

On the assumption diat an area 5 reach neuron populationexists Uiat is not driven directly from die moving arm, diequestion remains unsettled whether diat population is drivenby a central reentry—and used for die matching operationsdescribed above—or whedier diat population is an essentialnode in die command operations linking visual signals of thetarget and motor cortical compositions of die reach move-ment. Measurements of relative timing of onset of activity inrelation to movement onset may not setde die matter, for dieyhave usually been made in highly overtrained monkeys work-ing in reaction time tasks. Indeed, Kalaska (1991) has nowshown in studies using an instructed delay task diat die ac-tivity of reach neurons of area 5 consistendy leads diat ofneurons of area 4, and Burbaud et al. (1991) found diat die"early" area 5 reach neurons lead all odier cortical neuronalpopulations active in reaching. It appears diat these time re-lations depend critically upon die task in which die animalis engaged.

It was Kalaska and his colleagues who first discovered that

area 5 reach neurons are virtually unaffected by loads diatoppose die movements of die contralateral arm in visuallyguided reaching (Kalaska et al., 1990). The area 5 populationappears to encode movement kinematics, good evidence diatdiey are not driven, or not driven only, by sensory re-afferenceduring movement, for certainly diat afferent barrage will bechanged markedly during load-opposed movements. Neuronsof die motor cortical areas, by contrast, include many whosedischarge is markedly changed by opposing loads, particularlyunder dynamic conditions (Evarts et al., 1983; Georgopouloset al., 1992). This dissociation suggests diat area 5 reach neu-rons are not driven by a centrally contained reentrant dis-charge derived from the motor cortex, although it does notrule out die unlikely possibility diat such a reentrant dis-charge might originate elsewhere. Kalaska and Crammond(pp 410-428 in tills issue) now describe another remarkabledifference between parietal and frontal populations of reachneurons. They studied diese neuronal sets as monkeysworked in instructed delay tasks in which, cued by earlierappropriate signals for each trial, diey eidier emitted or witivheld movement at die end of die delay: die go/no-go para-digm. Bodi sets of neurons develop significant directionalitiesduring die delay in go trials, but only die parietal neurons doso during no-go trials. The signal not to go appears to beinserted "central" to die parietal lobe, perhaps in die premo-tor and motor cortical areas. This provides further evidenceagainst die central reentrant hypodiesis of parietal lobe func-tion in visually guided reaching.

In summary, a number of important discoveries have beenmade in recent years concerning die role of parietal lobemechanisms in visually guided reaching movements of thearm. Neuroanatomical tracing studies have revealed a robust,multistaged projection linking the prestriate visual areas todie putative motor mechanisms of area 5 of the superior pa-rietal lobule. The population vector describes die parietal ac-tivity during movement less precisely than it does for neuronsof die dorsal premotor and motor areas of the frontal lobe. Amodel based on positional coding in a bodycentered refer-ence frame anchored on die shoulder fits die activities ofparietal neurons adequately. The tiiree dimensions of move-ment in diis space appear to be encoded by separate butoverlapping sets of area 5 reach neurons. The demonstrationof kinematic coding by die area 5 population and dynamiccoding by die premotor and motor populations argues againstthe peripheral re-afferent explanation of parietal activity. Anew experiment made in botii frontal and parietal areas asmonkeys worked in instructed-delay, go/no-go reaching tasksexposed a second dissociation. The signal not to move ap-pears to be inserted between parietal and motor populations,or perhaps in the motor cortical areas diemselves. Furtherprogress will now depend, I suggest, upon development ofaccurate methods for identifying die types and laminar local-izations of neurons from which recordings are made (Tairaand Georgopoulos, 1993; Wilson et al., 1994).

Cerebral Cortical Mechanisms of the GraspingPhase of Directed ReachingOur first experiments on die posterior parietal cortex of diewaking monkey yielded a number of unusual observations;among diem was die discovery of the hand manipulation neu-rons (HM) of areas 5 and 7 (Lynch et al., 1973a; Mountcastleet al., 1975). HM neurons are virtually silent during the trans-port phase of visually guided reaches. They discharge intense-ly during the grasping phase, as the hand is molded to dietarget, or during odier exploratory manipulations. Our firstobservations of HM neurons were made as a monkey shapedhis hand to obtain a raisin from a receptacle sllghdy smallerthan die resting palm diameter (it was a 100 ml beaker). This

Cerebral Cortex Sep/Oct 1995, V 5 N 5 381

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activity was particularly intense when the receptacle was pre-sented 15-20 cm in front of the face, associated with visualfixation of as well as manipulation for the food object. Wesoon discovered that the activity of the majority of HM neu-rons was undiminished when the animal's view of the targetwas occluded before arm release, and this became one of thedefining characteristics of HM neurons. Other neurons of area7, but not of area 5, are active only during visual fixation, andanother set appears to sum the effects of visual fixation andhand manipulations.

Sakata and his colleagues have pursued study of the area 7HM neurons, with results described in a series of reports(Taira et al., 1990; Sakata et al., 1992; Jeannerod et al., 1995),and in Sakata et al., pp 429-438 in this issue. These investi-

gators discovered that area 7 HM neurons are selectivelytuned to several broad categories of the shapes of targets.Moreover, they found that certain of the special HM/visualfixation neurons referred to above are sensitive to the sameshapes, whether viewed or manipulated. The spatial patternsselected appear to be very broad, with considerable overlapin selectivity for individual neurons. It is still unknown wheth-er or not the selectivities observed are samples of a widerange existing a priori, though this appears unlikely. It remainsto be determined whether the selectivity for objects in theseexperiments resulted from prolonged preexperimental train-ing, and whether training with different objects might pro-duce posterior parietal neurons with spatial selectivities fit-ting the form of the training objects.

The HM neurons studied by Sakata et al. were located inthe anterolateral limb of the posterior bank of the intrapar-ietal sulcus, in a region he calls the anterior intraparietal area,AIP. However, his illustrations show that more than 50% of theHM neurons studied were located in the lateral intraparietalarea, LIP, a region studied by Andersen (pp 457-469 in thisissue) and by Colby et al. (pp 470-481 in this issue) for quitedifferent purposes and with what must certainly be quite dif-ferent and differentially selected populations of cells.

The zone of area 7 HM neurons is heavily and reciprocallyconnected with the inferior premotor area of the frontal lobe,where Rizzolatti and Gentilucci (1988) studied neurons withproperties similar to those of area AIP. The inferior premotorarea projects heavily upon the hand area of the motor cortexitself. How area AIP of the parietal lobe and the inferior pre-motor area of the frontal lobe are fitted into the distributedsystem controlling grasping is still uncertain. What is clear isthat the two parietofrontal systems concerned respectivelywith the transport and the grasping phases of visually direct-ed reaching are to a considerable degree independent untiltheir final convergence upon the motor cortex. Yet the resultis a smooth and neatly ordered sequence of skilled move-ments. How that conjunction is effected is a major subject forcontinuing study.

Figure 4. Drawing of the apparatus usedby Yin and Mountcastle (1977a) in ourfirst study of ths visual neurons of theinferior parietal lobule. A laser beam isprojected from above via stationary andgalvanometer-driven mirrors upon thetangent screen placed 57 cm from themonkey's eyes. The beam spot (1 mm di-ameter) could be moved at speeds up to380 degrees/sec, dimmed, and turned onor off all under computer control. Forstudy of saccade neurons, the tangentscreen was replaced by another con-taining 16 LEDs in a static spatial array.The I f Ds could be turned on or off in alarge number of spatial and temporal se-quences. Drawing by Mrs. E Bodian,from Yin and Mountcastle (unpublishedobservations).

332 The Parietal System and Some Higher Brain Functions • Mountcastle

Figure 5. Behavioral test apparatus usedin our special studies of the visual, track-ing, and saccade neurons of the inferiorparietal lobule. The headholder allowedpositioning in the neutral position shown,or turned HP left or right. Of freed in thehorizontal plane for periods of rest dur-ing recording sessions. Microdrive andchamber are not shown. Two back pro-jectors were used. The first positionedthe target laser spot wherever desired ormoved in any direction at velocities upto 800 degrees/sec. The second project-ed luminous stimuli of variable sizes, in-tensities, and directions of movementover the same velocity range. A panel of600 LEDs could be inserted in front of thescreen along guide rails, for studies ofsaccade neurons. Drawing by Mrs. E.Bodian, from Motter and Mountcastle(1381), reprinted with permission.

Nevertheless, the general conclusion appears certain, thatthe transformation of the intrinsic spatial properties of ob-jects—their three-dimensional form—into efferent signalsdriving a matching shaping of the hand takes place in a dis-tributed system that includes parietal areas ATP and LIP, andthe inferior premotor area of die frontal lobe.

The HM neurons of area 5, in the anterior bank of theintraparietal sulcus, have apparently not been studied furthersince their original description.

The Parietal Lobe System and Visuospatial PerceptionIt is an ancient problem in philosophy and psychology wheth-er we perceive space as such, or, indeed, for some philoso-phers whether space itself exists outside our brains! Thesematters need not detain us here, except to say what is obvi-ous, that we do not sense/perceive space as such. No sets ofafferent fibers we possess are activated by "space." When ahuman subject is placed in a structureless visual surround, aganzfeld, he is visually aware of only a gray, fog-like surround.We perceive space in terms of the spatial locations and rela-tions between objects and events within that space, and therelations of these to our own bodies, and the relations be-tween our body parts, and our relation to the direction ofgravity. Thus, spatial perception requires the integration ofsignals in many different afferent systems, visual, vestibular,somesthetic, proprioceptive, auditory. And, we interpret thesein relation to our stored and continually updated central im-age of the body form, what Head and Holmes called the "bodyschema," a happy metaphor disguising ignorance.

Tbe Parietal Lobe SyndromeThe syndrome produced by lesions of the parietal lobe sys-tem in humans is so well known it needs no detailed de-scription. The feature attracting the attention of experimen-talists is that it comprises a variety of disorders in the per-ceptual, attentional, intentional, and motor spheres, frequent-

ly without defects in what are loosely termed primarysensory and motor functions; that is, they are disorders of"higher functions." Given the variations in the locations andseverity of naturally occurring lesions in human brains, quitedifferent samples of the full panorama of defects appear indifferent patients. Briefly, there are disorders of attentionwith neglect of the contralateral body and immediately sur-rounding space, often with denial of neglect or indeed ofany disease at all. Disorders of volition are common, withreluctance to move a contralateral body part but with reten-tion of primary motor capacity. Errors are seen in both thetransport and grasping phases of visually guided reachingmovements of the arms into contralateral space, called opticataxia. The disorders of visuospatial perception are striking,for many such patients cannot identify the spatial relationsbetween objects seen, are defective in the topographicalsense, and are unable to recognize or reach to even familiarobjects in the periphery of the visual fields. There is a slow-ness in visual fixation of objects in the contralateral visualfield, but equal difficulty in disengaging fixation onceachieved, and in shifting gaze and attention to new objects.Many of these disorders have been produced in more pallidforms by parietal lobe lesions in nonhuman primates; thatof optic ataxia has been easiest to produce and measure. Itis important to emphasize that these disorders are producedby lesions in a widely and heavily interconnected distributedsystem (see Caminiti et al., 1996) in which the posteriorparietal cortex is one of several nodes. Equally important isthe fact we have known since the landmark report of Bisiachand Luzzati (1978) that information concerning the spatialsurround is not irretrievably lost after parietal lobe lesions.The deficit is one of access. Bisiach et al. now describe, intheir article on pp 439-447 of this issue, a dissociation be-tween two forms of neglect: an ophthalmokinetic one as-sociated with parietal lobe damage and a myelokinetic oneassociated with frontal or subcortical brain damage.

Cerebral Cortex Sep/Oct 1995, V 5 N 5 383

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Rgure 6. Impulse repScas (4) and radially oriented discharge histograms (B, Q for a parietal visual neuron, evoked by a 10° x 10° luminous stimulus, 0.6 log units more intensethan the 2 cd/itf background, moved inwardly and then outwardly with respect to the fixation point in each of eight radial directions for 100° through the visual field {long arrows),as the monkey fixated a small central light Trials along different axes were sequenced randomly. Vertical dashed lines in A indicate stimulus onset; small vertical arrows, the instantswhen the moving stimuli crossed the fixation point Each line shows the result for a single trial; each small upstroke, the instant at which the neuron discharged an impulse. Theradially oriented impulse histograms of B and their statistically reduced form in C (rates significantly above background control levels) show discharge frequencies as stimuli movedinwardly toward the fixation point {hatched) and outwardly {solid) away from it in each of the eight radial directions. Bin size, 50 msec; vertical bar, 100 impulses/sec; stimulusvelocity, 60 degrees/sec. Reprinted with permission, from Mountcastie et al. (1384).

Problems Posed in the Transition to tbeStudy of Higher FunctionsThe first is the transition required in thinking from that ap-propriate for study of sensory and motor systems to a com-pletely new arena. Here conditionality is prevalent, relationsof neuronal activity to behavioral states and actions obscure,and powerful general state control functions affect both be-havior and its relevant neuronal mechanisms. The latter arethought to result from the "integration" of a variety of afferentinputs with stored records of experience, and lead throughstates of intentionality to motor output. We found this tran-sition difficult at first, and it is clear that some investigatorsare still in transition, while others retain the attitude that all

neurons of the neocortex are either directly sensory or di-rectly motor.

A second problem is how do we define in neural termswhat is meant by phrases like "the body schema," or "con-struct a viridical image of surrounding space"—a phrase Imyself have used. One simple meaning is that all the partic-ular elements required for such "neural constructs" must con-verge upon or reside in the memory-induced repertoires ofdifferent but overlapping distributed systems. Well and good,but what next? How is such a "neural construct" brought toand maintained in action, and how does it flow through stagesof intentionality to output motor commands? I know of noway in which this central problem can be studied directly

384 The Parietal System and Some Higher Brain Functions • Mountcastie

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Hgare 7. Comparison of the responsesof a parietal visual neuron evoked in dif-ferent attentional states, to iDustrate thestrong facilitation by attention of re-sponses evoked from the nonfoveal re-ceptive field. In the no-task mode, theanimal is not working, and makes spon-taneous saccades to and oculomotorpauses at randomly distributed locationson the tangent screen. In task mode Athe animal is steadily fixating a targetlight whose dimming he cannot predictin time, but which he must detect for re-ward. In fast mode B the target lightblinks off before an during stimuli, andthe animal maintains steady fixation ofthe location at which he knows it willreappear, before dimming. The neuronsubtended a receptive field in the upperhalf of the visual field; all stimuli weredelivered close to the point of fixation, inidentical retinotopic coordinates on alltrials. The facilitation ratio between re-sponses evoked in the task modes andthe no-task mode was 83. The re-sponses in the no task mode and in taskmode A were also studied in total dark-ness, with similar results. Above, impulsereplicas: each line represents recordingin a single trial; each short upstroke, theinstant of neuronal discharge. Dashedlines, 1 SEM for each bin; bin size, 50msec. Diamonds indicate bins of the lefthistogram significantly different fromsimilarly marked bins in the histogramsat center and right Reprinted with per-mission, from Mountcastie et al. (1381).

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with presently available neurophysiological methods. Thus,for the time being, the most productive approach may be toclose in on the problem by studying one by one things thatcan be identified as constituent elements.

A third is the problem of spatial constancy: how are coor-dinate transforms executed, for example, from retinotopic tohead to body to external space frames, or, as some believe,whether such transforms are needed at all.

A fourth is the problem of the direction and redirection ofattention. Defects in attention are among the most obvious ofthe behavioral defects produced by parietal lobe lesions, andsome scholars believe that all the defects can be interpretedas primarily those of attention. What have been observed untilnow in neurophysiological studies of the parietal lobe cortexin waking monkeys are the pervasive effects of attention, notits mechanism. Efforts to infer the latter from the former haveso far been fruitless.

A fifth is the problem of visually guided reaching and grasp-ing, which I have discussed above and which is undoubtedlyat the present time the best understood of the many functionsof the parietal lobe system.

Survey Studies of the Inferior Parietal Lobe NeuronsOur first systematic recordings in the inferior parietal lobulebegan in monkey BM 25, from 8 February, 1972 onward, firstwith James Lynch, now at the University of Mississippi, andCarlos Acuna, and later in a long series of experiments withother colleagues listed above. We encountered a new and forus unusual problem: a vast area of neocortex in •which we

could make out no topographic pattern of any sort, and in-deed, none has been discovered there to this day. It is re-markable that there is no topographic mapping of space inthose cortical areas and systems preeminently concernedwith spatial perception, as defined above, and for the gener-ation of intentions and, conditionally, commands for visuo-motor and somatomotor operations within that immediatelysurrounding space. The area contains different sets of neuronswhose properties differ greatly; these sets are encountered inclosely adjacent (1 mm or less) penetrations of the exposedcortical surface, and appear in en bloc sequences during pen-etrations made down sulcal walls, parallel to the cortical sur-face. We therefore undertook two survey studies, I and n ofTable 1, made in sets of apparatus shown in Figures 3 and4, for we quickly learned that what is called "clinical" exam-ination is virtually useless in defining the functional proper-ties of parietal neurons. We attempted to make those defini-tions for every neuron whose action potential we could bringunder study.

The major classes we identified are listed in Table 1: thefixation, oculomotor, reach/hand-manipulation, visual, and spe-cial neurons. However, no certainty attaches to the propor-tions of neurons in each of the classes of Table 1, save thateach class is present in substantial numbers. There remaineda very large number whose properties we could not defineat all. The special class consists more often of neurons thatcombined the properties of two of the other classes, for ex-ample, oculomotor or reach neurons with visual receptivefields. These appear to have attracted considerable attention

Cerebral Cortex Scp/Oct 1995, V 5 N 5

Figure 8. Sinusoidal variation in the re-sponse of a parietal visual neuron tostimuli moving along radial axes throughthe visual field and across the fixationpoint, during a task requiring attentivefixation. The histograms show the timecourse of the change in discharge fre-quency during the inward {solid) andoutward [operii halves of the 100° stim-ulus movement in each of the eight di-rections indicated. The mean and peakfrequencies of discharge are plotted asfunctions of the directions of stimulusmovements for both inward and outwardhalves of stimulus movement Solid linesconnect data points; dashed lines showsine waves fitted to the data by periodicregression. Reprinted with permission,from Steinmetz et al. (1387).

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from later investigators, so much so that some have been ledto believe that they are the only class that exists in the infe-rior parietal lobule, where every neuron is said to possess avisual receptive field! While the special neurons may be moreplentiful than our experience indicated, the suggestion thatonly they exist in the inferior parietal lobule is simply absurd.

Visual fixation neurons increase their discharge rates withthe visual grasping of desired objects, or of the surrogate tar-get light in a trained paradigm. The increment is sustaineduntil reward, then subsides even without change in the lineof gaze. These neurons are inactive during fixations of blandobjects in the surround. The gaze fields of fixation neuronsare most often confined to a quarter or half of the visual field,the result of a powerful angle of gaze effect. Control experi-ments showed that fixation neurons are insensitive to visualstimuli per se. Nearly half of the fixation neurons are sup-pressed when fixation is interrupted by a saccade, and thosesuppressed are preferentially located in the infragranular lay-ers. Thus, a superimposed saccade loosens the output fixationsignal descending from the parietal cortex to brainstem struc-tures (Mountcastle et al., 1975; Lynch et al., 1977).

Two classes of oculomotor neurons were identified. Track-ing neurons are active during eye pursuits of slowly movingobjects, and are inactive during steady fixations. They are di-rectionally oriented, are suppressed by a saccade superim-posed upon the tracking movement, but are relatively insen-sitive to tracking speed. The saccade neurons are active be-fore and during visually evoked but not spontaneous sac-cades; the discharge leads and peaks during the eyemovement. Many saccade neurons are preferentially activewith saccades directed contralateral to the hemisphere inwhich they are located. The discharge rate is relatively insen-sitive to saccade amplitude. A powerful angle of gaze effectInfluences the activity of both classes of oculomotor neurons.Tracking neurons differ in discharge rate during tracks of sim-ilar length and speed located in different parts of the gaze

field, as do saccade neurons for differently located saccadesof equal amplitude and direction.

Special Studies oftbe Visual Neurons of theIftferior Parietal LobuleMy colleagues and I then initiated a series of special studiesof the visual neurons of the parietal lobe (Table 1). We firstmapped their receptive fields with small stationary stimuli, inthe apparatus shown in Figure 4 (Yin and Mountcastle,1977a,b). We identified two classes of visual neurons. The firstsubtends large and frequently bilateral receptive fields, inwhich the loci of greatest sensitivity are at the far periphery,exempting the foveal-parafoveal regions. Class I neurons re-spond with mean latencies of about 80 msec, and adapt slow-ly to steadily maintained stimuli. Class D visual neurons re-spond at longer latencies (115 msec), subtend smaller usuallycontralateral receptive fields in which the most sensitive lociare near the center of the field, and are enhanced when thestimulus becomes the target for a saccade. Of the first 98receptive fields mapped, not a one included the foveal region.

Our attention was riveted by the large class I parietal visualneurons (FVNs), for their properties indicated that the rep-resentation of the visual world in the inferior parietal lobulediffers strikingly from that in the temporal lobe componentof the transcortical visual systems. We studied them in theapparatus shown in Figure 5. PVN receptive fields are fre-quently large, bilateral, exempt the fovea, and cover from aquarter to—in the limit—the entire visual field, from one mo-nocular rim to the other (Motter and Mountcastle, 1981). Bi-lateral receptive fields of this extent are not known to occurin any of the way-stations between the striate cortex and theinferior parietal lobule, so that the interhemispheric conver-gence required to construct them must occur within the in-ferior parietal lobule itself. Such a field is illustrated by theimpulse replicas and radial histograms of Figure 6, which il-lustrates also another unusual property of PVNs: they are ex-

3SS The Parietal System and Some Higher Brain Functions • Mountcastle

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quisitely sensitive to stimuli moving inwardly or, for a differ-ent set, outwardly across the rim of the visual field. And, theyrespond rather indiscriminantly over a wide range of stimulusspeeds (Motter et al., 1987).

We then discovered the powerful effect of attentive fixa-tions upon the excitability of PVNs: the absence of a responsein the foveal-perifoveal region is produced by an active andpowerful suppression, associated with an equally strong facil-itation of the responses to moving stimuli in the field periph-ery (Figs. 6,7; Mountcastle et al., 1981). Thus, the effect ofattention upon the parietal system is reciprocal to that it ex-erts upon the striate-temporal lobe component, for in the pa-rietal system there is a suppression of response to the objectfixated, and a strong facilitation of response to novel stimuliappearing in the periphery. Thus, the head of the attendingprimate is surrounded by a halo of high sensitivity to movingobjects entering or leaving the visual field, a mechanism ofgreat survival value to primates who spend long periods oftime in intensely attentive close-in hand and eye work, forexample, the monkey during feeding. This effect also provides

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a suitable neuronal base for the flow field guidance of loco-motion, and perhaps also for the illusions of vection. Indeed,we observed in unpublished experiments that when balancedsymmetrical stimuli are delivered along the same axis, for ex-ample, inwardly pairs of stimuli moving along the horizontalmeridian, they may together evoke no PVN response at all,when either alone evokes a vigorous one: a null detectormechanism for signaling symmetrical flow on either side ofthe head during linear advance.

Steinmetz and Constantinidas describe, in their article onpp 448-456 of this issue, the results of an ingenious experi-ment in which they have been able to dissociate under well-controlled conditions the line of gaze and the line of atten-tion. Their result is that the central suppression and facilita-tory surround are anchored to the line of attention, not thatof gaze.

It is obvious from their huge receptive fields that any singlePVN can provide only a very inexact signal of a stimulus mov-ing across the visual field periphery. This is shown by theanalysis of Figure 8, which reveals the neat fit to the sinefunction of the intensity of responses to stimuli moving alongdifferent radial axes. This allows one to define a best directionfor such a neuron along a preferred radial axis, but showsalso what an imprecise signal it is, for stimuli moving alongaxes at 90° on either side of the best direction evoked re-sponses at 50% of that evoked by the stimulus at best direc-tion. We therefore applied to the population of PVNs the vec-tor summation analysis devised by K. O. Johnson, with theresult shown in Figure 9. There is no evidence at all that sucha summation is carried out in the cerebral cortex, but theanalysis shows that a very precise signal for direction couldbe extracted from a population of imprecise elements. Howprecise that might be is shown by the graph of Figure 10(Steinmetz et al., 1987).

We found in our earliest experiments that the angle of gazeinfluenced in a powerful way the fixation, tracking, and sac-cade cells of the inferior parietal lobule. Andersen and I dis-covered that this is true also for PVNs (Fig. 11; (Andersen andMountcastle, 1983). Andersen has exploited further the angleof gaze effect, and described in a number of important reportsthe results of several experiments made in the lateral intra-

Cerebral Cortex Scp/Oct 1995, V 5 N 5 387

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Figure 11. The experimental arrangement and the effect of the angle of gaze upon the responses of a parietal visual neuron to light stimuli. The monkey fixated a small target lightplaced at a series of positions on the tangent screen, with head fixed. The results obtained at two fixation positions are showa At each a 6° x 6° test stimulus of 1 sec durationwas flashed 10° above the fixation point as the monkey attentively fixated the target light to detect its dimming. Tests at different spatial positions interleaved randomly in a singlerun. Impulse replicas are shown be/owthe screen. Each line represents a single trial; each small upstroke, the instant of impulse discharge. Impulse replicas and histogram to theright show the intense response evoked during fixations 20° down and 20° to the left; those to the left, the responses with fixation 20° right 20° up. Dotted lines above histogrambins, SE of the means. Diamonds below corresponding bins of the two histograms indicate that a significant difference exists between the means of those bins (p < 0.05). Timemarts, 100 msec; divisions on ordinates, 10 impulses/sec. Reprinted with permission, from Andersen and Mwirrtcastie (1SS3).

The Parietal System and Some Higher Brain Functions • Mountcastle

parietal area (UP), which occupies the upper part of the pos-terior bank of the intraparietal sulcus. This area is designatedby Andersen as one specialized for saccadic eye movement,for 63% of the cells he observed there are saccade related.The results of these experiments are reviewed in his articleon pp 457-469 of this issue of Cerebral Cortex. Andersen'sgeneral hypothesis is consonant with classical ideas about thefunction of the parietal lobe system, that it forms a neuralimage of surrounding space. The central theme is that thisrepresentation is constructed from visual and eye positionsignals and, it is conjectured, from auditory, vestibular, andproprioceptive signals as well. Andersen and his colleaguespresent evidence that the visual and eye position signals arecombined to form "planar gain fields" that compose a popu-lation code for localizing visual targets in orbital coordinates.This initial coordinate transform is thought to be combinedwith others for converting it to a body-centered frame. An-dersen has enlarged this general hypothesis to include theconcept that the parietal system is part of an essential sen-sory-motor interface dealing with intentions, an idea that fitswith Sakata's results, as well as with those of Lacquaniti andCaminiti.

The problem of spatial constancy is a vexed one of longstanding in visual science. Many investigators, like Andersen,follow the idea that the stability of the visual world seenthrough constantly moving eyes depends upon a series ofcoordinate transforms from retinal to orbital to body space,and so on. Colby et al. present, in their article on pp 470-481of this issue, evidence they believe supports quite a differenthypothesis, that each saccadic movement of the eyes evokesconcurrently a rotation of the central representation of thevisual field, so that objects within it remain in a constant spa-tial position relative to head and body. That is, in their ownwords, that "stored visual information is remapped in con-junction with saccades. Remapping of the memory tracemaintains the alignment between the current image on theretina and the stored representation in cortex." This is a noveland interesting idea that deserves continued study. It is rem-iniscent of the old observation that a voluntary effort to movethe eyes in the direction of a paralyzed extraocular muscleevokes a transient rotation of the visual field. How this generalarea of study will play out is still uncertain, but it will certainlyprovide fruitful opportunities for future research.

This problem of spatial constancy and the associated oneof coordinate transformation both here and in the motorsphere are among the most difficult of the many difficultproblems in the study of the neocortical mechanisms in thehigher functions. Progress has been slow, particularly, I be-lieve, because of the complexity and diversity of the neuronaloperations that have been observed in the posterior parietalcortex. How to sort them out and how to put them togetherin a coherent and generalized scheme have, up to now, beenimpossible. Some investigators take the position that the in-ferior parietal lobule is divided into a large number of rela-tively small and independent cortical areas, each specializedfor a particular mode of neuronal processing, and each exert-ing its influence upon behavior via its own particvilar set ofextrinsic connections. Indeed, some evidence supports thisview, but other evidence does not.

A major conceptual problem is what is to be called visual,if as is customary we define as visual something directly in-volved in the perception of seen objects. How, then, shouldwe designate the large number of other cortically controlledoperations in which light ("visual") stimuli play an importantbut perhaps not a singular role. For example, the largely un-conscious "visual* guidance of the arm during the transportphase of reaching. I first encountered this problem when Iobserved reach neurons indiscriminantly brought to action by

either somesthetic or visual stimuli. And, Andersen (pp 457-469 in this issue) has now made a similar observation, thatparietal saccade neurons may be activated by either visual orauditory stimuli. This led him to the concept of the role ofthe parietal cortex in intentional operations, an idea withwhich I heartily agree. Intentionality leads, conditionally, towhat I originally called the command function of the parietalsystem, command regarded here as something more generalthan impulses in motoneurons, or motor cortical cells of ori-gin of the pyramidal tract! This brings to mind the old obser-vation that in a distributed system command may reside fromtime to time in different nodes of the system, and at any onetime in the node with the most and the most urgent infor-mation.

NotesCorrespondence should be addressed to Dr. Vernon B. Mountcastle,Krieger Mind/Brain Institute, Johns Hopkins University, Krieger Hall,Room 347, Charles and 34th Streets, Baltimore, MD 21218.

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The Pirietal System and Some Higher Brain Functions • Mountcastle