gaze during visually-guided locomotion in...

Research report

Gaze during visually-guided locomotion in cats

Garth A. Fowler *, Helen Sherk

Department of Biological Structure, University of Washington, Seattle, WA 98195, USA

Received 2 January 2002; received in revised form 25 March 2002; accepted 25 March 2002

Abstract

Visual guidance is often critical during locomotion. To understand how the visual system performs this function it is necessary to

know what pattern of retinal image motion neurons experience. If a locomoting observer maintains an angle of gaze that is constant

relative to his body, retinal image motion will resemble Gibson’s (The Perception of the Visual World (1950)) well-known optic flow

field. However, if a moving observer fixates and tracks a stationary feature of the environment, or shifts his gaze, retinal motion will

be quite different. We have investigated gaze in cats during visually-guided locomotion. Because cats generally maintain their eyes

centered in the orbits, their gaze can be monitored with reasonable accuracy by monitoring head position. Using a digital

videocamera, we recorded head position in cats as they walked down a cluttered alley. For much of the time, cats maintained a

downward angle of gaze that was constant relative to their body coordinates; these episodes averaged 240 ms in duration and

occupied 48�/71% of the total trial time. Constant gaze episodes were separated by gaze shifts, which often coincided with blinks.

Only rarely did we observe instances when cats appeared to fixate and track stationary features of the alley. We hypothesize that

walking cats acquire visual information primarily during episodes of constant gaze, when retinal image motion resembles Gibson’s

conventional optic flow field.

# 2002 Elsevier Science B.V. All rights reserved.

Keywords: Cat; Vision; Gaze; Locomotion; Visually-guided; Optic flow; Retinal image motion

1. Introduction

How does the visual system use information for

guidance during locomotion? To answer this question,

one needs to describe the pattern of retinal image

motion that occurs during locomotion. Helmholtz [13]

and subsequent investigators (e.g. Gibson, [9]; Koender-

ink, [15]) have described the image motion that is

generated by an observer’s motion through the environ-

ment: elements move approximately radially outward

from the heading point, expanding and accelerating as

they go (see Fig. 1A, the cross indicates the heading

point). However, the pattern of retinal image motion

may be quite different because of various gaze strategies

employed by the observer [23,26]. Fig. 1B shows the

motion of images seen by a walking observer who fixates

and tracks a stationary feature of the environment to the

left of his heading point. If the same observer instead

shifts his gaze to the left while walking during the gaze

shift he will experience a pattern of retinal image motion

like that in Fig. 1C.

In order to understand visual processing during

locomotion, we need to know what pattern of motion

neurons actually see. This is a challenging proposition

because it requires gaze to be monitored in a locomoting

subject. In stationary subjects, Robinson’s [25] magnetic

coil method for measuring eye position has been highly

successful, and has been refined and extended to

assessment of head position by Collewijn et al. [2,3].

But this method does not work on subjects who

locomote from one point to another, because they

quickly move out of the magnetic field. Solomon and

Cohen [27] have applied the magnetic coil method to

tethered monkeys that are walking or running in a circle,

but this paradigm cannot tell us about gaze during

visually-guided locomotion.

We have taken another approach to the problem of

gaze measurement in locomoting cats. Although it seems

natural to monitor gaze by measuring eye position, in

* Corresponding author. Tel.: �/1-206-543-1861; fax: �/1-206-543-

1524.

E-mail address: [email protected] (G.A. Fowler).

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the cat one can assess gaze with moderate accuracy by

looking at head position only. Cats can deviate their

eyes up to �/258 in the orbits [31,32], but such

deviations are brief. Guitton et al. [10] found that,

except during gaze shifts, cats maintain their eyes within

28 of the center of the orbits. They also noted that even

small gaze shifts include movement of the head as well

as the eyes. With the advent of digital VCs, it has

become possible to record head position in a locomoting

cat without attaching any sensors to the animal, and this

is the approach that we have taken. In this paper, we will

use the term gaze when the cat’s gaze was inferred from

static head position. We will avoid this usage when the

cat’s head was moving, and the linkage between gaze

and head position is less certain.

During locomotion, the importance of vision may

vary depending upon the environment. Walking across

an empty room or across an open field presents almost

no visual challenge, but picking one’s way across a

cluttered floor or up a rocky mountain trail requires

much more continuous visual attention. It is the latter

situation that we wished to simulate, and so we have

monitored gaze in cats that were walking down an alley

that was densely cluttered with small objects (Fig. 2).

We found that cats performing this task spent most of

their time with their gaze fixed relative to their bodies

(or heading points), so that the pattern of retinal image

motion resembled the relatively simple optic flow field

of Fig. 1A. But these episodes of constant gaze were

usually rather short, with cats making frequent gaze

Fig. 1. Patterns of retinal optic flow generated by locomotion along a

straight path. The simulated cat had an eye height of 18 cm and moved

at 80 cm/s, heading towards the cross. Vectors show the motion of

objects lying on a ground plane that extends 904 cm in front of the cat,

with each black spot indicating an object’s position after 67 ms of

motion. (A) Optic flow seen when the cat maintained a constant angle

of gaze relative to its heading. (B) Optic flow seen when the cat fixated

and tracked a stationary object 28 cm to the left of its path, and 70 cm

ahead (square). (C) Optic flow seen when the cat shifted its gaze to the

left at 508/s.

Fig. 2. Test alley, viewed from outside the exit end. Black objects can

be seen scattered across the alley floor. The cat’s speed was monitored

with photosensors, P1, P2, and P3, and gaze was monitored with a

digital VC directed down the first leg of the alley.

G.A. Fowler, H. Sherk / Behavioural Brain Research 139 (2003) 83�/9684

shifts. Their directions of gaze clustered near their mid-

sagittal planes and were angled downward. Only rarely

did walking cats fixate and track stationary features.

Some of these data have been published in abstractform [8].

2. Methods

2.1. General procedure

Six adult cats, five female and one male, were used in

this study. All methods were approved by the AnimalCare Committee of the University of Washington, and

conformed to NIH guidelines.

Cats were trained to walk down an L-shaped alley

whose floor was cluttered with small objects, typically

there were 44 objects in the first leg (Fig. 2). These were

irregularly shaped pieces of cardboard, about 3�/7 cm2,

on which were glued slices of PCV tubing, 0.8 cm in

height. With practice, cats learned to avoid stepping onthese objects. Because the locations of objects varied

randomly from trial to trial, cats relied on vision for

accurate foot placement [29]. Cats’ accuracy was

assessed by looking at the impressions left by their feet

in the sand that covered the alley floor. When the cat

stepped on an object, it indented the sand, or sometimes

was shifted out of position. In our analysis of gaze

during locomotion, we considered only trials in whichthe cat made 0 or 1 error in the first leg of the alley (the

great majority of trials analyzed had no errors). Since by

chance we would expect 4�/5 errors in this leg of the alley

[29], an error-free run indicated that the cat’s attention

was focused on the task. Visual distractions inside the

alley were minimal. The alley had blank white walls,

interrupted by fixed features that included vertical

struts, a fluorescent light, photosensors and bicyclereflectors. Practiced cats paid not evident attention to

these features.

Cats were initially taught to traverse the alley by

feeding them with canned tuna fish. One animal was

rewarded in this fashion on all subsequent trials, but the

other cats were thereafter rewarded only with petting.

No cat was food-deprived. Cats were free to move at

their own pace, and were rewarded regardless of thenumber of errors made. However, all cats became

increasingly skilled at avoiding stepping on objects,

suggesting that this is a natural behavior [29]. The

amount of practice required to reach a stable level of

performance varied from cat to cat, ranging from 30 to

190 days.

To assess gaze, we videotaped the cat as it walked

down the first leg of the alley, directly toward thevideocamera (VC in Fig. 2). For the first two cats

studied (Brie and Cheddar), we used a digital VC with a

frame rate of 30 Hz and a resolution of 720�/480 pixels,

interlaced (Canon ZR). For the other four cats, a similar

VC (Canon Elura) was used; it was capable of non-

interlaced image capture, thus doubling the effective

vertical resolution. The image quality obtained in thesevideotapes is illustrated in Fig. 3 and Fig. 6.

Out of a large number of trials (472 total), we chose

for analysis 10�/18/cat, based primarily on image

quality. The VC’s automatic zoom did not always

maintain the image in sharp focus, and we selected

only videotapes that showed excellent focus throughout.

However, the chief limitation on the size of the data set

was the amount of time required for the analysis.Videotaped images were downloaded to a computer

using PhotoDV (Digital Origin) and analyzed frame by

frame using Adobe Photoshop. In addition, movies were

reconstructed from captured frames using QuickTime

(Apple Computer, Inc.), and these movies were viewed

in slow motion or frame by frame to look for rapid eye

movements. We could not accurately measure eye

position but we could detect saccades. In the gazecalibration procedure described in the next section, in

which cats made gaze changes of known size, we found

that we could readily detect saccades as small as 3.58.Although we could not measure the size of saccades in

locomoting cats, we could use them to determine the

beginning or end of some episodes of constant gaze.

2.2. Measurement of head azimuth

We measured head azimuth and elevation, usually in

alternate frames, but sometimes in every frame when the

head was turning rapidly. Azimuth was found by taking

the ratio of the distances illustrated in Fig. 3A, that is,

from the temporal corner of the left eye to the left edge

of the head, and from the corner of the right eye to the

right edge of the head. To determine head azimuth fromthis ratio, we used a look-up table that was compiled

from measurements made in videotaped frames of

stationary cats that were fixating at known locations.

In this procedure, the cat sat in one investigator’s lap

with its head directly in line with the VC. In front of the

cat was a horizontal board with small holes at positions

corresponding to particular locations in the cat’s body

coordinate system (for example, 108 to the left and 108inferior). The cat fixated on the tip of a pipecleaner that

emerged, wiggling, from one hole. We found that cats

fixated repeatedly and reliably in this situation. Fifteen

different locations, 58 apart, were tested. Two cats were

used (Jack and Kraft), and we videotaped 256 fixations.

Repeated fixations at a given location yielded very

similar images (e.g. Fig. 3B), and values found for the

two cats were also quite similar. Close to the mid-sagittal plane, gaze was measured to within 9/18 of the

same value on repeated trials, while at 208 of azimuth,

repeatability was 9/28.

G.A. Fowler, H. Sherk / Behavioural Brain Research 139 (2003) 83�/96 85

2.3. Measurement of head elevation

Head elevation was measured by taking a ratio of two

distances: muzzle length (M ) (from the lower edge of the

eye to the point of the nose), and chin length (C ) (from

the point of the nose to the bottom of the chin) (Fig.

3C). For every cat we found the ratio C /(C�/M) that

corresponded to a horizontal gaze by videotaping the

cat from the side while it fixated an object that was at

eye height (Fig. 3D). This image was imported into

Adobe Illustrator and rotated in 58 increments, and M

and C were measured at each position. A linear

equation was found using these values that related

head elevation to the ratio C /(C�/M ). Equations varied

somewhat from one cat to another because of individual

variation in the lengths of muzzle and chin.

2.4. Predicted retinal image motion

When the walking cat’s gaze was constant relative to

its body, as occurred for much of the time during each

trial, we could determine the speed and trajectory of

images that corresponded to objects on the alley floor as

they passed through the center of the cat’s visual field.

The variables required for this calculation are (1) thewalking speed of the cat (measured using the photo-

sensors shown in Fig. 2); (2) the height of the cat’s eyes

above the alley floor (measured from the videotaped

Fig. 3. Measurement of head azimuth and elevation. (A) Azimuth was found by taking a ratio of the horizontal distances from the outer margin of

each eye to the edge of the head. (B) Four different fixations by one cat at a location with azimuth�/158 and elevation�/�/158 in the cat’s body

coordinates. (C) Front view showing the distances M and C as they were measured for the calculation of elevation. (D) Side view of cat fixating on a

point at eye level, also showing M and C .


image after taking into account the cat’s distance from

the camera); (3) the angle of gaze relative to the cat’s

heading direction (head azimuth and elevation). These

data were entered into a program that computed thespeed, azimuth, and elevation, in the cat’s visual field, of

an image passing through the center of gaze. These

variables were of interest for determining the expected

trajectory of the cat’s gaze if, instead of maintaining a

constant gaze angle, it tracked the image.

3. Results

All cats showed broadly similar patterns of gaze asthey walked down the alley. The examples in Fig. 4

illustrate the most common features of gaze that we

observed. (1) During every trial, there were several

intervals during which head azimuth was constant

(defined as a variation of 38 or less throughout the

interval). In Fig. 4, azimuth during these constant gaze

episodes (CGEs) is plotted using open circles. (2) CGEs

were separated from each other by either a gaze shift, a

blink (vertical lines indicate frames in which the cat’s

eyes were closed), or both. (3) Some gaze shifts

culminated in a brief glance to one side or the other,

followed by an immediate shift back towards the midline

(see arrow in Fig. 4D). (4) Head elevation was often

more variable than azimuth, and commonly oscillated in

time with the cat’s footfalls. At such low frequencies (�/

2�/3 Hz), the cat’s VOR is capable of fully compensating

for vertical head oscillation [5,6], and thus it seems likely

that counter-rotation of the eyes compensated for these

movements.

CGEs occupied the greatest amount of time, on

average 48�/71% of each trial (Fig. 5). Cats spent the

remainder of the time either shifting their gaze or closing

Fig. 4. Head azimuth and elevation, in degrees, during 4 trials by 4 different cats. When gaze was constant (that is, with azimuth maintained within

1.58 of the mean for the CGE), data points are marked with open circles. During gaze shifts, data points are marked with filled circles. In the azimuth

plots, points above 0 indicate head rotation to the left, and points below 0 indicate head rotation to the right. Cats turned their heads to the right at

the end of each record because they anticipated the right turn into the second leg of the alley. Vertical lines mark videotape frames in which the cat’s

eyes were closed (blinks).


their eyes. Although we had thought that they might

sometimes fixate and track stationary objects in the

alley, we rarely found evidence of such behavior (seebelow).

3.1. Constant gaze episodes

Every trial included several CGEs, typically about 5/

trial in the first leg of the alley, giving an averagefrequency of 2.5/s (Table 1). Fig. 6 illustrates the

constancy of gaze during 3 such episodes; in each case,

head azimuths were within 18 of each other in the first

and last frames of the CGE. CGE duration varied

considerably, from 67 ms (the briefest CGE that we

could identify) to 1000 ms, and averaged 247 ms (Fig. 7).

There was some cat-to-cat variability: Brie and Jack, for

example, tended to have prolonged CGEs.It is possible that we under-estimated the duration of

some CGEs because we over-estimated the duration of

the preceding gaze shift. If the cat combined a head

movement with a saccade, the saccade might bring gaze

to its final position before the head had finished moving,

resulting in an interval when the head continued to

move but the gaze was fixed because the eyes counter-

rotated [10,11]. However, this potential problem doesnot arise for a CGE that immediately follows a blink,

since the CGE cannot start until the cat opens its eyes.

We thus assumed that the durations of CGEs following

blinks were accurately measured, and compared them to

the durations of other CGEs. There was no difference in

the durations of CGEs that followed blinks compared to

those that did not follow blinks, suggesting that we had

not substantially under-estimated CGE duration.

During CGEs, the cat’s gaze was almost always

directed downward, and tended to remain close to its

midline. Fig. 8 shows gaze during CGEs in a coordinate

system that was centered on the cat’s heading point.

Open circles show episodes in which the center of gaze

would have fallen on the alley floor, and filled circles

show episodes in which gaze would have fallen on the

alley walls. All cats looked at the floor most of the time,

with a gaze angle on average 198 below the horizon

(Table 1). We speculated that CGEs might be longer

when gaze was close to the cat’s anticipated path than

when gaze was eccentric, but found only weak support

for this hypothesis. For one cat (Kraft) there was a slight

but significant tendency for more eccentric CGEs to be

briefer, but for the other cats duration and azimuth were

uncorrelated.

One might ask where walking cats typically looked in

physical space*/how far ahead, and how close to their

intended path. These locations are shown in Fig. 9 for

all CGEs in which gaze fell on the alley floor. Cats never

looked directly downward, but instead looked at points

on average 58 cm ahead (see ‘distance ahead’ in Table

1). Given a stride length of �/19 cm, cats were thus

Fig. 5. Time spent by each cat in different gaze behaviors while walking down the alley. CGEs dominated the behavior of all cats. The number of

trials analyzed for each cat is given as n .

Table 1

Cat CGEs/s Average CGE azimuth (8) Average CGE elevation (8) Average distance ahead (cm)

Brie 2.16 3.5 right �17.4 69.7

Cheddar 3.08 0.8 right �22.3 50.0

Gouda 2.60 1.8 left �16.9 69.0

Jack 2.28 3.5 right �20.6 51.0

Kraft 2.57 1.9 right �17.2 62.0

Leaf 2.25 3.7 left �22.0 47.0

Average 2.49 0.8 right �19.4 58.12


looking at points about 3 steps beyond their current foot

placement. Gaze strategies varied somewhat between

cats. Jack and Leaf focused their gaze over a rather

narrow range of distances ahead, so that their standard

deviations were only 9 cm, while Gouda and Kraft had

standard deviations that were twice as great.

If gaze is constant relative to the body, as during a

CGE, images move through the visual field in the optic

flow pattern shown in Fig. 1A. It was thus possible to

calculate the speed of images passing through the area

centralis during CGEs, and these speeds are shown for

each cat in Fig. 10. The most critical determinant of

image speed was the cat’s angle of gaze*/cats that

tended to look steeply downward experienced relatively

rapid image motion, and cats that maintained a less

steep angle of gaze experienced slower motion. Image

speeds were generally modest, averaging 158/s and rarely

exceeding 258/s for most cats.

3.2. Gaze changes

Between CGEs cats usually shifted their gaze. Gaze

shifts were moderate in size, with the vast majority being

less than 108 (Fig. 11A). Cats sometimes made a brief

but large gaze shift, usually to the left or right, which we

refer to as a glance. Glances were generally substantially

larger than gaze shifts between CGEs (compare histo-

gram in Fig. 11B with those in Fig. 11A). Fig. 4D shows

a 208 glance to the left. Cats varied in the frequency of

glances, from 0.9/trial (Leaf) to 0/trial (Cheddar) on

average.

Fig. 6. The first and last frames of typical CGEs for 3 different cats.

The time shown is that elapsed between the two frames. In each case,

the difference in head azimuth between the two frames was no greater

than 18.

Fig. 7. Durations of CGEs for each cat. Arrowheads indicate average

values.


3.3. Fixation and tracking

Do locomoting cats fixate and track static features of

the environment? If a cat fixated a feature while walking

down the alley, its gaze would rotate smoothly relative

to its own body (a behavior that we shall refer to as

‘tracking’). Tracking might have occurred during either

presumptive CGEs or during gaze shifts. During brief

CGEs we could not rule out this possibility since the

magnitude of gaze rotation that would occur during

tracking would be small. During longer CGEs, however,

the head rotation predicted during tracking would be

large enough to observe. We therefore identified all

CGEs that were long enough that gaze would shift by 58or more if the cat started tracking at the beginning of the

CGE, and for which tracking speed would be at least

108/sec, which is beyond the limit for smooth eye pursuit

by the cat (see Section 4). For each of 63 such CGEs we

calculated the head trajectory that would be predicted if

the cat were tracking rather than maintaining a constant

gaze (see Section 2). The match between predicted and

actual gaze trajectories is moderately good in Fig. 12A

and B, and somewhat less so in Fig. 12C. The remaining

plots (Fig. 12D�/L) are typical of the other 60 CGEs,

none of which showed a match. Thus fixation and

tracking during presumptive CGEs appeared to be rare.

Tracking might be more likely to occur during gaze

shifts than during CGEs. Although we observed a large

number of gaze shifts, blinks coincided with many (see

below), effectively precluding tracking. There were 223

gaze changes that were free of blinks and long enough to

compare to trajectories predicted by a tracking hypoth-

esis. In 179 cases the cat’s head moved in a direction

opposite to that predicted. In the remaining instances,

the head moved in the predicted direction, but not at the

predicted rate (usually it moved too fast). Thus none of

the gaze changes that we observed could be interpreted

as a tracking episode.

Fig. 8. Location of gaze during CGEs for each cat, plotted in a body-centered coordinate system. Azimuth and elevation are given in degrees. When

gaze would have fallen on the alley’s wall rather than on the floor, the corresponding circle is shaded.


3.4. Blinks

All cats blinked from time to time while walking down

the alley. Blinks could be brief, visible in only a single

videotaped frame, but more commonly lasted 100 ms or

more (Fig. 13). The frequency of blinks, and the total

amount of time spent with the eyes closed, varied

considerably among cats. Kraft and Leaf each spent

17% of the time with their eyes closed, while Jack, at the

other extreme, spent only 2% of the time blinking (Fig.

5).Blinks occurred most commonly during gaze shifts. In

the sample as a whole, 85% of blinks coincided with gaze

shifts, a pattern that is clear in the examples of Fig. 4.

Less commonly, a blink occurred in the middle of what

would otherwise be a single CGE (see, for example, the

blinks in Fig. 4C).

The high incidence of blinks during many trials

surprised us, and we wondered whether stationary cats

that were actively fixating visual targets blinked equally

frequently. We counted blinks made during the gaze

calibration task, in which the cat sat still and looked at a

wiggling pipecleaner (see Section 2). Both cats tested in

this fashion blinked very rarely when stationary. Jack

exhibited 0.018 blinks/s when stationary, compared to

0.16 blinks/s when walking. Kraft exhibited 0.035

blinks/s when stationary, compared to 1.31 blinks/s

when walking.

4. Discussion

The primary goal of this study was to determine what

pattern of retinal image motion locomoting cats experi-

ence. We found that, like stationary observers, cats

displayed many short episodes of constant gaze that

were separated by gaze shifts. During these CGEs,

images would have moved through the visual field in a

pattern approximating a Gibsonian optic flow field (Fig.

1A). Because cats almost always looked downward,

their fixation points did not coincide with the focus of

expansion, and thus even at the center of the area

centralis they saw image motion.

Fig. 9. Location of gaze during CGEs, plotted in physical space.

Ordinate plots distance in cm to the left or right of the cat’s mid-

sagittal plane. Only episodes in which gaze fell on the floor of the alley

are shown.

Fig. 10. Retinal image speeds during CGEs in which gaze fell on the

alley floor. Arrowheads indicate average values.


4.1. Methodological considerations

Because conventional methods for monitoring eye

and head movements are not feasible for locomoting

observers, we have used a novel method to assess gaze.

When a cat fixates, head position indicates the direction

of gaze within about 28 because cats maintain their eyes

centered in the orbits, or nearly so [10]. During gaze

shifts, however, gaze does not necessarily coincide with

head position because cats may combine a saccade witha head rotation. We could detect fairly small saccades

(see Section 2) but we could not measure their size; thus

although we could describe the direction of gaze shifts,

we could not describe gaze trajectory during the shift.

As noted above, without knowing the size of such

saccades we might have over-estimated the duration of

associated gaze shifts, and consequently under-esti-

mated the duration of subsequent CGEs. However,when we compared potentially under-estimated CGEs

with ones whose starting times were unambiguous

because they immediately followed blinks, we found

no difference between the two groups.

The temporal resolution of our method was limited by

the VC’s frame rate, which was 30 Hz. Although modest

compared to the temporal resolution of magnetic coil

systems, this resolution was quite adequate for measur-ing the duration of gaze events (CGE’s, blinks, and gaze

shifts), since these events lasted at least 33 ms.

4.2. Constant gaze episodes

The most common gaze event that we observed was

the CGE. In duration and frequency, these resembled

the fixations exhibited by a stationary, unrestrained cat

in a study done by Collewijn [2]. Collewijn’s stationarycat made about 2.7 fixations/s, and our cats averaged 2.5

CGEs/s. The average fixation duration for the station-

ary cat was �/303 ms, and for our locomoting cats,

CGEs averaged 247 ms. In humans, the duration of

fixations depends on the task [12]: during reading

English text, for example, fixation durations generally

average 250 ms [28], and during free viewing of a

painting they averaged �/400 ms [35].It is generally assumed that stationary observers

acquire visual information primarily during fixations,

and it seems likely that our cats likewise obtained

information primarily during CGEs and not during

gaze shifts. In many cases this must have been true

because the cat closed its eyes during the gaze shift.

Similarly, Orchard and Stern [20] observed that humans

tend to concentrate their blinks during saccades ratherthan fixations when reading. Cats’ blinks during gaze

changes might serve the same function as saccadic

suppression, which decreases visual sensitivity during

rapid eye movements [34].

The conclusion that cats acquired information pri-

marily during CGEs implies that they ignored visual

cues during about 40% of each trial (the time occupied

by gaze shifts and blinks). Although 40% seems like asurprisingly large amount of time during which to

exclude visual information, this outcome is consistent

with percentages found by Patla et al. [21]. Their human

Fig. 11. Sizes of gaze changes (A), and of glances (B). Arrowheads

indicate average size of gaze change for each cat. Glance sizes were

pooled for all cats because they were too infrequent to show

individually.


subjects, who were fitted with liquid crystal goggles,

blocked out visual information for 60% or more of the

time while performing a visually-demanding walking

task (placing their feet on ‘stepping-stones’). This

parsimonious strategy was sufficient to produce a high

level of performance, just as our cats’ gaze strategy

sufficed for accurate foot placement in a difficult task.

During a CGE, the pattern of retinal image motion

presumably resembled the well-known optic flow field

illustrated in Fig. 1A. But locomoting cats did not keep

their gaze centered on their heading point, as has

sometimes been assumed (e.g. [1,24]). Instead, they

looked downward at the path ahead of them. The

average downward angle of gaze, 198 below the horizon,

Fig. 12. Examples of actual CGEs, and of gaze azimuth and elevation predicted if the cat had fixated and tracked the point on the alley floor where

its gaze fell at the beginning of the CGE. Actual values are indicated by filled circles, and predicted values are indicated by shaded circles. The best

matches are the first 3 examples (A)�/(C).


placed gaze 58 cm ahead of the cat’s eyes. At a walking

speed of 43 cm/s (the average for cats in this study), the

cat would step on this location 1.3 s (or about 3 steps)

after its image crossed the center of gaze.

A strategy of maintaining a constant angle of gaze

during locomotion has both advantages and disadvan-

tages. A constant gaze yields a predictable, stereotyped

pattern of retinal image motion (the optic flow field of

Fig. 1A), but it also results in continuous image motion

across the center of gaze. Rapid image motion would

make precise visual analysis difficult. Typically, how-

ever, when cats looked at the alley floor, images movedat modest speeds through the area centralis, on average

158/s. The image speeds that we observed during CGEs

would strongly activate many cells in several areas of

visual cortex, including areas 17 [18], 18 [19], and the

lateral suprasylvian visual area ([30]; unpub. observ.).

Indeed, retinal image motion appears to be not only

consistent with visual analysis during locomotion, but

also necessary for accurate foot placement, since elim-ination of retinal image motion by the use of strobe light

has devastating effects on accuracy in this task [29].

Walking cats sometimes glanced to one side or the

other (and occasionally downward). Glances might be

considered to be particularly brief instances of CGEs,

but they were generally much more eccentric than CGEs

(Fig. 10). In some cats they were also more stereotyped.

One cat habitually glanced far to the right as sheemerged from the start box, and another usually glanced

to the left just before turning the corner of the L-shaped

alley. Patterns of constant gaze, in contrast, varied

unpredictably from trial to trial.

4.3. Tracking during locomotion

Do cats sometimes fixate and track stationary fea-

tures in the alley while walking? One might at first think

such behavior unlikely since previous studies have

shown that cats with immobilized heads use smooth

pursuit eye movements to track only slowly moving

targets (2�/68/s at most; [4,7], Malpeli, pers. commun.see, however, [17]), much slower than the image motion

that our locomoting cats typically experienced (Fig. 10).

However, smooth pursuit gaze movements, in which a

cat is free to move its head, have not been investigated.

We have found that stationary, unrestrained cats use

head movements to track a moving object such as a

bouncing ball1 (Sherk and Fowler unpub. observ.), and

thus walking cats should be quite capable of trackingstationary features. Another line of evidence points to

the same conclusion: when a patterned drum rotates

around a head-fixed cat, the drum elicits an optokinetic

response in which the cat’s eyes track the pattern with

speeds up to �/308/s, though with a gain substantially

less than one at moderate or high speeds [7,33]. But even

though walking cats appear capable of tracking static

features, we found very little evidence that they did so inthe alley task. Like cats tracking bouncing balls, walking

cats would presumably employ head movements, but

head trajectories rarely matched those predicted by the

Fig. 13. Durations of blinks for each cat.

1 In unrestrained monkeys, the head also contributes most of the

motion during smooth pursuit [16].


cat’s direction of gaze and walking speed. Two caveats

should be mentioned. First, we only compared predicted

and actual head trajectories when the total predicted

head movement was at least 58, which excluded most

CGEs because of their brevity. However, there is no

reason to suppose that shorter CGEs differ from longer

ones in any way except duration, and thus the absence of

tracking during longer episodes suggests that cats did

not track during shorter ones either. Second, we

assumed that cats would track stationary objects with

a gain of one. If their gain was substantially lower, we

might well have missed tracking episodes. Cats follow-

ing such a strategy would see a pattern of image motion

intermediate between conventional optic flow (Fig. 1A),

and ‘tracking’ optic flow (Fig. 1B). Although possible,

this strategy would fail to provide the benefits of either

constant gaze, which yields a stereotyped and thus

predictable pattern of motion, or of fixation and

tracking, which minimizes image motion in the area

centralis.In two studies on visually-guided human locomotion,

investigators concluded that humans frequently fixate

and track stationary features [14,22]. This conclusion

must be considered tentative, since these studies mea-

sured eye movements (in one case, only horizontal eye

movements) but not head position. Assuming that

humans do fixate and track in these situations, does

this indicate a difference from the cat? Not necessarily,

since both of the tasks employed in the human studies

may have promoted a fixation and tracking strategy. In

one study subjects had to place their feet on small,

irregularly-spaced stepping-stones, which apparently

resulted in fixation of each stepping-stone until the

foot had touched it. As readers will know from their

own experience, this is not a normal visual guidance

strategy; one rarely looks at one’s foot as it makes

contact with the substrate. In the other study, subjects

had to step over a solitary barrier. Although not visually

complex, this latter situation may have prompted

fixation on the barrier because it was the only object

present. Interestingly, in this study subjects also spent

about 33% of their time in CGEs (events termed by the

authors ‘travel fixations’ [22]). Thus there are similarities

as well as differences between the gaze strategies

employed by humans and cats during locomotion.

Possibly the differences between the studies reflect

differences in the tasks used more than a fundamental

difference between species.

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