1990 - C D Gilbert - Theinfluenceofcontextualstimuliontheorientationsel[Retrieved-2016!01!15]

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Vidm Ru. Vol. 30,No. Il. pp.

16894701, 1990

Printed

n Great Britain. All rights rcaerd

0042-6989/903.00 0.00

w Ymt0~~perpmon~pl c

THE INFLUENCE OF CONTEXTUAL STIMULI ON THE

ORIENTATION SELECTIVITY OF CELLS IN PRIMARY

VISUAL CORTEX OF THE CAT

CHARLES . GILBERTand TORSTENN. WIFSEL

The Rockefeller University, 1230 York Ave, New York, NY 10021, U.S.A.

(Received 10 Augwt 1989; in revi sed orm 10 January 1990)

Abatrae-Perception of a visual attribute, such as orientation, is strongly dependent on the context within

which a feature is presented, such as that seen in the tilt illusion. The possibility that the neurophysiological

basis for this phenomenon may be manifest at the level of cells in striate cortex is suggested by anatomical

and physiological observations of orientation dependent long range horizontal connections which relate

disparate points in the visual field. This study explores the dependency of the functional properties of single

cells on visual context. We observed sevtral influences of the visual field area surrounding cells receptive

5elds on the properties of the receptive 5eld ceoterz inhibition or facilitation dependent on the orientation

of the surround, shifts in orientation preference and changes in the bandwidth of orientation tuning. To

relate these changea to perceptual changes in orientation we modeled a neuronal ensemble encoding

orientation. Our results show that the filter characteristics of striate cortical cells are not nazua14y fixed.

but can be dynamic, changing according to context.

visual

cortex

Chientation selectivity Contextual stimuli

Horizontal connect.ions Tilt illusion

Neuronal ensembles

INTRODUCTION

A common theme to many areas of visual psycho-

physics is that perception of a feature in one

part of the visual field is influenced by the visual

context within which that feature is presented.

This has been an area where Gerald Westheimer

has made an important contribution. Together

with collaborators he has found that perception

of position, depth and orientation can be

altered by the presence of neighboring points or

contours (Westheimer, Shimamura 8t McKee,

1976; Westheimer & McKee, 1977; Butler 8c

Westheimer, 1978; Badcock & Westheimer,

1985; Westheimer, 1986). In the domain of

form, where line orientation plays a major part,

the tilt illusion provides dramatic evidence that

estimation of orientation at a given visual field

locus is dependent on information converging

from widely separated points in the visual field

(Gibson & Radner, 1937; for review see

Howard, 1986). In the current study we have

attempted to look for such influences at the

level of single cells in the cat striate cortex. A

dominant feature of the receptive fields of cells

in primary visual cortex is their orientation

selectivity (Hubel & Wiesel, 1959), so it is

natural to ask whether the influences on orien-

tation perception measured psychophysically

may be seen in striate cortex.

An important aspect of cortical circuitry that

may represent the underlying mechanism for

lateral interactions in the cortex and in the

visual field are the long range horizontal

connections (Gilbert & Wiesel, 1979, 1983;

Rockland & Lund, 1983; Martin & Whitteridge,

1984). Evidence from anatomical and cross-

correlation studies indicates that in the

superficial layers the horizontal connections can

mediate communication between cells with

nonoverlapping receptive fields and similar

orientation preference (Gilbert & Wiesel, 1979;

1989; Tso, Gilbert & Wiesel, 1986). Thus an

individual cell integrates information from a

larger part of the visual field than would be

indicated by the receptive field map. One should

keep in mind, however, that the very concept of

receptive field is stimulus dependent, and the

receptive field map obtained by using a simple

stimulus such as a single oriented bar of light

may be very different from that obtained by

using more complex stimuli. The idea that the

horizontal connections may mediate influences

that are orientation dependent is supported by

the finding that they relate cells with similar

orientation specificity.

1689


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CHARLESD.

GILBERT and TOWN N WIESEL

The current study represents a preliminary

attempt to explore influences outside the recep-

tive field in the domain of orientation. The

results indicate that the functional properties of

individual cells do show contextual sensitivity,

and further suggest that the functional

specificity of a cell is to a degree not necessarily

fixed but can be dynamic, adapting to different

visual environments.

METHODS

We recorded from 65 cells in area 17 of

33 adult cats. The animals were initially

anesthetized with ketamine HCl (10 mg/kg,

i.m.) followed by sodium thiopental (initial dose

20 mg/kg, i.v., supplemented by further injec-

tions as needed). EKG, EEG (through silver

wires implanted between the skull and the dura),

rectal temperature and expired CO2 concen-

tration were constantly monitored. The animal

was intubated with an endotracheal tube, para-

lyzed with succinylcholine (10 mg/kg hr), and

artificially respirated. The stroke rate and the

volume of the respirator was adjusted to yield

4% end-tidal C02. Rectal temperature was

maintained near 38C with a thermostatically

controlled heating pad. During the experiment

sodium thiopental was given i.p. at a rate

suiiicient to produce a slow wave EEG pattern

(l-3 mg/kg hr). The pupils were dilated with 1%

atropine sulfate, and the nictitating membranes

were retracted with 10% phenylephrine. The

refraction of the eye was measured with a

retinoscope and appropriate contact lenses were

used to focus the eyes on a tangent screen 1.5 m

from the animal. The positions of the areae

centrales were back projected onto the screen

with the aid of a fundus camera.

A small hole was drilled in the skull above

the striate cortex, and the dura opened. Single

cell recordings were done with insulated

tungsten microelectrodes (Hubel, 1957) and

were restricted to the superficial layers of the

cortex, in order to sample a more uniform

population of cells.

When a cell was isolated, we mapped the

extent and orientation of the receptive field

using a hand held projector. The orientation

was determined quantitatively with a computer

generated (Adage raster graphics frame buffer

system) bar on a Tektronix 690SR monitor.

Having determined the receptive field character-

istics with a single oriented bar, we then placed

a number of bars surrounding the receptive field

in the arrangement shown in Fig. 1. Using this

arrangement, we could determine the influence

of the surround bars on the response charac-

teristics of the cell. The surround bars did not

activate the cell when presented in isolation, but

they often did modulate the response of the cell

to a bar presented within the receptive field (the

center bar). We determined the dependency

of this modulation on the orientation of the

surround bars and the effect of surround bars

of a given orientation on the tuning of the cell

to the orientation of the center bar. The

cells studied had receptive field located within

5-6 deg of the area centralis, with field size

ranging from 1 to 2 deg in diameter. The length

of the stimulating bars was chosen to approxi-

mate the length of the receptive field of the cell

under study. In most experiments the center and

surround lines were moved in tandem (same

Fig. 1. Stimulus configuration. The dotted line represents the extent of the receptive field center. The lines

in the surround are placed to prevent any one of them from entering the receptive field and activating

the cell. Lines can be placed in the center, surround or both, and moved in tandem to stimulate the cell.

In some instances the center bar is moved and the surround bars are kept stationary.


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influence of contextual stimuli

i6 x

velocity and period), though occasionally the

surround lines were kept stationary while the

center line was allowed to move. The separation

between the center line and the innermost sur-

round lines was adjusted so that the surround

lines would not enter the receptive field at any

of the orientations used. The stimulus con-

figuration chosen allowed us to test separately

the effect of simulating outside the receptive

field along the movement axis vs along the

orientation axis.

Stimuli were presented in blockwise random

fashion. Usually we presented any given stimu-

lus condition 10 times when making a given

tuning curve. When making o~e~tatio~ tuning

curves for a celi, each block of conditions was

used to obtain an estimate of the orientation

optimum by fitting a spline through the points,

and the set of 10 blocks was used to obtain an

estimate of the mean peak position and stan-

dard deviation of the peak position. The statisti-

cal significance of a shift in orientation could

then be determined by using a standard r-test.

For the surround tuning curves, the data were

fit by a polynomial regression, which provided

an estimate of the sizes and positions of the

maxima and minima in the curves.

RESULTS

We first studied single cells in oat striate

cortex for the effect of the surround stimuli on

the responses of cells s~rnula~ with an opti-

mally oriented bar moving within the receptive

field center. Individual cells were only activated

when the line was within the receptive field.

Though the lines surrounding the receptive field

could not by themselves activate the cell, they

altered the response of the ceil when they were

of a certain orientation and position, The effect

of the surround lines on the center response

varied from cell to ce& some cells were inhibited

and some were facilitated by the presence of the

surround lines. The inhibition or fa~li~tion

was dependent on the orientation of the

surround lines, some cells showing maximal

response with surround lines matching the

optimal orientation of the cell, some when the

surround lines were o~hogonal to the cells

optimal orientation and others for orientations

in between. All of the

ells

in our sample were

located in the superficial layers of the cats

primary visual cortex.

Figure 2 illustrates the diversity of orientation

tuning seen for the lines in tbe surround

VR

3X11 K

spi kes/

Sweep

spi kes/

sxeep

70 110 150 10 50

orwntatron

16

o--

100

140 0

40 80

orientahon

Fig.

2. Comparison of center and surround tuning curves for

three superfcial layer complex ceils. The anter tuning

curves are reprcseutcd by the small open circles and the

surrwnd curves by the large so&d triangles. The surround

t~g~~~~~p~

of a center bar at

the optimal urierttatiun, and the level of Wng of the c&l

without the surround is indicated by the horizontal

dotted line. The suxwtmd tmdng curvea are generated by

a polynomial fit, and the symbols indicate the mean value

at each orientation. I$@op part of the figure shows a

call with an optimal oriantation of 8odcg. The surround

tuning curw p#lltJ at 9Ode& and is facilitatory at the

peak, and the minimmu is roughly at the orthogonal

orientation. The oall in the center of the figure has an

optimal orientation of 16Odeg; the psak in the surround

tuning is at 20 deg and the minimum around 60 deg. The ~11

at the buttom has an optimal orientation of fOdeg and the

surrmind tuning curw has a minim- at ~r~~~~ly the

same OtititiQn.


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1692

~ZHAIUBD. GILBERTnd TORSTEN . WIESEL

for superficial layer cells in cat area 17. The

response of a complex cell with optimum orien-

tation of 80 deg is shown in the top of Fig. 2.

The orientation tuning curve of this cell is quite

broad, having a half bandwidth (full width at

half height) of 60 deg. When stimulating the

center of the receptive field with a bar of the

optimal orientation, and changing the orien-

tation of the surrounding bars, the response of

the cell was most facilitated when the surround

bars were at orientation 90 deg, 10 deg from the

optimum. The cell was most inhibited by sur-

round bars at 10 deg, 70 deg from the optimum.

The facilitated response was roughly 20%

greater than the response to the center bar alone

(represented by the dotted line), and the most

inhibited response was 65% reduced from the

response to the single center bar. Other cells

were similar in the relationship of the center and

surround orientation tuning curves, but the

degree of inhibition or facilitation differed.

-100

I

0

20

40

60 a0

orientation

An example of a different relationship be-

tween the orientation tuning of the center and

surround is shown in Fig. 2 (middle, bottom).

The cell in the middle part of the figure was

optimally oriented at 160 deg. The surround

tuning curve was most inhibitory at 60-70 deg

(80-90 deg away from the optimal orientation)

and least inhibitory at 20 deg, 40 deg from the

optimum. For the orientations tested, the cell in

Fig. 2 (bottom) was strongly inhibited by a

surround oriented within 10 deg of the optimum

center orientation of the cell, the reduction in

response being 40% of the center only response.

Fig. 3. Plot of the maxima and minima of the surround

tuning of a sample of 13 cells. The maxima (12) are

rqrcscnted by the open circles and the minima (13) by the

solid triangles. The abscissa shows the absolute vale of the

orientation difference between the optimum orientation of

the center and the peak or valley in the surround tuning

curve. The amount of facilitation or inhibition is indicated

on the ordinate. Most of the &ects were inhibitory. Though

the peaks and valleys covered a range of relative orien-

tations, the maxima tended to be found near the orientation

prefmncc of the cell (0 deg orientation difference) and the

minima congregated towards the orthogonal orientation.

Other cells showed a broadly tuned surround, or

were uniformly inhibitory at all orientations.

We also observed, however, that the signs and

magnitudes of the surround effects were not

hxed for a given cell but could be influenced

by changing the brightness or contrast of the

surround lines.

The relationship between the orientation pro-

To explore other effects of the surround that

ducing maximal excitation or inhibition in the

may pertain to the tilt illusion, we focused on

surround and the orientation optimum of the surround effects for surround orientations near

center is shown for 13 cells in Fig. 3. We

the optimum of the cell (f40 deg), since in

included in the sample only cells for which we humans the most effective orientations for pro-

determined orientation tuning to the surround

ducing tilt illusions are those with an orien-

across the full range of orientations, and which tation contrast*

of 20-30 deg (Westheimer,

had a statistically significant peak and/or valley 1990). Surprisingly, the effect of the surround

in the surround tuning curve. Usually, the was not restricted to simple inhibition or facili-

surround inhibition was not complete, and tation, in that surround lines of the appropriate

the orientation tuning curve of the surround

orientation could in fact change the orientation

was broader than the orientation tuning of preference of a cell. In these experiments we

the center bar response. The positions of the fixed the orientation of the surround and deter-

minima and maxima of the surround tuning mined the orientation tuning to the center bar

curves varied from cell to cell, but there was a when displayed concurrently with the surround

tendency for the maxima to aggregate towards and with all lines moved in tandem. This was

the optimal orientation of the cell, and for the repeated for surround lines of different orien-

minima to aggregate towards the orthogonal tations. For the cell illustrated in Fig. 4 the

orientation. Furthermore, surround effects

optimum orientation without surround lines

that were largely inhibitory were much more

was 30deg. However, when the surround lines

commonly seen than facilitatory surrounds. were oriented at 0 deg (30 deg away from the


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Influence of contextual stimuli

1693

central Gtr angle O)

Fig. 4. Orientation tuning curves for a superficial layer

complex cell without surround (bold line) and with sur-

rounds of different orientations. The peak orientation is at

30 deg, but in the presence of a surround of 0 deg the peak

shifts away from the surround orientation, to 40deg. In

addition to the peak shift seen for a 0 deg surround, there

is varying degrees of inhibition for surrounds of other

orientations. Note also the broadening of the tuning for the

Odcg surround condition.

optimal orientation of the cell, which is near

the most inhibitory surround orientations), the

tuning curve peaked at 40 deg, representing a

shift in the peak position of 10 deg. Note that in

this instance the effect of the surround was

repulsive, with the tuning curve shifting in

a direction away from the orientation of the

surround lines. The shift was reversible and

repeatable, such that surround lines of any other

orientation produced tuning curves peaking

again at 30 deg, and each time the surround

orientation was put at Odeg, the peak shifted

back to 40 deg (as seen by the three curves on

the right in Fig. 4). The effect was statistically

significant, with

P

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1990 - C D Gilbert - Theinfluenceofcontextualstimuliontheorientationsel[Retrieved-2016!01!15]