Evidence for implication of primate area V1 in neural 3

Journal of Physiology - Paris 98 (2004) 125–134
www.elsevier.com/locate/jphysparis
Evidence for implication of primate area V1 in neural
3-D spatial localization processing
Yves Trotter *, Simona Celebrini, Jean Baptiste Durand
Faculte de Medecine Rangueil, Centre de Recherche Cerveau & Cognition, CNRS, Universite Paul Sabatier, 133 route de Narbonne,
31062 Toulouse Cedex, France
Abstract
We investigated the neural mechanisms underlying visual localization in 3-D space in area V1 of behaving monkeys. Three
different sources of information, retinal disparity, viewing distance and gaze direction, that participate in these neural mechanisms
are being reviewed. The way they interact with each other is studied by combining retinal and extraretinal signals. Interactions
between retinal disparity and viewing distance have been shown in foveal V1; we have observed a strong modulation of the
spontaneous activity and of the visual response of most V1 cells that was highly correlated with the vergence angle. As a consequence of these gain effects, neural horizontal disparity coding is favoured or refined for particular distances of fixation.
Changing the gaze direction in the fronto-parallel plane also produces strong gains in the visual response of half of the cells in
foveal V1. Cells tested for horizontal disparity and orientation selectivities show gain effects that occur coherently for the same
spatial coordinates of the eyes. Shifts in preferred disparity also occurred in several neurons. Cells tested in calcarine V1 at retinal
eccentricities larger than 10°, show that horizontal disparity is encoded at least up to 20° around both the horizontal and vertical
meridians. At these large retinal eccentricities we found that vertical disparity is also encoded with tuning profiles similar to those of
horizontal disparity coding.
Combinations of horizontal and vertical disparity signals show that most cells encode both properties. In fact the expression of
horizontal disparity coding depends on the vertical disparity signals that produce strong gain effects and frequent changes in peak
selectivities. We conclude that the vertical disparity signal and the eye position signal serve to disambiguate the horizontal disparity
signal to provide information on 3-D spatial coordinates in terms of distance, gaze direction and retinal eccentricity. We suggest that
the relative weight among these different signals is the determining factor involved in the neural processing that gives information on
3-D spatial localization.
Ó 2004 Published by Elsevier Ltd.
Keywords: 3-D space localization; Foveal and peripheral V1; Horizontal and vertical disparities; Viewing distance; Gaze direction
1. Introduction
The simple motor act of grasping an object viewed in
the immediate environment is the result of a series of
neural transformations processed by the brain, that are
still poorly understood and even difficult to replicate
artificially. We will focus on the initial step that consists
in localizing the objects in the near space. Three
dimensional (3-D) spatial localization includes at least
stereopsis, viewing distance and gaze direction. The
relative position of the images of an object on both
retinae will give information on relative depth of the
*
Corresponding author.
E-mail address: [email protected] (Y. Trotter).
0928-4257/$ - see front matter Ó 2004 Published by Elsevier Ltd.
doi:10.1016/j.jphysparis.2004.03.004
object, its shape and volume (stereopsis). Evaluation of
the distance between the object and the observer will
combine stereoscopic and ocular vergence information.
If the eyes fixate straight ahead, they converge symmetrically. If the eyes fixate on other positions in space,
on the horizontal meridian or obliquely, they converge
asymmetrically. Both symmetrical and asymmetrical
convergences define gaze directions for a particular
orientation of the head. Therefore, to localize visually
objects in space, the brain needs to combine information
about the position of their images on the retinae with
information about the location of the eyes in the orbits
and the position of the head.
A major question in neurosciences is to determine the
neural processing for 3-D spatial localization. Clinical
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studies in humans have described, among other disorders, the difficulty in locating visual targets in space
following lesions of the posterior parietal cortex [2,42].
Electrophysiological studies performed in behaving
monkeys showed that this cortical area integrates signals
from several modalities, among them visual and oculomotor signals. Depending on where the monkey is
looking, light sensitive cells respond with a certain
neural gain. This neural modulation by the direction of
gaze would be the basis for encoding the position of
objects in multiple frames of reference, such as eye- and
head-centered [3,4]. An alternative is that this transformation is accomplished by dynamic updating of spatial
representation in conjunction with voluntary eye movements [16,25]. For many years the parietal cortex was
believed to be the main cortical site for processing space
localization following the pioneering work of Andersen
and col. [1,3]. Since then other cortical areas, from the
pre-striate cortex to the pre-motor cortex [12], were also
shown to be involved. We will review and give recent
evidence that the so-called primary visual cortex, area
V1, also closely participates to the neural 3-D space
localization processing.
2. Stereopsis and viewing distance
2.1. Stereopsis and horizontal disparity sensitivity
Stereoscopic depth perception depends on binocular
vision, and because of the interocular distance, the
image of the viewed object is projected on both retinae
in slightly different angular positions, called horizontal
retinal disparity. The brain uses this binocular clue to
reconstruct relative depth. The demonstration that stereopsis is mainly due to retinal horizontal disparity was
given by Wheatstone [96] when he invented the mirror
stereoscope. This device allows the simulation of depth
by presenting two photographs, one to each eye, taken
with a slightly different angular direction. Subsequently
Julesz [47] used psychophysical experiments with random dot stereograms to demonstrate that a difference in
the horizontal position of corresponding elements of left
and right images is sufficient to reconstruct depth. These
stereograms are composed of two identical patterns of
random dots, except that some or all of them are slightly
shifted horizontally. When perceived through a stereoscope, color filters or stereo glasses, the two monocular
images are fused and the angular disparity is then
interpreted in terms of relative depth with a vivid 3-D
percept of a shape floating in front of or behind the
background depending on the sign of angular disparity
(positive: behind; 0: the plane; negative: in front)
introduced between the two images.
From the neurophysiological point of view, area V1
is the first cortical site that integrates retinal inputs
from both eyes. Left and right receptive fields of a
binocular neuron may be in exact topographic correspondence in the two eyes or may have slightly disparate locations. An alternative model to the positional
disparity has been proposed, in which retinal disparity
information originates from differences in the internal
structure of receptive fields of the left and right eyes,
described in terms of phase differences [31]. In fact both
position and phase differences between the monocular
receptive fields appear to coexist for encoding retinal
disparities [5]. In both cases, two identical stimuli falling in the same position in both receptive fields or in
slightly different positions will produce binocular
interactions such as binocular suppression and/or
facilitation as first shown in the primary visual cortex
of the anaesthetized paralyzed cat [8,28,46,60]. This
property of disparity selectivity is generally considered
as being the neural basis for stereopsis [69,73]. Experiments performed in the alert behaving monkey in
normal conditions of binocular vision have shown in
area V1 of the rhesus macaque, the existence of several
categories of cells preferentially activated by stimuli
located in front, behind or in the plane of fixation (Fig.
1), that appear to share a continuum in space [70–
72,89].
Recent investigations have challenged the statement
that disparity sensitivity of cortical neurons in area V1
is used for depth perception. On one hand, relative
disparity signals used in primate depth perception
would be constructed outside area V1 [85] since the
depth sensation is not reflected in the firing rate of V1
neurons [19]. On the other hand single V1 neurons may
outperform the depth discrimination performance of
the monkey [75]. Neuroimaging experiments in human
reveal clear activations of area V1 with PET [39,40,76]
or fMRI [7,90], whereas other sudies do not find such
activation of area V1 [30,57,61]. Thus the question of
the participation of V1 neurons in depth perception is
not yet resolved. The clearest demonstration to date of
a role of disparity cells in depth perception per se has
been shown in area MT of the monkey, as electrical
stimulation of clusters of disparity selective MT neurons can bias the monkey perceptual judgements of
depth, and this bias is predictable from the disparity
preference of neurons at the stimulation site [21]. There
is still the unexplored possibility in primates, using
such an approach, that intermediate cortical areas such
as V3–V3a could also be directly involved in depth
perception, as proposed by brain imaging studies [7,
61].
Disparity sensitive cells of area V1 could also be used
as a 3-D signal for eliciting rapid involuntary control of
vergence eye movements to bring images of both retinae
into register as suggested by the use of anticorrelated
patterns [51], and/or to maintain precise binocular
alignment during stereoscopic vision.
Y. Trotter et al. / Journal of Physiology - Paris 98 (2004) 125–134
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Fig. 1. Categories of horizontal disparity selective cells in area V1. (A) Raster display of a cell sensitive to negative disparities (Near type) with the
corresponding tuning curve in B. In C is displayed a schematic representation of the disparity sensitive cell categories.
2.2. Viewing distance and horizontal disparity sensitivity
Relative disparity provides information about relative distance between objects, independently of where
the eyes are looking. It does not give any information on
the spatial localization of the objects in terms of distance
or retinal eccentricity. Evaluation of distances of objects
can be directly calculated by the angle formed by the
lines of sight or angle of convergence in the fixation
plane. For an object lying outside the fixation plane, it
requires a calculation that combines the angle of convergence with the retinal disparity (absolute disparity) of
the object. Both types of disparity, relative and absolute,
must interact to yield the impression of real depth. A
simple way for understanding the interaction between
relative and absolute clues is to look at a stereogram in a
book, at a close distance. While looking at the stereogram with a fixed relative disparity, if we move the book
away from the eyes, it follows that the perceived relative
depth of the anaglyph increases rapidly as the absolute
distance increases. This is done according to a certain
law since retinal disparities are proportional to relative
stimulus depth and inversely proportional to the square
of the viewing distance [64,66, for reviews]. According to
that law any object that is moved away should appear to
flatten very rapidly. However this is not the case. A cup
for example appears as having the same shape and
volume when perceived at 20 or 80 cm despite the fact
that disparities are smaller by a factor of 16. This
capacity to judge accurately relative depth at various
viewing distances refers to depth constancy. This implies
that the decrease in retinal disparity as a function of the
viewing distance has to be internally compensated.
Several candidates have been proposed to explain this
transformation process such as ocular vergence,
accommodation [29,35,67,79,94] and/or vertical disparity [11,45].
The idea that disparity selective cells in area V1 may
have a link with oculomotor signals has been strengthened by experiments in which neural activity has been
shown to be dependent on the viewing distance [88,89].
These studies investigated how relative and absolute
cues interact in the visual pathway, in area V1 of
behaving monkeys. Experiments were conducted to test
disparity sensitivity using static random dot stereograms
(RDS) at different viewing distances set at 20, 40 or 80
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cm. It was found that more than 75% of recorded cells
drastically changed their visual response when the distance of fixation changed, with the consequence that
disparity selectivity could be present at a given distance
but absent at another one. This is illustrated by the
example of Fig. 2A in which the visual response drops
close to the spontaneous activity level for a distance of
40 cm. For other cells disparity selectivity was present at
all distances but better expressed at one particular distance with higher response amplitude and sharper tuning curves as shown in the example of Fig. 2B for a
distance of 40 cm. These modifications of the visual
response were independent of the retinal pattern. Another consequence concerned the level of spontaneous
activity level that was also modified for half the recorded
cells. Because there was no retinal pattern during the
time that the spontaneous activity was collected, the
source of the modifications could only be extraretinal.
Since modulations of both the visual response and the
spontaneous activity level appeared nonretinal in origin
and possibly related to the ocular convergence, we tested
this possibility by using prisms, base out, that produce a
change in the vergence angle without changing the distance of fixation, therefore involving the accommodation to a lesser degree [89]. Since then, other studies have
been devoted to investigating the effects of manipulating
the ocular convergence on disparity coding in area V1.
Gonzalez and Perez [36] observed similar modulations
of the visual responses for half of the cells of area V1
sensitive to horizontal disparity. On the other hand
Cumming and Parker [18] could not reproduce the results of changing the ocular vergence angle. The range of
vergence angles that these last authors used (from 1° to
3.5° in monkeys equivalent to about 2–7° in humans
taking the interocular distance into account) was probably too small to sufficiently activate vergence signals, in
contrast to the Gonzalez and Perez [36] (3–6.5° range
equivalent to about 6–13° in humans) and Trotter et al.
[88,89] (2–10° range equivalent to about 4–20° in
human) studies. It should be noticed that about 90% of
the vergence angle is used within this last range [92].
Finally Dobbins et al. [23] studied the effects of the
Fig. 2. Effects of changing the viewing distance (A, B) or the gaze direction (C–F) on visual activity in V1. In A the cell is clearly a Near type cell at a
distance of 80 cm but is nonvisually responsive at 40 cm. In B this cell shows a sharper tuning curve (Tuned Far type) and a higher visual amplitude
response at 40 cm than at 20 or 80 cm viewing distances. Dashed curves are gabor fittings. In C the cell is a Tuned Excitatory type (TE) for a gaze
oriented to the left at )10° or in the center (0°) of a video monitor screen but its visual activity almost disappears for a gaze to the right at +10°.
Dashed curves are gabor fittings. In D the cell shows a higher visual response (orientation selective) for a gaze at the center of the screen than for the
other directions. The dashed curves are gaussian fittings. In E (recorded in calcarine V1, retinal eccentricity )22.5° the cell is a Near type cell. Its
activity increases and the peak of disparity selectivity changes progressively with the deviation of the gaze. In F (calcarine V1, eccentricity )12.5°) this
cell shows progressive changes in peak selectivities as the gaze turns from 10° on the right (Tuned Near), to 15° (TE type) and becomes Tuned Far at
18°. Dashed curves are gabor fittings.
Y. Trotter et al. / Journal of Physiology - Paris 98 (2004) 125–134
viewing distance in area V1 on another retinal feature,
i.e. the size of an image, using similar angular vergence
angles to those of Trotter et al. [88,89]. They observed
strong modulations of the visual response and of the
spontaneous activity, and extended their observations to
the cortical area V4. Strong modulations of cell activities
in cortical areas V1, V2 and V4 of the behaving monkey
were reported recently by changing the viewing distances
in similar conditions [82].
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gaze and to a lesser extent for a leftward position of the
eyes than for a rightward position. For cells that were
tested for both horizontal disparity and orientation
selectivities the gain effect was congruent for a common
gaze direction. Other studies also reported influences of
the gaze direction on the visual excitability of foveal
V1 neurons in primates [41,82] and in cat area 17
[95].
3.2. Gaze angle and horizontal disparity in peripheral V1
3. Stereopsis and gaze angle
3.1. Gaze angle and horizontal disparity in foveal V1
Gaze direction has been shown to modulate the
neural activity of most cortical areas in the dorsal
pathway [12] and has been interpreted as being a neural
process involved in spatial localization [1]. Similar
modulations also appear to occur in the ventral pathway
[14,62]. The question still debated [18] is whether the
primary visual cortex (area V1) is involved in the neural
process of spatial localization or not. The demonstration
of the effects of changing the viewing distance (see
above) on the neural activity of V1 cells strongly suggest
that area V1 also participates to the neural process of
spatial localization. To test this possibility, a series of
experiments [87] was performed on behaving monkeys
trained to fixate a small target located in the frontoparallel plane at three positions on a video monitor
screen (center 0°, left )10°, right +10°). Stimuli such as
dynamic RDSs generated through ferro-electric stereo
glasses at 60 Hz per eye were projected in the visual field,
centered on the receptive field. Static square wave
gratings of the same size were also used to test orientation selectivity for evaluating whether the eventual
gaze effects could be extended to other cortical properties in a coherent way or not.
Neurons were recorded extracellularly in area V1 in
the central representation of the visual field. Responses
to horizontal disparity and grating orientation as well in
about half of the tested cells were strongly modulated in
that these properties were present at a given gaze
direction, but absent or poorly expressed at another
direction. This gain effect was present for 72% of cells
studied for disparity and 85% of cells studied for orientation. The cell illustrated in Fig. 2C detects the
presence of the stimulus RDS in the plane of fixation (0°
disparity angle, i.e. Tuned Excitatory cell) when the
monkey fixates straight ahead or on the left ()10°) but
very poorly for a fixation on the right (+10°). Shifts in
peak selectivity occurred for 17% of disparity selective
cells. Similar observations were made concerning stimulus orientation except for changes in peak (0%). Fig.
2D shows an example of a cell whose orientation
selectivity (oblique) is better expressed for a centered
A second series of experiments was performed in the
peripheral region of the primary visual cortex called
calcarine V1, anatomically located just below foveal V1.
Except for the cortical mapping of receptive fields located at retinal eccentricities larger than 10° along either
the horizontal meridian (dorsal calcarine V1) or the
vertical meridian (ventral calcarine V1) [20,33,91], very
little is known concerning their functional properties
[9,68].
A Rhesus monkey, with scleral coils implanted in
both eyes, was trained to fixate at up to seven directions
in the fronto-parallel plane. Visual stimuli were the same
as those used in the foveal V1 study. Experimental
recordings show that cells in this region are still highly
selective to stimulus disparity (36% of cells) and/or
stimulus orientation (100% of cells) and also to the
direction of gaze (75% of cells). Gaze effects are similar
to those reported in foveal V1. The example in Fig. 2E
illustrates a cell (Near type) that combines modulation
of the visual response and progressive changes in peak
positions as the gaze rotates progressively from 8° to
12°. In Fig. 2F the cell shows changes in peak selectivity
not associated with the modulations of the visual response. It is a Tuned Near cell for a gaze at 10° on the
right, then is Tuned 0° for a gaze at 15° and becomes a
Tuned Far cell at 18°.
For these changes in the peak of disparity selectivity
that appear in the foveal and peripheral V1, one possible
explanation is the following. For a gaze directed in the
center of the screen, the normal to the binocular axis
and the tangent to the Vieth-M€
uller circle, that is used as
a reference for stereoscopic judgements, are superimposed. For a gaze directed on the left or on the right
(asymmetrical convergence) the normal to the direction
of gaze is rotated away from the tangent, that should
induce a change in binocular correspondence and
therefore errors in stereoscopic judgements. However
psychophysical experiments do not find such misjudgements. Therefore for the normal surface to yield correct
stereoscopic spatial perception, a compensation process
must take place [56,65]. The subset of neurons that
change their preferred disparity angle may be a part of
the neural substrate that allows the compensation for
this shift in depth. Indeed after calculation, taking into
account the hemisphere and retinal eccentricity, the shift
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in peaks corresponds exactly to the angular rotation in
depth of the normal axis to the tangent.
4. Eye position signals, retinal versus extraretinal
Concerning the gain effects in foveal V1 produced by
changing the viewing distance, the signal responsible for
it, is probably oculomotor in origin related to the eye
position. Modulation of the visual response and of the
spontaneous activity by ocular vergence indicates that
the visual pathway receives an extraretinal source related to ocular motility. If the modulations of the visual
response resulted from feedback influences from higher
cortical areas, they should occur with some delay in the
course of the visual response. But this was not the case
as these modulations were present at the beginning of
the visual response and remain constant throughout
[87]. A probable source of feed-forward interaction between retinal and extraretinal signals may reflect a
neural gating that could be mediated from the dorsolateral geniculate nucleus (LGNd). It should be pointed
out that spontaneous activity modulation of about onethird of the LGNd cells has been described by manipulating the vergence angle with prisms in the awake
monkey [78]. Also eye position signals have been shown
to influence visual activity of LGNd neurones in other
species such as the cat [24,50] and the rabbit [55]. What
are the possible origins of these signals? The two classical possible sources are efference copy and extraocular
muscle proprioception (EMP). Both are probably involved to a certain degree in spatial localization [34] and
many studies have provided evidence for a functional
role of EMP in spatial location, construction of extrapersonal space, eye alignment control, postnatal development of depth perception and of neuronal selectivities
including disparity coding [15,83,86, for reviews].
There is another signal that may possibly account for
the gaze effects on V1 cells, not in the foveal representation of the visual field where it is negligible, but in the
peripheral field where it occurs naturally: this is vertical
disparity that has been recently shown to be encoded in
area V1 at peripheral eccentricities [26].
5. Vertical disparity
Differences in the position of similar binocular images
in the vertical dimension are called vertical disparities.
In normal use of the eyes, they occur when the eyes
converge at a close distance. In that case, the images of
all points located above or below the visual plane, except those lying in the median plane, are vertically disparate. Vertical disparities occur in all situations where
an object is closer to one eye (eccentric images, oblique
gaze. . .). Its image is larger on the retina of this eye
resulting in angular disparities that include the vertical
dimension. Vertical disparities decrease with distance
but increase with retinal size, with horizontal and vertical eccentricities and with gaze directions. Whether
vertical disparities affect the binocular perception of
depth has been and still is a matter of debate. They affect
depth perception if the vertical angular deviations are
too important [59] and can be regarded as just a geometrical defect (an error) more or less tolerated by the
visual system. As a result, an ocular shift must occur to
compensate for the vertical angular deviations in order
to recover the binocular matching involved in stereopsis.
Vertical disparities may thus act as retinal signals sent to
the oculomotor centers for driving vergence movements
in the vertical dimension to align the eyes, just as horizontal disparities do for driving horizontal ocular vergence. In other words horizontal vergence occurs when
the gaze is shifted from one depth plane to another and
vertical vergence occurs when the gaze shifts in oblique
directions towards a target in a tertiary position [43].
Gain for vertical vergence increases as the stimulus area
increases around the fovea [44].
Vertical disparities occur naturally in stereoscopic
vision, the angular range depending on the size of the
images and on their retinal eccentricities [66]. The first
demonstration of a functional role of vertical disparity
in depth perception was given by ‘the induced effect’
[63]. When a meridional lens (one that produces a horizontal size disparity) is placed in front of one eye, the
apparent plane appears rotated around the vertical axis
in a way predicted by geometry (geometrical effect). If a
vertical lens (one that produces a vertical size disparity)
is placed in front of one eye, the apparent plane appears
rotated in the opposite direction in a way not predictable by geometry, as if a meridional lens was applied in
front of the other eye (induced effect). Psychophysical
experiments have confirmed the functional role of vertical disparity in stereoscopic vision [6,10,13,48,80,
81,84]. Vertical disparity carries information that theoretically permits the disambiguation of horizontal disparity signals in terms of 3-D localization. Several
models have been proposed to explain how horizontal
and vertical disparity signals could interact to recover
the 3-D space characteristics with or without an extraretinal source of information on the position of the eyes
in their orbits [32,49,53].
In contrast to horizontal disparity that has been the
object of increasing interest at the neurophysiological
level during the past few years, very few studies have
been devoted to vertical disparity sensitivity [37,69].
Vertical incongruities of receptive fields of binocular
neurons were first shown in the cortical areas 17 and 18
of the anaesthetized cat [8,46,60,93]. In primates, sensitivity of cortical neurons to vertical disparity was shown
in the foveal area V1 of the behaving monkey [17,38], in
area MT of the anaesthetized monkey [52] and in the
Y. Trotter et al. / Journal of Physiology - Paris 98 (2004) 125–134
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disparity encoding, the percentage of selective cells is
lower than what is found in the foveal part of V1 (about
half) but half of them are Tuned Near and Tuned Far
types. Since stereoscopic vision is low or absent at such
retinal eccentricities, these disparity sensitive cells can
hardly account for a neural process involved in stereoscopic depth per se but rather in a fine ocular alignment
control.
6. Conclusions
Fig. 3. Vertical disparity tuning profiles of cells located in the calcarine
V1. On top, cells exhibit tuning profiles similar to those of horizontal
disparity selective cells. Red curves are gabor fittings. In at the bottom
example of a cell tested for 70 combinations of horizontal and vertical
disparities. This cell is selective to both dimensions, to horizontal
disparity (HD of 0.4–0.6°, Far type) and vertical disparity (VD of 0.4–
0.6°, Far-like).
wulst of the awake barn owl [58]. These studies were
usually performed in the central part (within 10°) of the
representation of the visual field, paying less attention to
the peripheral field probably because stereoscopic vision
rapidly vanishes outside of the fovea [54,77]. In contrast
vertical disparity increases with retinal eccentricity.
Therefore it is in the peripheral field that one should
expect this signal to be encoded rather than in the central field.
We have conducted a study in a behaving monkey
[26] to test vertical disparity selectivities, and horizontal
disparity as well, in the calcarine area V1 and area V2,
hence beyond 10° of retinal eccentricity. A Rhesus macaque was trained to perform a fixation task, gaze
straight ahead, with scleral coils implanted in both eyes.
Both horizontal and vertical disparity selectivities were
tested using dynamic RDS. A large proportion of the
tested cells were selective to both types of disparities
(47%), and to a lesser extent to only one type (horizontal: 8%; vertical: 23%). We found a true encoding of
vertical disparity, with the same diversity in the tuning
profiles as described for horizontal disparity (Fig. 3, top
view), that cannot be assimilated with a simple disturbance of the binocular matching process as proposed
earlier [69]. Moreover, cells sensitive to vertical disparities cover a finer angular scale than those of horizontal
disparities, which is coherent with the smaller range of
naturally occurring vertical disparities. The cell in Fig. 3
(bottom) was tested for combined horizontal and vertical disparities (matrix of 70 combinations). This cell
shows a clear interdependence between horizontal and
vertical disparity codings, which is a Far type cell for
horizontal disparity and Far-like type for vertical
disparities both centered on 0.4–0.6°. For the horizontal
The viewing distance effects on the activity of foveal
V1 cells most probably originate from eye position signals since vertical disparity of the receptive fields within
3° of retinal eccentricity is too small, around 1 min of
arc at 20 cm and 0.3 min of arc at 80 cm, to account for
the strong modulations of visual responsiveness. And
vertical disparity obviously cannot account for the
modulations of the spontaneous activity in absence of
visual stimulation. On the other hand, the gaze direction
effects in the cortical area V1 likely originate from various combinations of eye position signals, horizontal
and vertical disparity signals. Horizontal disparity by
itself is not informative about 3-D characteristics of
space in terms of distance or eccentricity. Eye position
and vertical disparity signals must contribute at least
with a relative weight depending on the 3-D configurations (small image size/large size, foveal/peripheric, close
distance/far, gaze direction ahead/oblique. . .) as proposed by psychophysical [13,80] and modelling studies
[6,10,27,32]. These different weighted combinations
should allow transformations of frame coordinates in
Fig. 4. Schematic representation of the activity of a neurone (Far type)
that is dependent on 3-D eye coordinates. The activity of this cell is
optimally expressed for a gaze of )10° on the left, at 40 cm of viewing
distance. The elliptic shape in gradual blue represents this zone in space
and can be regarded as a 3-D module defined by eye position coordinates.
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order to reconstruct the 3-D space for reaching the objects accurately, possibly through a basis function representation that predicts that a large majority of cells
should encode two or more signals simultaneously and
combine these signals nonlinearly [22,74]. However, the
way these combinations are processed at the neuronal
level remains to be investigated. Preliminary experiments on these combinations in our laboratory show
that some neurons in area V1 have gain effects that
cannot be explained totally by vertical disparity signal
alone or by eye position signal alone, while others can be
explained mostly by one or by the other. Further neurophysiological studies will be needed to determine the
weight of these respective factors at the cellular level, to
better understand sensorimotor transformation processing necessary to navigate in 3-D space.
If we bring together the results on the effects of the
viewing distance and those of the gaze direction in area
V1, we come up with the proposal that cortical properties such as orientation and retinal disparity selectivities, that define shapes and volumes of objects, are
optimally expressed in a limited range of 3–D gaze
directions so that information about stimuli in the V1
area is conveyed by cell populations only when the object is present within restricted volumes of space. Fig. 4
illustrates for one hypothetical neuron this spatial representation inside a restricted volume of space defined
by 3-D eye position and/or vertical disparity signals.
These modules should be regarded as 3-D fields, as
being a part of the neural substrate that is involved in
sensory-motor transformations for 3-D space localization.
Acknowledgements
We thank E. Galy and S.P. Zhu for their participation in some of the experiments.
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