Download SHORT COMMUNICATION Interocular temporal delay

European Journal of Neuroscience, Vol. 11, pp. 2593±2595, 1999
ã European Neuroscience Association
SHORT COMMUNICATION
Interocular temporal delay sensitivity in the visual cortex
of the awake monkey
Rogelio Perez,1,2 Francisco Gonzalez,1,2 Maria S. Justo1 and Carlos Ulibarrena1
1
Departamento de Fisiologia, Laboratorios ¢Ramon Dominguez', Facultad de Medicina, Universidad de Santiago de
Compostela, Spain
2
Servicio de Oftalmologia, Complejo Hospitalario Universitario de Santiago, Santiago de Compostela, Spain
Keywords: binocular vision, Macaca mulatta, stereopsis, striate cortex, temporal disparity
Abstract
Due to the separation of the eyes, temporal retinal disparities are created during binocular stimulation and they have been proposed
to be the basis of several stereo-visual effects. This paper studies the sensitivity of cortical neurons from area V1 to interocular
temporal delay in the awake monkey (Macaca mulatta). Forty-four cells were included in this study. Temporal delay sensitivity was
observed in 59% of them. About half of these temporal-delay-sensitive cells were also sensitive to the stimulation sequence of the
eyes. The cells that preferred one eye to be stimulated ®rst were termed asymmetrical (46%); those which were not sensitive to the
eye sequence of stimulation were termed symmetrical (54%). No clear differences were observed in the distribution of delay-sensitive
cells according to their eye dominance. Fifty-six percent of balanced cells and 65% of unbalanced cells were sensitive to interocular
delay. These data underline the importance of temporal cues for depth perception.
Introduction
Methods
Because of horizontal eye separation, the left and right retinal images
are slightly different. These differences are termed spatial disparities
and the visual system makes use of them to achieve depth perception,
as demonstrated by the use of random dot stereograms (Julesz, 1960).
Sensitivity to spatial disparities has been described in cortical neurons
of monkeys, cats and other animals (see Gonzalez & Perez, 1998 for
review).
Additionally, the separation of the eyes also causes temporal retinal
disparities to occur during object or observer motion. Interocular
temporal input delays are believed to be the basis of stereo-effects
such as Pulfrich's or March-Dvorak's phenomena (Howard &
Rogers, 1995). Sensitivity of cortical neurons to interocular temporal
disparities is known to exist in cats. It has been shown that cortical
visual cells in this animal are driven with unequal latencies which
could provide the substrate for a temporal disparity depth perception
mechanism (Gardner et al., 1985; Gardner & Raiten, 1986). These
observations suggest that visual neurons can use time-based cues to
calculate stereoscopic depth. Thus, sensitivity to spatial disparity and
sensitivity to interocular temporal disparity should be regarded as two
complementary mechanisms to achieve reliable depth perception. The
purpose of this study was to investigate the cell responses of visual
area V1 to binocular stimulation with different interocular stimulus
delays in awake monkeys.
The experimental procedures are described in detail elsewhere
(Gonzalez et al., 1993a,b) and are brie¯y outlined here.
One male Macaca mulatta weighing 5 kg was trained to maintain a
steady binocular ®xation on a small bright bar (0.2 3 0.1 °). The
animal was sitting with his head ®xed in front of two cold mirrors to
allow simultaneous and separate viewing of two black±white
monitors located 57.7 cm away. The stimulus was delivered during
the period of ®xation and consisted of a static square bright ®gure
(1.5 3 1.5°) on a dark background brie¯y ¯ashed (one monitor frametime, 20 ms) over the cell's receptive ®eld. Cells were stimulated by
presenting the stimulus over a range of interocular delays at 20-ms
steps. The temporal delays and eye sequence of stimulation were
randomized.
Cell responses were quanti®ed by subtracting the basal discharge
rate from the discharge rate (spikes per second) calculated for a
period of 150 ms after the stimulus was presented to the delayed eye.
The average of at least 15 stimulus presentations under the same
conditions was used to construct plots of cell response against
stimulus delay for each cell (Figs 1 and 2). In order to assess
sensitivity to interocular temporal delay, and the symmetry of the
responses relative to zero delay, the analysis of variance (ANOVA,
P < 0.05) was used.
Monocular stimulus presentations lasting 750 ms were used to
assess the cell's ocular dominance. Eye dominance was de®ned by the
eye dominance index which resulted from dividing the cell response
evoked from the contralateral eye by the sum of the responses obtained
from the contra- and ipsilateral eyes. According to the eye dominance
index, the cells were organized in seven groups (Hubel & Wiesel,
1962, 1968). Cells belonging to groups 1, 2, 6 and 7 were considered
Correspondence: Dr Francisco Gonzalez, Departamento de Fisiologia,
Facultad de Medicina, E-15705 Santiago de Compostela, Spain.
E-mail: [email protected]
Received 25 January 1999, revised 19 April 1999, accepted 20 April 1999
2594 R Perez et al.
FIG. 1. Visual responses of a cell recorded from area V1 of an awake monkey
to a binocularly, brie¯y ¯ashed stimulus (20 ms) with different interocular
delays. Each dot represents the difference between the stimulus response to the
second eye stimulus and the basal activity of the cell (2.5 spikes/s). The
vertical bars represent the SD (see methods). Negative delays indicate that the
right eye was stimulated ®rst. Positive values indicate that the left eye was
stimulated ®rst. The cell optimal response is slightly shifted towards negative
delays (ANOVA, P < 0.05). This cell was considered an asymmetrical delaysensitive cell. Monocular responses to the left (L, ®lled circle) and right eye
(R, triangle) stimuli are also represented.
unbalanced cells, whereas those included in groups 3, 4 and 5 were
considered balanced cells.
To access the cortex with metal electrodes, several craniotomies
were performed on the skull covering the occipital lobe under
ketamine anaesthesia (7 mg/kg, i.m.). For major surgical procedures
the animal was anaesthetized with sodium pentobarbital (27 mg/kg,
i.v.) after induction with ketamine (25 mg, i.m.). Antibiotics
(Penicillin, 50 000 IU/kg, i.m.) and analgesics (Noramidopirine,
150 mg/kg, i.m.) were given after surgery. All efforts were made to
minimize animal suffering and the surgical and experimental
procedures followed the guidelines of the Bioethic Committee of
our institution.
Results
This study was conducted in 44 cells recorded from the dorsal and
dorsomedial surface of area V1. The eccentricity of the receptive ®eld
positions ranged from 6.6 to 18.1 ° (mean, 10.9 °). Sixty-one percent
of cells (27 out of 44) were ocular-balanced while 39% (17 out of 44)
were considered ocular-unbalanced cells.
Slightly more than half of recorded neurons (26 out of 44, 59%)
showed different responses to different interocular delays and
therefore they were termed delay-sensitive cells. Typically, delaysensitive units (Figs 1 and 2) displayed an interocular facilitation for a
given range of delays, and a relatively ¯at response pro®le for delays
exceeding this range. This facilitation was centred at, or around, zero
interocular delay, within the range of 6 100 ms and lasted from 100
to 200 ms in most cells (ANOVA, P < 0.05).
In about half of delay-sensitive cells (12 out of 26, 46%) there was
an increased response away from zero interocular delay, indicating
that the cell was sensitive to the sequence of eye stimulation (Fig. 1).
In these cells, termed asymmetrical delay-sensitive cells, the
responses obtained under left±right and right±left sequences of eye
stimulation were statistically different (ANOVA, P < 0.05). In the
remaining delay-sensitive cells (14 out of 26, 54%) there was an
increased response centred at zero interocular delay, showing no
FIG. 2. Responses of a visual cell of monkey area V1 to a binocularly, brie¯y
¯ashed stimulus (20 ms) with different interocular delays. The plot was
constructed as in Fig. 1. The basal activity of the cell was 13.5 spikes/s. The
cell displays and enhancement of the response to the stimulation of the second
eye for delays ranging from ±100 to +100 ms (ANOVA, P < 0.05). This cell was
considered a symmetrical delay-sensitive cell.
signi®cant statistical differences regarding the eye sequence of
stimulation (ANOVA, P > 0.05). These cells were termed symmetrical
delay-sensitive cells (Fig. 2). We were unable to ®nd any relationship
between eye dominance and these two types of cells (asymmetrical
and symmetrical).
Delay-sensitive cells were in quite similar percentages from both
balanced (15 out of 26, 58%) and unbalanced (11 out of 26, 42%)
groups. In contrast, delay-insensitive cells were twice as frequently
balanced (12 out of 18, 67%) than unbalanced (six out of 18, 33%).
Discussion
Psychophysical observations suggest that the visual system is
sensitive to temporal disparities. It was shown that a target is
perceived beyond the ®xation point when it is ¯ashed ®rst to one eye
and then to the other with a temporal offset, and that the distance
increases with increasing temporal offset (Wist, 1968). Moreover,
interocular delay elicited by stroboscopic stimulation has been shown
to be a potent source for depth perception (Burr & Ross, 1979).
There is also experimental evidence that cortical visual cells are
capable of signalling interocular temporal disparities. It has been
observed that some cortical cells of the cat modulate their response to
spatial disparity when interocular delay is added to the stimulus
(Pettigrew et al., 1968) and that they are selectively tuned to both
spatial and temporal disparities (Cynader et al., 1978; Gardner et al.,
1985). Interocular temporal delay generated by placing a ®lter before
one eye was associated with a shift in the tuning of cortical cells to
spatial disparity in cats, similar in magnitude to the Pulfrich effect in
humans (Carney et al., 1989). In agreement with these ®ndings, the
present study shows that there is a population of cells in monkey
visual area V1 sensitive to interocular stimulus delay.
The delay-sensitive cells we found are able to encode interocular
temporal disparity; this could be used to detect object trajectories in
depth. Indeed, a target which moves in front or behind the ®xation
point from left to right will stimulate a given corresponding retinal
area ®rst in one eye and then in the other eye. The delay will be a
function of the speed and trajectory of the target relative to the
®xation point. For cells with their left and right receptive ®elds in
register, a null delay would indicate that the target is on the horopter,
Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 2593±2595
Sensitivity to interocular temporal delay in macaque V1 2595
whereas a given delay would indicate that the target is moving in
front or behind the horopter. There is evidence that cortical cells may
have left and right receptive ®elds which are not in register in
monkeys (Hubel & Wiesel, 1970) and cats (Barlow et al., 1967; von
der Heydt et al., 1978; Ferster, 1981; Maske et al., 1984; Bishop &
Pettigrew, 1986). For these cells with disparate receptive ®elds a null
delay would indicate the target is moving on a plane in front or
behind the horopter matching their receptive ®eld disparity, whereas a
given delay would indicate the target is in front or behind this plane.
The cells we have termed symmetrical are unable to provide
information about the direction of motion of the object. In contrast,
asymmetrical cells would signal object trajectories off the plane
matching their receptive ®elds and would be able to detect which eye
was stimulated ®rst. Therefore they provide information about the
direction of motion. It is clear however, that additional information
on the position of the object relative to the horopter is needed to
de®ne the direction of movement fully.
The responses of symmetrical and asymmetrical cells are
consistent with the ®nding that some cortical visual cells in cats
may have equal or unequal latencies with the two eyes (Gardner et al.,
1985). If a neuron has facilitatory interocular interaction, is activated
with equal latencies from both eyes and its receptive ®elds are located
on corresponding retinal points, then the cell would be maximally
activated when the stimulus is on the horopter. This would be the case
with symmetrical cells. On the other hand, if one of the two eyes has
longer latency, an optimal response would be evoked when the
stimulus is moving in front or beyond the horopter, crossing the left
and right visual axis with a delay matching the eye latency. This
would be the case with asymmetrical cells.
The response pro®le of symmetrical cells was centred at zero
delay, whereas that of asymmetrical cells was centred at positive or
negative delays. The half-width of the temporal selectivity curves
varied from cell to cell, having an average duration of » 150 ms.
Although the delay between the stimulation of two corresponding
retinal points depends on the speed and trajectory of the stimulus, the
interaction time characteristics we observed suggest that the
sensitivity to interocular delay is more appropriate for detection of
trajectories of objects moving slowly on or around the horopter
(probably restricted to the Panum's area) or fast moving objects
moving off the horopter.
Our data indicate that the visual system is able to monitor the
temporal difference in the stimulation of points on the two retinas
which could account for depth perception and stereopsis. This
®nding emphasizes the similarities among different sensory
systems. For instance, experiments made in hearing showed that
small time differences between the stimulation of the left and
right ear induced a spatial shift in sound perception. Similar
results were obtained for taste stimulation on both sides of the
tongue and with odourous substances introduced to both nostrils
(von Bekesy, 1969). It must be pointed out however, that
interocular temporal disparity, by itself, does not provide enough
information to compute the trajectory of an object moving in
depth. However, the information available from both types of
delay-sensitive cells we have described here can be completed
with additional information about speed, direction of movement
and spatial disparity of the stimulus. There is currently plenty of
evidence that these parameters are accurately encoded by cortical
visual cells (Orban, 1991; Gonzalez & Perez, 1998).
Acknowledgements
This work was supported by grant PB97±0521 (DGESIC-PGC) from the
Spanish Ministerio de Educacion y Cultura.
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Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 2593±2595