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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. References Barlow, H.B., Blakemore, C. & Pettigrew, J.D. (1967) The neural mechanism of binocular depth discrimination. J. Physiol. (Lond.), 193, 327±342. von Bekesy, G. 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Pettigrew, J.D., Nikara, T. & Bishop, P.O. (1968) Binocular interaction on single units in cat striate cortex: simultaneous stimulation by single moving slit with receptive ®elds in correspondence. Exp. Brain Res., 6, 391±410. Wist, E.R. (1968) The in¯uence of the equidistance tendency on depth shifts resulting from an interocular delay in stimulation. Perception Psychophysics, 8, 89±92. Ó 1999 European Neuroscience Association, European Journal of Neuroscience, 11, 2593±2595