- Email: [email protected]
Modulation of cell responses to horizontal disparities by ocular vergence in the visual cortex of the awake macaca mulatta monkey
Neuroscience Letters 245 (1998) 101–104
Modulation of cell responses to horizontal disparities by ocular vergence in the visual cortex of the awake macaca mulatta monkey Francisco Gonzalez a ,*, Rogelio Perez b a
Departamento de Fisiologia, Laboratorios ‘Ramon Dominguez’, Facultad de Medicina, E-15705 Santiago de Compostela, Spain b Servicio de Oftalmologia, Complejo Hospitalario Universitario de Santiago, Universidad de Santiago de Compostela, E-15705 Santiago de Compostela, Spain Received 6 February 1998; received in revised form 23 February 1998; accepted 23 February 1998
Abstract Horizontal retinal disparity is the most important cue for stereopsis. However, accurate stereoscopic perception requires additional information on fixation distance. The ocular vergence angle may provide information on fixation distance and therefore may be used to calibrate horizontal disparities. We studied the responses of cells from cortical visual area V1 of one macaca mulatta monkey to dynamic random dot stereograms at different ocular vergence angles. We observed that in about half of cells sensitive to horizontal disparity the vergence angle modifies the cell responses to horizontal disparities. These results suggest that vergence angle may be used to calibrate horizontal disparities for fixation distance. 1998 Elsevier Science Ireland Ltd.
Keywords: Stereopsis; Ocular vergence; Depth perception; Binocular vision; Monkey
It is well known that horizontal retinal disparities are a powerful cue to produce a vivid depth perception as it can be shown by viewing random dot stereograms [1,17]. There are cells in various visual cortical areas of the monkey that encode horizontal disparities and therefore represent a neural substrate for computing stereodepth in the visual system [4,11,12,14,15,22–25,27]. These disparity sensitive cells were grouped by Poggio et al. [23–25] into two main categories, tuned and reciprocal. Since horizontal disparities produced by two fixed points decrease with viewing distance, the visual system must calibrate horizontal disparity information for fixation distance in order to compute veridical stereoscopic depth. There is experimental evidence that changes in fixation distance modify the response of cortical cells to horizontal disparity and that these cells use vergence information to calibrate horizontal disparity for viewing distance [30,31]. Some reports suggest that vergence angle affects perceived depth [8,9,26]. Indeed, information about eye position could be obtained from corollary discharges or * Corresponding author. Tel.: +34 81 563100 ext. 12259; fax: +34 81 574145; e-mail: [email protected]
periocular proprioceptive feedback [26,28,29]. It has been shown that the early section of trigeminal afferents may disrupt depth perception in cats [13]. On the contrary, other reports suggest that vergence is not used for the computation of stereoscopic depth [32] and that humans do not perceive changes in depth when looking at random dot stereograms while vergence movements are induced [5]. To clarify whether the ocular vergence angle accounts for calibration of horizontal disparities we have investigated its effect on the responses of cells from cortical visual area V1 to dynamic random dot stereograms in one behaving rhesus monkey. The animal preparation, visual stimulation, cell activity recording and data analysis were essentially as described elsewhere [11,24] and are briefly outlined here. One male macaca mulatta monkey was trained to perform a task that required a steady binocular fixation on a small bright bar (0.2 deg) for a few seconds. The animal was sitting in a primate chair viewing separately with each eye two black and white monitors placed 57.7 cm away (Fig. 1). The displacements of the monitors induced symmetrical ocular convergence angles of 3.3, 4.3 and 6.3 deg that simulate fixation distances of 573, 440 and 300 mm, respectively. The background of the image was a dynamic
0304-3940/98/$19.00 1998 Elsevier Science Ireland Ltd. All rights reserved PII S0304- 3940(98) 00191- 8
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F. Gonzalez, R. Perez / Neuroscience Letters 245 (1998) 101–104
random dot pattern made up of a matrix of 320 × 200 pixels subtending 24.4 × 14 deg of visual angle. Horizontal disparity was created by shifting a small rectangular area in opposite directions on the left and right images [10]. Several craniotomies of 5 mm diameter were made under ketamine anesthesia (7 mg/kg, intramuscularly (i.m.)) to access the visual cortex with metal microelectrodes. To perform all major surgical procedures the monkey was anesthetized with sodium pentobarbital intravenously (27 mg/kg, induction by 25 mg ketamine i.m.). Postoperatively, antibiotics (Penicillin, 50.0 IU/kg) and analgesics (Noramidopirine 150 mg/kg; NOLOTIL, Europharma) were given i.m. All efforts were made to minimize animal suffering and the surgical and experimental procedures followed the guidelines of the Bioethic Committee of our institution. Coarse ocular movements were monitored by means of a videocamera under infrared illumination and the EOG recorded by two Ag–AgCl electrodes placed subcutaneously in the external rims of the orbits. Fine eye alignment was assessed by determining the receptive field position of the cell by means of reverse cross correlation [6,16,18,21]. Additionally, the cell responses to uncorrelation were used to ensure that both retinal images were in register [11,24]. The shape of the response profile (Figs 2 and 3) allowed us to include each cell in one of the categories described by
Fig. 1. Schematic representation of the experimental setup used in our experiments. Two black and white monitors were used to generate dynamic random dot stereograms and placed at a constant distance away from the eyes of the animal. Two cold mirrors allowed a separate view of each monitor. The broken lines indicate the visual axis of both eyes. The drawings below the monitors represent the left and right eye images. Each image was composed of background, figure and fixation target. The ‘stereo-figure’ is outlined for better clarity. Because the background and the figure had the same density of bright dots, the figure could be perceived only when horizontal disparity was present. Horizontal disparities were created by producing symmetrical horizontal shifts of the figure area on each monitor. To test the effect of vergence on horizontal disparity sensitivity both monitors and mirrors were rotated to vary the ocular vergence angle to simulate fixation distances of 573 (P1), 440 (P2) and 300 (P3) mm.
Fig. 2. Sensitivity to ocular vergence. (A) Response profile of a cell from area V1 to horizontal disparity at three symmetrical convergences, 3.3 deg (open circles), 4.3 deg (filled circles) and 6.3 deg (triangles). The responses are statistically different (ANOVA, P , 0.05) and had a correlation coefficient of 0.80 (3.3 vs. 4.3), 0.82 (3.3 vs. 6.3) and 0.79 (4.3 vs. 6.3). (B) Response profile of a cell from area V1 to horizontal disparities made at two convergence angles of 3.3 deg (open circles) and 4.3 deg (filled circles). The responses are statistically different (ANOVA, P , 0.05) with a correlation coefficient of 0.89. In (A) and (B) the cell response is represented as spikes per second and was calculated by dividing the number of elicited spikes by the time the stimulus was delivered. For each disparity the average of at least 10 stimulus presentations is presented. Vertical lines indicate the standard error. The stimulus was a stereogram with a rectangular figure of size 2 × 1 deg, with the long axis oriented at 90 deg and flashed over the cell’s receptive field for periods of 750 ms.
Poggio et al. [23–25]. Response profiles were determined at two or three ocular vergences. For each recorded cell the analysis of variance (ANOVA) and correlation coefficient were used to evaluate the effect of vergence on the response of the cell to horizontal disparity (P , 0.05). We studied the responses of 75 cells from V1 to horizontal disparities at two (n = 53) or three (n = 22) vergence angles. The eccentricity of the receptive field position ranged from 0.7 to 8.4 deg (mean 3.3 deg). About 25% (19/75) of the studied cells were responsive to horizontal disparities present in dynamic random dot stereograms. About half (10/ 19, 53%) of these cells showed a statistically different response profile to horizontal disparities when the vergence angle varied (ANOVA, P , 0.05). Two main changes in response were found. First, a change in amplitude of the peaking response (Fig. 2A) and second an offset of the cell response (Fig. 2B). These changes did not involve shifts in the disparity tuning of the cells since the preferred disparity remained constant. No cell was found to be sensitive to horizontal disparity at one particular vergence and not at other vergences. We did not find any evident relationship between the category of the cell regarding the sensitivity to horizontal disparity and the effect of eye vergence. The remaining half of disparity-sensitive cells (9/19, 47%) did not show statistically significant differences in their responses when the vergence angle varied (ANOVA, P , 0.05). Fig. 3 shows two of these vergence unsensitive cells. Sensitivity or unsensitivity to ocular vergence was not related to eccentricity of the cell receptive field. Among the cells whose activity was affected by the vergence angle two
F. Gonzalez, R. Perez / Neuroscience Letters 245 (1998) 101–104
Fig. 3. Unsensitivity to ocular vergence. (A) Response profile of a cell from area V1 to horizontal disparity at binocular symmetrical convergences of 3.3 (open circles) and 6.3 deg (filled circles). The cell response peaks for approximately -0.2 deg of crossed (near) disparity. The response is the same for both vergences. The correlation coefficient was 0.92. The responses are not statistically different (ANOVA, P , 0.05). (B) Response profile of a cell from area V1 to horizontal disparities made at vergence angles of 3.3 and 4.3 deg. In both cases the response is similar and peaks at −0.7 deg of crossed (near) disparity. The correlation coefficient was 0.97. The responses at both vergences are not statistically different (ANOVA, P , 0.05). In both cells the stimulus was similar to that used in Fig. 2. Both graphs were constructed as in Fig. 2.
were near, four were tuned inhibitory and four were tuned excitatory. Among those not affected by the vergence angle four were near, four were tuned inhibitory and one was tuned excitatory. Under our conditions of stimulation, there is almost a 2fold change in magnitude of perceived depth between the furthest and nearest simulated fixation distances (P1 and P3 in Fig. 1). Since the actual fixation distance did not vary, the response modulations we have observed should be attributed to proprioceptive or corollary neural activity related to the vergence angle. It is not clear why not all cells sensitive to horizontal disparity in our study are modulated by the vergence angle. A possible explanation would be that information about vergence angle is limited to near viewing distances [2]. Indeed, changes in fixation distance require larger vergence changes when the fixation distance is near. It is likely that for nearer distances than we have tested more disparity sensitive cells would be modulated by the vergence angle. Our results agree with the observations made in monkeys by Trotter et al. [31] that disparity-sensitive cells show changes in amplitude of response related to changes in vergence but rarely show changes in disparity selectivity category (only two cells out of 43 (,5%) in their report). These authors, by using prisms, demonstrated on a small sample of cells, that the changes they found were related to the vergence angle. Similar observations were reported by Roy et al. [27] in area MSTd who studied the disparity sensitivity of 20 cells under different vergence angles. They found that for most of them (75%, 15/20) no effect of ocular vergence on disparity sensitivity could be demonstrated but some (four cells) showed changes in amplitude similar as those we found in our study (Fig. 2A). According to our observations, the vergence angle mod-
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ulates the cell response in about half of cells sensitive to horizontal disparities recorded from V1. These results suggest that information about vergence could be used to calibrate horizontal disparity at this stage of the visual pathway. Buisseret and Maffei [3] found that stimulation of extraocular proprioceptive fibers evokes responses in 25% of the units of the striate cortex of the cat and that mechanical stretching of extraocular muscles evokes multiunit activity in the same area. There is also direct evidence of modulation of cell activity in the lateral geniculate nuclei by extraocular proprioceptive afferents in the cat [7,19,20]. According to these observations, the changes in sensitivity to horizontal disparity we found in V1 may have been caused by extraocular proprioceptive information related to the ocular vergence angle. We are grateful to F. Krause for his help in computer programming and to Luz Casas and Rosalı´a Gallego for their technical assistance. This work was supported by a grant XUGA20814B96. [1] Aschenbrenner, C.M., Problems in getting information into and out of air photographs, Photogramm. Eng., 20 (1954) 398–401. [2] Bishop, P.O., Size constancy, depth constancy and vertical disparities: a further quantitative interpretation, Biol. Cybern., 71 (1994) 37–47. [3] Buisseret, P. and Maffei, L., Extroacular proprioceptive projections to the visual cortex, Exp. Brain Res., 28 (1977) 421–425. [4] Burkhalter, A. and Van Essen, D.C., Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in macaque monkey, J. Neurosci., 6 (1986) 2327–2351. [5] Collewijn, H., Erkelens, C.J. and Regan, D., Absolute and relative disparity: a re-evaluation of their significance in perception and oculomotor control. In E.L. Keller and D.S. Ze (Eds.), Adaptative Processes in Visual and Oculomotor Systems, Pergamon, New York, 1986, pp. 177–184. [6] DeBoer, E. and Kuyper, P., Triggered correlation, IEEE Trans. Biomed. Eng., 15 (1968) 169–179. [7] Donaldson, I.M. and Dixon, R.A., Excitation of units in the lateral geniculate and contiguous nuclei of the cat by stretch of extrinsic ocular muscles, Exp. Brain Res., 38 (1980) 245–255. [8] Fisher, S.K. and Ebenholtz, S.M., Does perceptual adaptation to telestereoscopical enhanced depth depend on the recalibration of binocular disparity?, Percept. Psychophys., 40 (1986) 101–109. [9] Foley, J.M. and Richards, W., Effects of voluntary eye movement and convergence on the binocular appreciation of depth, Percept. Psychophys., 11 (1972) 423–427. [10] Gonzalez, F. and Krause, F., Generation of dynamic randomelement stereograms in real time with a system based on a personal computer, Med. Biol. Eng. Comput., 32 (1994) 373– 376. [11] Gonzalez, F., Krause, F., Perez, R., Alonso, J.M. and Acun˜a, C., Binocular matching in monkey visual cortex: single cell responses to correlated and uncorrelated stereograms, Neuroscience, 52 (1993) 933–939. [12] Gonzalez, F., Krause, F., Perez, R., Alonso, J.M. and Acun˜a, C., Cell responses to vertical disparity in the monkey visual cortex, Neurosci. Lett., 160 (1993) 167–170. [13] Graves, A.L., Trotter, Y. and Fregnac, Y., Role of extraocular muscle proprioception in the development of depth perception in cats, J. Neurophysiol., 58 (1987) 816–831.
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[14] Hubel, D.H. and Livingstone, M., Segregation of form, color and stereopsis in primate area 18, J. Neurosci., 7 (1987) 3378– 3415. [15] Hubel, D.H. and Wiesel, T.N., Cells sensitive to binocular depth in area 18 of the macaque monkey cortex, Nature, 225 (1970) 41–42. [16] Jones, J.P. and Palmer, L.A., The two-dimensional spatial structure of simple receptive fields in the cat striate cortex, J. Neurophysiol., 58 (1987) 1187–1211. [17] Julesz, B., Binocular depth perception of computer generated patterns, Bell Syst. Tech. J., 39 (1960) 1125–1162. [18] Krause, F., Gonzalez, F., Nelson, J.I. and Eckhorn, R., A fast method for predicting coding properties of visual cortical simple cells, Perception, 16 (1987) 269 (A45). [19] Lal, R. and Friedlander, M.J., Effect of passive eye position changes on retinogeniculate transmission in the cat, J. Neurophysiol., 63 (1990) 502–522. [20] Lal, R. and Friedlander, M.J., Gating of retinal transmission by afferent eye position and movement signals, Science, 243 (1989) 93–96. [21] Marmarelis, P.Z. and Marmarelis, V.Z., Analysis of Physiological Systems, Plenum, New York, 1978. [22] Maunsell, J.H.R. and Van Essen, D.C., Functional properties of neurons in middle temporal visual area of the macaque monkey. II. Binocular interaction and sensitivity to binocular disparity, J. Neurophysiol., 49 (1983) 1148–1167. [23] Poggio, G.F. and Fischer, B., Binocular interaction and depth sensitivity of striate and prestriate cortical neurons of the behaving rhesus monkey, J. Neurophysiol., 40 (1977) 1392– 1405.
[24] Poggio, G.F., Gonzalez, F. and Krause, F., Stereoscopic mechanisms in monkey visual cortex: binocular correlation and disparity selectivity, J. Neurosci., 8 (1988) 4531–4550. [25] Poggio, G.F., Motter, B.C., Squatrito, S. and Trotter, Y., Responses of neurons in visual cortex (V1 and V2) of the alert macaque to dynamic random-dot stereograms, Vision Res., 25 (1985) 397–406. [26] Ritter, M., Effect of disparity and viewing distance on perceived depth, Percept. Psychophys., 22 (1977) 400–407. [27] Roy, J.P., Komatsu, H. and Wurtz, R.H., Disparity sensitivity of neurons in monkey extraextriate area MST, J. Neurosci., 12 (1992) 2478–2492. [28] Steinbach, M.S., Proprioceptive knowledge of eye position, Vision Res., 27 (1987) 1737–1744. [29] Toyama, K., Komatsu, Y. and Shibuki, K., Integration of retinal and motor signals of eye movements in striate cortex cells of the alert cat, J. Neurophysiol., 51 (1984) 649–665. [30] Trotter, Y., Celebrini, S., Stricanne, B., Thorpe, S. and Imbert, M., Modulation of neural stereoscopic processing in primate area V1 by the viewing distance, Science, 257 (1992) 1279– 1281. [31] Trotter, Y., Celebrini, S., Stricanne, B., Thorpe, S. and Imbert, M., Neural processing of stereopsis as a function of viewing distance in primate visual cortical area V1, J. Neurophysiol., 76 (1996) 2872–2885. [32] Tychsen, L., Binocular Vision. In W.M. Hart Jr. (Ed.), Adler’s Physiology of the Eye, 9th edn., Mosby Year Book, St. Louis, MO, 1992, pp. 773–853.
Modulation of cell responses to horizontal disparities by ocular vergence in the visual cortex of the awake macaca mulatta monkey Francisco Gonzalez a ,*, Rogelio Perez b a
Departamento de Fisiologia, Laboratorios ‘Ramon Dominguez’, Facultad de Medicina, E-15705 Santiago de Compostela, Spain b Servicio de Oftalmologia, Complejo Hospitalario Universitario de Santiago, Universidad de Santiago de Compostela, E-15705 Santiago de Compostela, Spain Received 6 February 1998; received in revised form 23 February 1998; accepted 23 February 1998
Abstract Horizontal retinal disparity is the most important cue for stereopsis. However, accurate stereoscopic perception requires additional information on fixation distance. The ocular vergence angle may provide information on fixation distance and therefore may be used to calibrate horizontal disparities. We studied the responses of cells from cortical visual area V1 of one macaca mulatta monkey to dynamic random dot stereograms at different ocular vergence angles. We observed that in about half of cells sensitive to horizontal disparity the vergence angle modifies the cell responses to horizontal disparities. These results suggest that vergence angle may be used to calibrate horizontal disparities for fixation distance. 1998 Elsevier Science Ireland Ltd.
Keywords: Stereopsis; Ocular vergence; Depth perception; Binocular vision; Monkey
It is well known that horizontal retinal disparities are a powerful cue to produce a vivid depth perception as it can be shown by viewing random dot stereograms [1,17]. There are cells in various visual cortical areas of the monkey that encode horizontal disparities and therefore represent a neural substrate for computing stereodepth in the visual system [4,11,12,14,15,22–25,27]. These disparity sensitive cells were grouped by Poggio et al. [23–25] into two main categories, tuned and reciprocal. Since horizontal disparities produced by two fixed points decrease with viewing distance, the visual system must calibrate horizontal disparity information for fixation distance in order to compute veridical stereoscopic depth. There is experimental evidence that changes in fixation distance modify the response of cortical cells to horizontal disparity and that these cells use vergence information to calibrate horizontal disparity for viewing distance [30,31]. Some reports suggest that vergence angle affects perceived depth [8,9,26]. Indeed, information about eye position could be obtained from corollary discharges or * Corresponding author. Tel.: +34 81 563100 ext. 12259; fax: +34 81 574145; e-mail: [email protected]
periocular proprioceptive feedback [26,28,29]. It has been shown that the early section of trigeminal afferents may disrupt depth perception in cats [13]. On the contrary, other reports suggest that vergence is not used for the computation of stereoscopic depth [32] and that humans do not perceive changes in depth when looking at random dot stereograms while vergence movements are induced [5]. To clarify whether the ocular vergence angle accounts for calibration of horizontal disparities we have investigated its effect on the responses of cells from cortical visual area V1 to dynamic random dot stereograms in one behaving rhesus monkey. The animal preparation, visual stimulation, cell activity recording and data analysis were essentially as described elsewhere [11,24] and are briefly outlined here. One male macaca mulatta monkey was trained to perform a task that required a steady binocular fixation on a small bright bar (0.2 deg) for a few seconds. The animal was sitting in a primate chair viewing separately with each eye two black and white monitors placed 57.7 cm away (Fig. 1). The displacements of the monitors induced symmetrical ocular convergence angles of 3.3, 4.3 and 6.3 deg that simulate fixation distances of 573, 440 and 300 mm, respectively. The background of the image was a dynamic
0304-3940/98/$19.00 1998 Elsevier Science Ireland Ltd. All rights reserved PII S0304- 3940(98) 00191- 8
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F. Gonzalez, R. Perez / Neuroscience Letters 245 (1998) 101–104
random dot pattern made up of a matrix of 320 × 200 pixels subtending 24.4 × 14 deg of visual angle. Horizontal disparity was created by shifting a small rectangular area in opposite directions on the left and right images [10]. Several craniotomies of 5 mm diameter were made under ketamine anesthesia (7 mg/kg, intramuscularly (i.m.)) to access the visual cortex with metal microelectrodes. To perform all major surgical procedures the monkey was anesthetized with sodium pentobarbital intravenously (27 mg/kg, induction by 25 mg ketamine i.m.). Postoperatively, antibiotics (Penicillin, 50.0 IU/kg) and analgesics (Noramidopirine 150 mg/kg; NOLOTIL, Europharma) were given i.m. All efforts were made to minimize animal suffering and the surgical and experimental procedures followed the guidelines of the Bioethic Committee of our institution. Coarse ocular movements were monitored by means of a videocamera under infrared illumination and the EOG recorded by two Ag–AgCl electrodes placed subcutaneously in the external rims of the orbits. Fine eye alignment was assessed by determining the receptive field position of the cell by means of reverse cross correlation [6,16,18,21]. Additionally, the cell responses to uncorrelation were used to ensure that both retinal images were in register [11,24]. The shape of the response profile (Figs 2 and 3) allowed us to include each cell in one of the categories described by
Fig. 1. Schematic representation of the experimental setup used in our experiments. Two black and white monitors were used to generate dynamic random dot stereograms and placed at a constant distance away from the eyes of the animal. Two cold mirrors allowed a separate view of each monitor. The broken lines indicate the visual axis of both eyes. The drawings below the monitors represent the left and right eye images. Each image was composed of background, figure and fixation target. The ‘stereo-figure’ is outlined for better clarity. Because the background and the figure had the same density of bright dots, the figure could be perceived only when horizontal disparity was present. Horizontal disparities were created by producing symmetrical horizontal shifts of the figure area on each monitor. To test the effect of vergence on horizontal disparity sensitivity both monitors and mirrors were rotated to vary the ocular vergence angle to simulate fixation distances of 573 (P1), 440 (P2) and 300 (P3) mm.
Fig. 2. Sensitivity to ocular vergence. (A) Response profile of a cell from area V1 to horizontal disparity at three symmetrical convergences, 3.3 deg (open circles), 4.3 deg (filled circles) and 6.3 deg (triangles). The responses are statistically different (ANOVA, P , 0.05) and had a correlation coefficient of 0.80 (3.3 vs. 4.3), 0.82 (3.3 vs. 6.3) and 0.79 (4.3 vs. 6.3). (B) Response profile of a cell from area V1 to horizontal disparities made at two convergence angles of 3.3 deg (open circles) and 4.3 deg (filled circles). The responses are statistically different (ANOVA, P , 0.05) with a correlation coefficient of 0.89. In (A) and (B) the cell response is represented as spikes per second and was calculated by dividing the number of elicited spikes by the time the stimulus was delivered. For each disparity the average of at least 10 stimulus presentations is presented. Vertical lines indicate the standard error. The stimulus was a stereogram with a rectangular figure of size 2 × 1 deg, with the long axis oriented at 90 deg and flashed over the cell’s receptive field for periods of 750 ms.
Poggio et al. [23–25]. Response profiles were determined at two or three ocular vergences. For each recorded cell the analysis of variance (ANOVA) and correlation coefficient were used to evaluate the effect of vergence on the response of the cell to horizontal disparity (P , 0.05). We studied the responses of 75 cells from V1 to horizontal disparities at two (n = 53) or three (n = 22) vergence angles. The eccentricity of the receptive field position ranged from 0.7 to 8.4 deg (mean 3.3 deg). About 25% (19/75) of the studied cells were responsive to horizontal disparities present in dynamic random dot stereograms. About half (10/ 19, 53%) of these cells showed a statistically different response profile to horizontal disparities when the vergence angle varied (ANOVA, P , 0.05). Two main changes in response were found. First, a change in amplitude of the peaking response (Fig. 2A) and second an offset of the cell response (Fig. 2B). These changes did not involve shifts in the disparity tuning of the cells since the preferred disparity remained constant. No cell was found to be sensitive to horizontal disparity at one particular vergence and not at other vergences. We did not find any evident relationship between the category of the cell regarding the sensitivity to horizontal disparity and the effect of eye vergence. The remaining half of disparity-sensitive cells (9/19, 47%) did not show statistically significant differences in their responses when the vergence angle varied (ANOVA, P , 0.05). Fig. 3 shows two of these vergence unsensitive cells. Sensitivity or unsensitivity to ocular vergence was not related to eccentricity of the cell receptive field. Among the cells whose activity was affected by the vergence angle two
F. Gonzalez, R. Perez / Neuroscience Letters 245 (1998) 101–104
Fig. 3. Unsensitivity to ocular vergence. (A) Response profile of a cell from area V1 to horizontal disparity at binocular symmetrical convergences of 3.3 (open circles) and 6.3 deg (filled circles). The cell response peaks for approximately -0.2 deg of crossed (near) disparity. The response is the same for both vergences. The correlation coefficient was 0.92. The responses are not statistically different (ANOVA, P , 0.05). (B) Response profile of a cell from area V1 to horizontal disparities made at vergence angles of 3.3 and 4.3 deg. In both cases the response is similar and peaks at −0.7 deg of crossed (near) disparity. The correlation coefficient was 0.97. The responses at both vergences are not statistically different (ANOVA, P , 0.05). In both cells the stimulus was similar to that used in Fig. 2. Both graphs were constructed as in Fig. 2.
were near, four were tuned inhibitory and four were tuned excitatory. Among those not affected by the vergence angle four were near, four were tuned inhibitory and one was tuned excitatory. Under our conditions of stimulation, there is almost a 2fold change in magnitude of perceived depth between the furthest and nearest simulated fixation distances (P1 and P3 in Fig. 1). Since the actual fixation distance did not vary, the response modulations we have observed should be attributed to proprioceptive or corollary neural activity related to the vergence angle. It is not clear why not all cells sensitive to horizontal disparity in our study are modulated by the vergence angle. A possible explanation would be that information about vergence angle is limited to near viewing distances [2]. Indeed, changes in fixation distance require larger vergence changes when the fixation distance is near. It is likely that for nearer distances than we have tested more disparity sensitive cells would be modulated by the vergence angle. Our results agree with the observations made in monkeys by Trotter et al. [31] that disparity-sensitive cells show changes in amplitude of response related to changes in vergence but rarely show changes in disparity selectivity category (only two cells out of 43 (,5%) in their report). These authors, by using prisms, demonstrated on a small sample of cells, that the changes they found were related to the vergence angle. Similar observations were reported by Roy et al. [27] in area MSTd who studied the disparity sensitivity of 20 cells under different vergence angles. They found that for most of them (75%, 15/20) no effect of ocular vergence on disparity sensitivity could be demonstrated but some (four cells) showed changes in amplitude similar as those we found in our study (Fig. 2A). According to our observations, the vergence angle mod-
103
ulates the cell response in about half of cells sensitive to horizontal disparities recorded from V1. These results suggest that information about vergence could be used to calibrate horizontal disparity at this stage of the visual pathway. Buisseret and Maffei [3] found that stimulation of extraocular proprioceptive fibers evokes responses in 25% of the units of the striate cortex of the cat and that mechanical stretching of extraocular muscles evokes multiunit activity in the same area. There is also direct evidence of modulation of cell activity in the lateral geniculate nuclei by extraocular proprioceptive afferents in the cat [7,19,20]. According to these observations, the changes in sensitivity to horizontal disparity we found in V1 may have been caused by extraocular proprioceptive information related to the ocular vergence angle. We are grateful to F. Krause for his help in computer programming and to Luz Casas and Rosalı´a Gallego for their technical assistance. This work was supported by a grant XUGA20814B96. [1] Aschenbrenner, C.M., Problems in getting information into and out of air photographs, Photogramm. Eng., 20 (1954) 398–401. [2] Bishop, P.O., Size constancy, depth constancy and vertical disparities: a further quantitative interpretation, Biol. Cybern., 71 (1994) 37–47. [3] Buisseret, P. and Maffei, L., Extroacular proprioceptive projections to the visual cortex, Exp. Brain Res., 28 (1977) 421–425. [4] Burkhalter, A. and Van Essen, D.C., Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in macaque monkey, J. Neurosci., 6 (1986) 2327–2351. [5] Collewijn, H., Erkelens, C.J. and Regan, D., Absolute and relative disparity: a re-evaluation of their significance in perception and oculomotor control. In E.L. Keller and D.S. Ze (Eds.), Adaptative Processes in Visual and Oculomotor Systems, Pergamon, New York, 1986, pp. 177–184. [6] DeBoer, E. and Kuyper, P., Triggered correlation, IEEE Trans. Biomed. Eng., 15 (1968) 169–179. [7] Donaldson, I.M. and Dixon, R.A., Excitation of units in the lateral geniculate and contiguous nuclei of the cat by stretch of extrinsic ocular muscles, Exp. Brain Res., 38 (1980) 245–255. [8] Fisher, S.K. and Ebenholtz, S.M., Does perceptual adaptation to telestereoscopical enhanced depth depend on the recalibration of binocular disparity?, Percept. Psychophys., 40 (1986) 101–109. [9] Foley, J.M. and Richards, W., Effects of voluntary eye movement and convergence on the binocular appreciation of depth, Percept. Psychophys., 11 (1972) 423–427. [10] Gonzalez, F. and Krause, F., Generation of dynamic randomelement stereograms in real time with a system based on a personal computer, Med. Biol. Eng. Comput., 32 (1994) 373– 376. [11] Gonzalez, F., Krause, F., Perez, R., Alonso, J.M. and Acun˜a, C., Binocular matching in monkey visual cortex: single cell responses to correlated and uncorrelated stereograms, Neuroscience, 52 (1993) 933–939. [12] Gonzalez, F., Krause, F., Perez, R., Alonso, J.M. and Acun˜a, C., Cell responses to vertical disparity in the monkey visual cortex, Neurosci. Lett., 160 (1993) 167–170. [13] Graves, A.L., Trotter, Y. and Fregnac, Y., Role of extraocular muscle proprioception in the development of depth perception in cats, J. Neurophysiol., 58 (1987) 816–831.
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[14] Hubel, D.H. and Livingstone, M., Segregation of form, color and stereopsis in primate area 18, J. Neurosci., 7 (1987) 3378– 3415. [15] Hubel, D.H. and Wiesel, T.N., Cells sensitive to binocular depth in area 18 of the macaque monkey cortex, Nature, 225 (1970) 41–42. [16] Jones, J.P. and Palmer, L.A., The two-dimensional spatial structure of simple receptive fields in the cat striate cortex, J. Neurophysiol., 58 (1987) 1187–1211. [17] Julesz, B., Binocular depth perception of computer generated patterns, Bell Syst. Tech. J., 39 (1960) 1125–1162. [18] Krause, F., Gonzalez, F., Nelson, J.I. and Eckhorn, R., A fast method for predicting coding properties of visual cortical simple cells, Perception, 16 (1987) 269 (A45). [19] Lal, R. and Friedlander, M.J., Effect of passive eye position changes on retinogeniculate transmission in the cat, J. Neurophysiol., 63 (1990) 502–522. [20] Lal, R. and Friedlander, M.J., Gating of retinal transmission by afferent eye position and movement signals, Science, 243 (1989) 93–96. [21] Marmarelis, P.Z. and Marmarelis, V.Z., Analysis of Physiological Systems, Plenum, New York, 1978. [22] Maunsell, J.H.R. and Van Essen, D.C., Functional properties of neurons in middle temporal visual area of the macaque monkey. II. Binocular interaction and sensitivity to binocular disparity, J. Neurophysiol., 49 (1983) 1148–1167. [23] Poggio, G.F. and Fischer, B., Binocular interaction and depth sensitivity of striate and prestriate cortical neurons of the behaving rhesus monkey, J. Neurophysiol., 40 (1977) 1392– 1405.
[24] Poggio, G.F., Gonzalez, F. and Krause, F., Stereoscopic mechanisms in monkey visual cortex: binocular correlation and disparity selectivity, J. Neurosci., 8 (1988) 4531–4550. [25] Poggio, G.F., Motter, B.C., Squatrito, S. and Trotter, Y., Responses of neurons in visual cortex (V1 and V2) of the alert macaque to dynamic random-dot stereograms, Vision Res., 25 (1985) 397–406. [26] Ritter, M., Effect of disparity and viewing distance on perceived depth, Percept. Psychophys., 22 (1977) 400–407. [27] Roy, J.P., Komatsu, H. and Wurtz, R.H., Disparity sensitivity of neurons in monkey extraextriate area MST, J. Neurosci., 12 (1992) 2478–2492. [28] Steinbach, M.S., Proprioceptive knowledge of eye position, Vision Res., 27 (1987) 1737–1744. [29] Toyama, K., Komatsu, Y. and Shibuki, K., Integration of retinal and motor signals of eye movements in striate cortex cells of the alert cat, J. Neurophysiol., 51 (1984) 649–665. [30] Trotter, Y., Celebrini, S., Stricanne, B., Thorpe, S. and Imbert, M., Modulation of neural stereoscopic processing in primate area V1 by the viewing distance, Science, 257 (1992) 1279– 1281. [31] Trotter, Y., Celebrini, S., Stricanne, B., Thorpe, S. and Imbert, M., Neural processing of stereopsis as a function of viewing distance in primate visual cortical area V1, J. Neurophysiol., 76 (1996) 2872–2885. [32] Tychsen, L., Binocular Vision. In W.M. Hart Jr. (Ed.), Adler’s Physiology of the Eye, 9th edn., Mosby Year Book, St. Louis, MO, 1992, pp. 773–853.