Influence of oculomotor activity on visual processing

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Influence of oculomotor activity on visual processing Fhe maintenance of the spatial stability of the perceived visual world in the face of constant eye movements requires an interaction between incoming visual information and a 'corollary discharge '18 related to the internal generation of the eye movements. Interactions between saccadic eye movements and visual threshold have been demonstrated in man s,17, and have been found to be accompanied by changes in the visually evoked response (VER) 6,1°. Similar changes in the VER with eye movements have been reported in experimental animal preparations3, 9. Such changes presumably reflect alterations in the activity of individual neurons making up the visual pathway 4,5. Wurtz 14,15 has recently reported that neurons in the visual cortex of the monkey show no changes in their temporal firing pattern when a visual stimulus is associated with the voluntary eye movement and he concluded that the 'corollary discharge' has no effect on visual processing up to and including the striate cortex. However, Orban et al. 11, in a brief report, claim to have demonstrated an effect of eye movements on the information processing of visual cortical neurons. Oculomotor activity might be expected to alter the temporal firing pattern of a neuron in the visual system and/or to alter the receptive field of that neuron. Given that the function of these interactions is to maintain the spatial constancy of the visual world in the face of eye movements it seems reasonable to us that changes in the receptive field of the neuron are the more likely. An example of effects of this kind have been reported by Horn and Hill 7 who demonstrated changes in the spatial organization of the receptive fields in cats undergoing changes in body orientation. We have, therefore, determined the poststimulus time histograms (PSH) and the receptive fields of lateral geniculate (LGB) neurons during periods of oculomotor activity (OMA) and compared these to the same PSHs and receptive fields obtained when no OMA was occurring. The LGB was chosen for study because of reports by Bizzi 1 and Cohen et al. z that eye movements produce a slow potential in the LGB and that presynaptic inhibition of the optic nerve fibers occurs. In addition, Richards 12 has presented preliminary evidence that accommodative convergence can change visual processing carried out by LGB neurons. Single unit activity (extracellular) o f LGB neurons in enc6phale isol6 cats (prepared under sodium methohexatol anesthesia and treated with local anesthetics) was monitored in a conventional manner with tungsten microelectrodes. The electrocorticogram was recorded with a silver electrode on the surface of the posterior lateral gyrus. Neural pulse trains were analyzed and visual evoked responses obtained with the use o f an on-line, real-time computer system. Oculomotor activity was produced by continuous electrical stimulation of the lateral vestibular nucleus 16. The resulting eye movements were monitored with a reflected infrared technique. One eye was mechanically restrained so that visual stimuli could be delivered to a stationary retina; the other eye was left free to move but was occluded so that visual stimulation was monocular. Both eyes were fitted with contact lenses and the eye receiving visual stimuli was refracted so that stimuli were in sharp focus on the retina. Brain Research, 22 (1970) 249-253

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Action potential pulse trains were analyzed with a PDP-8 computer. Poststimulus time histograms were calculated in a conventional manner using a stroboscope flash to drive LGB neurons. Receptive fields were plotted using a small spot of light (approximately 0.2 °) flashed 'on' and 'off' on a cathode ray tube (CRT) placed in front of the cat. The spot sequentially occurred at each of the 100 positions in the 10 by 10 matrix (2 ° separation between positions). At each spot location the number of action potentials that occurred was counted. After 2-4 repetitions of the entire matrix a three-dimensional bar graph was displayed in which the height of each bar was proportional to the total number of action potentials that had occurred with the spot at that particular location. Two-dimensional 'maps' of the field were prepared by marking those locations at which there occurred activity equal to or greater than some predetermined percentage of the maximum activity found in the array. Visual evoked responses were elicited with a stroboscope and calculated with a small on-line averaging computer. At the beginning of each experiment VERs were elicited. In this and all other parts of the experiment, whenever O M A was present it was produced by continuous stimulation of the lateral vestibular nucleus (LVN). Eye movements were, of course, produced, but visual stimuli were not s y n c h r o n i z e d to the eye movements. Presentation of visual stimuli during periods of O M A resulted in the VERs that differed significantly from those elicited without O M A ; these changes though small were consistent, occurring on repeated paired trials, and similar to the changes in the VERs reported by Michael and Starkg, 10. An example of these responses can be seen in Fig. 1A. It is clear that some interaction between visual processing and oculomotor activity is occurring. A microelectrode was then advanced into the LGB contralateral to the eye receiving visual stimulation until the activity of a single neuron was being recorded. PHSs were then obtained with and without accompanying OMA. In each case, the occurrence of oculomotor activity produced no change in the temporal firing pattern

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Fig. 1. A, Visual evoked responses to stroboscope flashes obtained with and without accompanying oculomotor activity. The second peak at approximately 80 msec is greatly reduced when OMA is present. This difference, though small, is consistent. Furthermore, it is very similar to the responses reported by Michael and Stark 9,1°. B, Poststimulus time histograms (PSHs) for a single LGB neuron. The occurrence of OMA has no effect on the temporal firing pattern of this or other LGB units. Brain Research, 22 (1970) 249-253

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251

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Fig. 2. Receptive field maps of a neuron in the LGB. Those locations in the visual field are marked at which a stimulus produced neural activity falling in the indicated ranges. The lowest level indicated was chosen on the basis of a determination of the rate of spontaneous firing of this unit; 60~ is equivalent to an activity level two standard deviations greater than the spontaneous activity level. It is clear that there is no significant change in the organization of this field even though visual-oculomotor interactions were occurring as evidence by the change in the VER. The fields are not identical, but all of the prominent features do remain constant (the location of maximum activity at X = 6, Y = 8 and the 'hole' at X = 5, Y = 7). o f the L G B n e u r o n being monitored. A n example o f one such experiment can be seen in Fig. lB. The receptive field o f the neuron being recorded from was then determined with and without a c c o m p a n y i n g O M A . A n u m b e r o f paired trials ( O M A / n o O M A ) was obtained for each single unit studied. Finally, a measure o f the spontaneous activity o f the neuron was obtained for use in determining the activity levels to be displayed in the receptive field maps. N o n e o f the 12 units (in 4 cats) that have been studied demonstrated any change in the organization o f their receptive fields with the occurrence o f O M A . Fig. 2 contains 3 fields (with and without O M A ) from one unit studied; this field was located within 1-2 ° o f the area centralis and was approximately 8 ° × 8 ° in size. A l t h o u g h the 3 fields are not identical, there appears to be no significant difference between the fields with and without O M A ; the differences that are present are no longer than the differences observed on repeated control determinations. The change in the V E R f o u n d with O M A points to an interaction between visual processing and o c u l o m o t o r activity occurring somewhere in the central nervous system. The apparent failure to find any signs o f this interaction at the level o f single neurons in the L G B (as seen in the lack o f change in the P S H a n d the receptive field) suggests that other areas must be studied• The failure o f Wurtz14,15 to find evidence for this interaction at the level o f the striate cortex should, we believe, be regarded as provisional since he did not examine receptive field organization at this locus. Furthermore, it is not clear that the data processing carried out by W u r t z was sensitive e n o u g h to detect the subtle changes in the o u t p u t o f cortical neurons that might occur. The findings o f O r b a n et al. 12 support this contention. Given the role o f such interactions, it seems highly probable that oculomotor-visual interactions should be reflected in receptive field changes. Further studies are currently u n d e r w a y in our l a b o r a t o r y in which fields o f neurons in polysensory as well as striate and nonstriate visual areas are being monitored. A final c o m m e n t seems appropriate. Neither the locus o f stimulation for oculom o t o r activity (the vestibular system) nor the lack o f synchrony between visual stimuli Brain Research, 22 (1970) 249-253

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a n d eye m o v e m e n t s is a c c o u n t a b l e for our results; psychophysica115 a n d electrophysiologicala, a correlates of interactions between o c u l o m o t o r activity a n d visual processing have been d e m o n s t r a t e d with a variety o f ' i n v o l u n t a r y ' eye m o v e m e n t s , a n d changes in the V E R 9 a n d single u n i t responses 11 have previously been seen with n o n - s y n c h r o n ized visual stimulation. This supports the c o n t e n t i o n that signs of o c u l o m o t o r - v i s u a t interaction should be looked for at sites other t h a n the LGB. P o r t i o n s of this report were presented at the T h i r d I n t e r n a t i o n a l Biophysics Congress, A u g u s t 2 9 - S e p t e m b e r 3, 1969, Cambridge, Mass. This research was supported by U.S. Public Health Service Research G r a n t NB-8296. L.Y.I. was supported by a post-doctoral fellowship from N a t i o n a l Institutes o f M e n t a l Health I n t r a d i s c i p l i n a r y T r a i n i n g G r a n t MH8396 to the University of Illinois at the Medical Center. The authors are i n d e b t e d to G. M a s e k for assistance with the c o m p u t e r hardware a n d software a n d to R. G r o c h o w s k i for assistance with the experiments.

Department of Biomedical Engineering, Presbyterian-St. Luke's Hospital, Chicago, Ill. 60612, and Department of Physiology, University of Illinois at the Medical Center, Chicago, IlL 60680 (U.S.A.}

JOEL A. MICHAEL LESTER Y. ICHINOSE

1 BIZZI, E., Changes in the orthodromic and antidromic response of optic tract during the eye movements of sleep, J. Neurophysiol., 29 (1966) 861-870. 2 COHEN,B., FELDMAN, M., AND DIAMOND, S. P., Effects of eye movement, brain-stem stimulation, and alertness on transmission through lateral geniculate body of monkey, J. Neurophysiol., 32 (1969) 583-594. 3 COLLEWIJN,H., Changes in visual evoked responses during the fast phase of optokinetic nystagmus in the rabbit, Vision Res., 9 (1969) 803-814. 4 DILL, R. C., VALLECALLE,E., AND VERZEANO, M., Evoked potentials, neuronal activity and stimulus intensity in the visual system, Physiol. Behav., 3 0968) 289-293. 5 FOX, S. S., AND O'BRIEN, J. H., Duplication of evoked potential waveform by curve of probability of firing of a single cell, Science, 147 (1965) 888. 6 GROSS, E. G., VAUGHAN,H. G., JR., AND VALENSTEIN, E., Inhibition of visual evoked responses to patterned stimuli during voluntary eye movements, Electroenceph. clin. Neurophysiol., 22 (1967) 204-209. 7 HORN, G., AND HILL, R. M., Modifications of receptive fields of cells in the visual cortex occurring spontaneously and associated with bodily tilt, Nature (Lond.), 221 (1969) 186-188. 8 LATOUR, P. L., Visual threshold during eye movements, Vision Res., 2 (1962) 261-262. 9 MICHAEL, J. A., AND STARK,L., Interactions between eye movements and the visually evoked response in the cat, Electroenceph. din. NeurophysioL, 21 (1966) 478--488. 10 MICHAEL,J. A., AND STARK,L., Electrophysiological correlates of saccadic suppression, Exp. Neurol., 17 (1967) 233-246. 11 Om3AN,G., WZSSA~RT,R., AND CALLENS, M., Influence of brain stem oculomotor area stimulation on single unit activity in the visual cortex. Mathematical analysis of results, Brain Research, 17 (1970) 351-354. 12 RICHARDS, W., Spatial remapping in the primate visual system, Kybernetik, 4 (1968) 146-156. 13 SPERRY, R. W., Neural basis of the spontaneous optokinetic response produced by visual inversion, J. comp. physiol. PsychoL, 43 (1950) 482-489. 14 WURTZ,R. H., Response of striate cortex neurons to stimuli during rapid eye movements in the monkey, J. NeurophysioL, 32 (1969) 975-986. 15 WURTZ, R. H., Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey, J. Neurophysiol., 32 (1969) 987-994.

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16 YULES, R. B., AND GAULT, F. P., The relationship of nystagmus to lateral vestibular nucleus stimulation, Exp. Neurol., 15 (1966) 475-483. 17 ZUBER,B. L., AND STARK,L., Saccadic suppression: elevation of visual threshold associated with saccadic eye movements, Exp. Neurol., 16 (1966) 65-79. (Accepted June 1st, 1970)

Brain Research, 22 (1970) 249-253