Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. R H Wurtz
J Neurophysiol 32:987-994, 1969. ; You might find this additional info useful... This article has been cited by 16 other HighWire-hosted articles: http://jn.physiology.org/content/32/6/987.citation#cited-by
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Comparison
of Effects of Eye Movements
Movements
on Striate Cortex Neurons of the Monkey
ROBERT Laboratory National
H. WURTZ of Neurobiology, Institutes of Health,
National Bethesda,
Institute Maryland
IMAGE
MOVES
with
respect
both when our eves move
Received
for
publication
April
4, 1969.
of Mental 20014
Health,
METHODS
Two rhesus monkeys, Macaca mulatta, were used in these experiments. The methods used for training the monkey to look at a fixation point, for restraining the monkey, and for recording unit activity have been described in detail (4-6, 23). For each unit studied there were three experimental steps. First, the receptive-field characteristics of the unit were determined, sometimes only approximately. The units considered in this report gave excitatory responses to a stationary or slowly moving slit of light, had receptive fields located around the fovea1 area with circular, simple, or complex organization (when such detail was determined), and were in the striate cortex (as verified from histological sections after the experiments). Second, a rapid 20” eye movement across a stationary stimulus was elicited. The stimulus was somewhat longer than the most effective stationary slit of light and was placed so that the receptive field of the unit crossed it at the midpoint of the eye movement. Other details of steps one and two were the same as in the preceding experiments (24). Finally, the monkey held its eyes stationary during a fixation period and the same stimulus was moved rapidly across the receptive field. The slit of light produced by the projector was reflected off a mirror onto the screen in front of the monkey. The mirror was mounted on the stem of a galvanometer so that it could be rotated rapidly to produce stimulus movements as rapid as eye movements. Slower rates of movement could also be produced by movement of the galvanometer or the projector. Rate of movement was measured by passing the moving slit of light over two photocells a known distance apart, measuring the time interval between the crossings, and computing the rate of movement. Comparisons of the unit responses following eye movements and stimulus movements were made when the direction of image movement across the retina was the same. For example, unit responses following eye move987
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to the retina a nd when the object moves, but in one case we perceive a stationary object, in the other case a moving object. How can we tell the difference? One approach to this question was proposed by Helmholtz (10) over a century ago. He suggested that when efferent impulses go to the eye muscles, other impulses go simultaneously to areas within the brain. The impulses to the brain would indicate that an eye movement is occurring and that movement of the image with respect to the retina is due to movement of the eye and not to movement of the object. W. James (12) vigorously disputed this hypothesis, but similar hypotheses have been suggested to explain how an insect differentiates between its own movement and movement generated by external forces (1 1), why salamanders make continuous circling movements after eye rotation (Is), and how stability of perceived space is maintained in man (19). The impulses from a motor area to a sensory system have been referred to as a “corollary discharge” (18, 19). If such a corollary discharge exists, one would expect to see a difference at some point in the visual system in the neural response depending on whether the retina moves past a stationary image or whether the image moves across a stationary retina. The purpose of the present experiments was to see whether in striate cortex neurons there is any difference between the response to rapid eye movements across a stationary stimulus and the response to rapid stimulus movements across a stationary eye. A brief report of these experiments has been published previously (22). AN
and Stimulus
R. H. WURTZ
988 ments from left to responses following right to left.
right were compared stimulus movements
with from
Some of the units in these experiments included in previous reports on receptive (23) and responses during eye movement
were fields (24).
RESULTS
Eye and stimulus
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FIG. 1. Response of a unit that continued to give an excitatory response during rapid eye movements (A) and during equally rapid stimulus movements (B). In A, the upper trace is an oculogram of a horizontal eye movement. The 200 eye movement (represented at the beginning of the line) swept the receptive field of the unit across the stationary stimulus. The eye movement triggered the sweep of the oscilloscope, which displayed unit responses as dots by intensifying the beam with each unit discharge. The beginning and end of each line is also indicated by dots. Successive lines of dots represent unit responses associated with successive eye movements. In B, a photocell triggered the sweep of the oscilloscope as the rapidly moving stimulus crossed over the stationary receptive field; successive lines display unit responses following successive stimulus movements. In this and succeeding figures, each time-scale interval represents 50 mscc; entire line is 400 msec.
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The response of each of 142 units to an effective stimulus during a rapid eye movement was determined. Each unit could be placed into one of the three categories considered in the previous paper (24), based on the type of response produced as the receptive field of the unit passed over the effective stimulus during a rapid eye movement: I) units that responded with a burst of discharges, 2) units that failed to respond, and 3) units that responded with a suppression of activity. Figures 1, 2, and 3 illustrate the three types of unit response and permit comparison in each case of the response following rapid eye movement with the response following rapid stimulus movement. The response of one of the units that gave an excitatory response during a rapid eye movement is illustrated in Fig. 1A. The top trace is an electrooculogram showing a 20” horizontal rapid eye movement. The eye movement is indicated at the start of each line, and the receptive field of the unit crosses the stationary stimulus at about the midpoint of the eye movement. Each unit discharge is represented by a dot (produced by intensifying the beam of the oscilloscope), and the unit discharges associated with successive eye movements are presented on successive lines (produced by successive displaced sweeps of the oscilloscope). Each time the receptive field moved across the stimulus during an eye movement there was a burst of unit discharges. The response of this same unit is shown in Fig. lB, but here the eye was stationary and the stimulus moved. The rate of stimulus movement was about 900”/sec, comparable to that of the eye as it moved across the stimulus at the midpoint of a 20” rapid eye movement (8). As the stimulus moved it passed first over a photocell and then over the receptive field of the unit. The output of the photocell (one of the
pair used to determine rate of stimulus movement) triggered the sweep of the oscilloscope, and successive lines were produced by successive stimulus movements. The brief burst of unit responses following each stimulus movement (Fig. 1B) was similar to the burst following each eye movement (Fig. 1~2). Experiments with stimulus movement at 900”/sec were done on 33 units that gave excitatory responses during eye movement across a stimulus. The response of each unit following a stimulus movement was similar to its response following an eye movement. For an additional 16 units giving an excitatory response the
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FIG 2. A unit not responding during rapid eye movements (A) and rapid stimulus movements (U). Unit responses are indicated by dots; responses following successive eye or stimulus movements are shown on successive lines.
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FIG. 3. Suppression of rcsponsc of a unit during rapid eye movements (A) and rapid stimulus movcments (B). Dots represent unit responses, successive lines represent responses following successive eye or stimulus movements.
Rate
of stimulus
movement
The responses of striate cortex neurons to eye movement across a stationary stimulus and to stimulus movement in front of a stationary eye were remarkably similar. This similarity indicated that the responses resulted from rapid movement, regardless of whether the eye or the stimulus moved. To demonstrate further that any differences between the response of a unit to slow and rapid stimulus movements resulted simply from the change in rate of movement, the responses of 3’2 units were studied for a series of stimulus speeds ranging from several degrees per set up to 900” /sec. For units that gave an excitatory response during eye movement, Fig. 4A illustrates the change of response that occurred with increasing speed of stimulus movement. Successive lines in the figure were produced by successive stimulus movements. After the stimulus was moved across the receptive field a number of times at lOO/sec, the rate of movement was increased to 20” /set for another series of stimulus movements. This procedure was repeated for movements up to 900°/sec. The response (in Fig. 4A) con-
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stimulus was moved only as fast as 200” /set, and there was an excitatory response up to this speed. A unit that gave no response following an eye movement across a stationary stimulus is shown in Fig. 2A. The response of this unit following rapid stimulus movement (Fig. 2B) was similar to its response following rapid eye movement. All 54 nonresponding units for which responses followingeye movement and stimulus movement w&e compared gave the same result. The stimulus was moved at a maximum rate of 2OO”/sec for another 16 nonresponding units, and all failed to respond at this speed. The rate of discharge of the unit shown in Fig. 3A was suppressed following an eye movement, and with the eye stationary the same suppression was observed when the stimulus was moved as rapidly as the eye had moved (Fig. 3B). The same comparison was made for each of 23 units showing suppression following eye movement across a stationary stimulus, and all showed suppression with both eye and rapid stimulus movement.
STIMULUS
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tinued to be excitatory with movements between 10 and 900”/sec. With increased speed of movement, the duration of the response decreased, but more discharges usually occurred per unit time. The decrease in latency at successive speeds of movement was accounted for in large part by the progressively shorter intervals between the time the stimulus crossed the photocell and the time it reached the receptive field. (The trigger of the sweep for the lOO/sec records was delayed 110 msec to permit the response to appear within the 400-msec period.) The response of this same unit to an eye movement across a stationary stimulus is shown in Fig. 413 for comparison. The units that did not respond during an eye movement all failed to respond with stimulus movement above 150°/sec. For example, the unit illustrated in Fig. 5A gave a clear excitatory response with movement of the stimulus up to SO”/sec but little response to movement at 150” /set and none above 150”/sec. The unit failed to respond following an eye movement (Fig. 5B). Other units ceased responding at lower rates of stimulus movement, including some that responded to a moving stimulus but stopped responding when the stimulus moved at only 20-4-O” /sec. Since the stimulus was on the receptive field for shorter periods as the rate of stimulus movement increased, an increasingly brief response or no response at all was not surprising. But whether the change in response was related just to the decreased time on the receptive field or to the more rapid movement across the field would require further experiments to compare the response to a flashed stationary stimulus with the response to a rapidly moving stimulus. The change from an excitatory response with slow stimulus movement to a suppression response with fast stimulus movement is illustrated in Fig. 6A. With stimulus movement at only 1O” /set, there was a clear excitatory response (sweep delayed 140 msec to permit response to appear) and at 2040”/sec a slight excitatory response. Stimulus movement at 80”/sec gave no clear response either of excitation or of suppression. At ltiO”/sec a suppression was barely
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detectable; it became clearer at 300 and 500” /set; at 900” /set the suppression was comparable to that following rapid eye movements across a stationary stimulus (Fig. 6B). In the suppression-response units, the excitatory response to slow stimulus movement faded out with rates of movement at or below 150°/sec; with slightly higher rates
STIMULUS
MOVEMENT
991
of movement there was no clear response either of excitation or of inhibition; with still higher rates of stimulus movement, ranging as low as 150”/sec for some units but as high as 500 or 900”/sec for other
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FIG. 5. Failure of a unit to respond to rapid movement of the stimulus. In A, response of the unit has become undetectable with stimulus movements above 150°/sec. Rate of stimulus movement is indicated in O/set on left. In B, lack of response of same unit following a rapid eye movement is shown.
FIG. 6. Transformation of an excitatory response to a suppression response with increasing rates of stimulus movement. In A there are clear excitatory responses with slow stimulus movements (lo-40°/ set) , suppression responses with rapid stimulus movements (barely detectable at 150°/sec, clear at 300-900°/sec), and ambiguous responses in between (80°/sec). In B, suppression response follows an eye movement across the stationary stimulus.
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.
992
R. H. WURTZ
units, the suppression response became evident. What mechanism converts the exci tatorv response into a suppression response with increasing speed of stimulus movement has not been determined. One possible factor might be that in some way the slowly moving stimulus produces its excitatory effect by activating mainly the excitatory center of the receptive field whereas the rapidly moving stimulus produces its suppressive effect by stimulating an antagonistic surround or adjacent area.
If there were a corollary discharge to the neurons of striate cortex, the eiect of a stimulus on these neurons during eye movement should be different from that during stimulus movement. No such difference was detected, which suggests that there is no corollary discharge ;o striate cortex neurons during , the rapid eye movements of wakefulne& In addition, no corollary discharge is necessary to explain the dramatic changes in response between slow stimulus movement and rapid stimulus or eye movements. These changes were directly related to speed of movement since a stepwise increase in speed of stimulus movement produced a gradual alteration in the response of the neurons. Finally, there was no indication of a corollary discharge associated with eye movements alone since eye movements in the absence of a stimulus failed to produce a response in striate cortex neurons
(24) . ..
The similarity of the response of cortical neurons during rapid eye and stimulus movement also argues against a corollary discharge that impinges on the lateral geniculate nucleus. Since in the primate visual system the cells of the lateral geniculate nucleus project massively to striate cortex (14), the effect of a corollary discharge at a more peripheral level would presumably have shown up as a difference in single neuron activity at the cortex during eye and stimulus movements. This apparent absence of a corollary discharge at the lateral geniculate nucleus is surprising since in the cat Bizzi (1) has demonstrated an extravisual input to this nucleus during rapidsleep. Monophasic waves eye-movement
%gest
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DISCUSSION
appeared in the lateral geniculate nucleus duri ng th e rapid eye movements of sleep, and these waves were apparently associated with a presynaptic inhibition at the lateral The activity of single cg;enicula te nucleus. neurons in the lateral geniculate nucleus was also altered during the monophasic waves (2). Since these monophasic wa ves and modifications of unit activity occur in total darkness, they are not related to visual input. The present experiments on striate cortex neurons differ in at least two ways from the experiments on the lateral qeniculate nucleus: the lateral qeniculate ieurons c were studied dl lring rapid-eye-movement sleep (a state in which presynaptic inhibition is also found in other areas-of nervous system (15)) rather than in the awake animal; the lateral geniculate neurons studied were in the cat rather than the monkev (and there are clear anatomical differences between the lateral geniculate nucleus and its projections in the cat and in the monkey (14, 20)). In the awake monkey, unit activity in the lateral geniculate nucleus did not show any alteration with rapid eye movements (3); the only neurons that responded in relation to eye movements were in the pregenicula te nucleus. These findings led Bizzi (3) to s that an eye movement geni culate numaY not act on the lateral cleus 0 f the awa ke m onkey as it does on that of the sleeping cat. Al though monophasic waves have been recorded n the la teral genicl .llate n ucleus of awake monke YS during eye movements (7), what these waves indicate remains to be determined. Neither the present study of single neuron activitv in striate cortex nor the work on single neuron activity in the lateral geniculate nucleus of the monkey (3) gives any indication of a corollary discharge in the primate visual pathway up to the striate cortex during the rapid eye movemen ts of wakefulness. Whether SUCll a corollary discharge reaches other parts of the vis1ial system or occurs under different experimental conditions remains to be se&. A corollarv discharge might impinge on higher levels o/f visual cortex, including other levels in the striate cortex and areas 18 and 19, on neurons with receptive fields in the fovea1
COMPARISON
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or in the peripheral area of the retina, or on other divisions of the visual system such as the superior colliculus. A corollary discharge might also be associated with other types of eye movements such as the slow tracking movements that differ from rapid eye movements in several perceptual and physiological characteristics (9, 13, 16, 17). SUMMARY
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sponses similar to the responses they had given with a rapid eye movement. Whether the rapid movement was made by eye or stimulus, the neuronal response appeared to be the same. As the speed of stimulus movement was increased in steps from 10 to 9OO”/sec, the response of the units gradually changed from that seen with a slow stimulus movement to that seen with a rapid stimulus or eye movement. The differences in neuronal response to slow and rapid stimulus movement were therefore related to the change in speed of movement. If an eye movement were accompanied by a corollary discharge from the oculomotor system to the neurons of striate cortex, one would expect the striate cortex neurons to show a difference between responses following rapid eye movement and responses following rapid stimulus movement. Since no such difference was detected, there was no evidence for a corollary discharge to the levels of the striate cortex studied or to more peripheral parts of the retinocortical branch of the visual pathway such as the lateral genicula te nucleus.
REFERENCES 1. BIZZI, E. Changes in the orthodromic and antidromic response of optic tract during the eye movements of sleep. J. Neurophysiol. 29: 861-870, 1966. 2. BIZZI, E. Discharge patterns of single geniculate neurons during the rapid eye movements of sleep. J. Neurophysiol. 29: 1087-1095, 1966. 3. BIZZI, E. Vestibular effects on visual input. In: Handbook of Sensory Physiology, cditcd by H. H. Kornhuber. Berlin: Springer. In press. 4. EVARTS, E. V. Methods for recording activity of individual neurons in moving animals. In: Methods in Medical Research, edited by R. F. Rushmcr. Chicago: Year Book, 1966, vol. 11, p. 241-250. 5. EVARTS, E. V. Relation of pyramidal tract activity to force exerted during voluntary movement. J. Neurophysiol. 31: 14-27, 1968. 6. EVARTS, E. V. A technique for recording activity of subcortical neurons in moving animals. Electroencephalog. Clin. Neurophysiol. 24: 8386, 1968. 7. FELDMAN, M. AND COHEN, B. Electrical activity in the lateral geniculate body of the alert monkey associated with eye movement. J. Neurophysiol. 31: 455-466, 1968. 8. FUCHS, A. F. Saccadic and smooth pursuit eye
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movements in the monkey. J. Physiol., London 191: 609-631, 1967. GWCORY, R. L. Eye movements and the stability of the visual world. Nature 182: 12141216, 1958. HELMHOLTZ, H. VON. Treatise on Physiological Optics (vol. III), edited and transl. from 3rd edition by J. P. C. Southall. Menasha, Wis.: Opt. Sot. Am., 1925. HOIST, E. VON. Relations between the central nervous system and the peripheral organs. Brit. J. Animal Beha-oiour 2: 89-94, 1954. JAMES, W. The Principles of Psychology. New York: Henry Holt, 1890; reprinted New York: Dover, 1950. KAWAMURA, H. AND MARCHINAVA, P. L. Excitability changes along visual pathways during eye tracking movements. Arch. Ital. Biol. 106: 141-156, 1968. POLYAK, S. P. The Vertebrate Visual System. Chicago: Univ. Chicago Press, 1957. POMPEIANO, 0. Sensory inhibition during motor activity in sleep. In: SymfIosium on Neurophysiological Basis of Normal and Abnormal Motor Activities, edited by M. D. Yahr and D. P. Purpura. Hewlett, N.Y.: Raven Press, 1967, p. * 323-373.
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Experiments were designed to determine whether any corollary discharge associated with rapid eye movements could be detected at the striate cortex of the monkey. The response of a single neuron when a rapid eye movement was made across an effective stationary stimulus was compared with its response when an equally rapid stimulus movement (9OO”/sec) was made in front of the stationary eye. All neurons studied gave an excitatory response to a stationary stimulus. With a rapid eye movement across a stationary stimulus, some neurons gave an excitatory response, some gave no response, and some gave a suppression response. With a rapid stimulus movement in front of a stationary eye, neurons of all three types gave re-
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R. H. C. The relationship between saccadic and smooth tracking eye movements. J. Physiol., London 159: 326-338, 1961. ROBINSON, D. A. Eye movement control in primates. Science 161: 12191224, 1968. SPERRY, R. W. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Camp. Physiol. Psychol. 43: 482-489, 1950. TEUBER, H.-L. Perception. In: Handbook of Physiology. Neurophysiology. Washington, D.C.: Am. Physiol. Sot., 1960, sect. 1, vol. III, &apt. 65, p. 1595-1668. WILSON, M. E. AND CRAGC, B. G. Projections RASHBASS,
WURTZ from the lateral geniculate nucleus in the cat and monkey. J. Anat. 101: 677-692, 1967. 21. WURTZ, R. H. Visual cortex neurons: response to stimuli during rapid eye movements. Science 162: 1148-l 150, 1968. 22. WURTZ, R. H. Effects of eye movement and stimulus movement on striate cortex neurons in awake monkeys. Federation Proc. 28: 332, 1969. 23. WURTZ, R. H. Visual receptive fields of striate cortex neurons in awake monkeys. J. Neurophysiol. 32: 727-742, 1969. 24. WURTZ, R. H. Response of striate cortex neurons to stimuli during rapid eye movements of the monkey. J. Newophysiol. 32: 975-986, 1969.
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