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Evidence for efference copy for eye movements in fish
Comp. Biochem. Physiol., 1969, Vol. 30, pp. 931 to 939. Pergamon Press. Printed in Great Britain
EVIDENCE FOR EFFERENCE COPY FOR EYE M O V E M E N T S IN FISH* J. R. J O H N S T O N E
and R. F. M A R K
Department of Physiology, Monash University, Clayton, Victoria 3168, Australia (Received 27 ffanuary 1969)
Abstract--1. Common goldfish at rest move their eyes back and forth in the horizontal plane in a series of regular saccadic steps, three or four forward and the same number back. 2. Microelectrode recordings from the tectal commissure show two kinds of response in time with eye movement, one of which is a sensory evoked response, while the other appears to be neither sensory nor motor. 3. This paper discusses the latter response in relation to the general problem of distinguishing movement in the visual environment from apparent movement generated by displacement of the eye. INTRODUCTION MANY authors have recognized that central nervous mechanisms for the control of muscular contraction must take account of the change in sensory inflow that accompanies movement (Paillard, 1960). This need is nowhere more apparent than in the scanning movements of vertebrate eyes because displacement of the retinal image has a different significance depending on whether it is caused by moving objects in the visual field or by movement of the eye in an otherwise stable environment. T h e perceptual stability that persists in the face of a constantly changing retinal image led in the nineteenth century to two different theories. Sherrington (1918) suggested that changing eye position could be signalled by peripheral receptors; yon Helmholtz (1867) favoured a purely internal representation of eye position corresponding to the effort of will needed to change the direction of gaze. More recent work in man supports yon Helmholtz. Brindley & Merton (1960) have shown that he was right to assume that judgement of eye position did not depend on peripheral receptors but on some internal monitoring of motor commands. Sperry (1950) and yon Holst & Mittelstaedt (1950), studying the orientation of various animals including fish, found it necessary to postulate that active movement was accompanied by neural messages that were destined to interact with the resulting sensory inflow and prevent any behavioural response to self-induced stimulation. These messages were called "corollary discharge" by Sperry and "efference copy" by yon Holst (1954). It has since been argued (Teuber, 1966) * This work was supported by a grant from the Australian Research Grants Committee. We thank the Fisheries and Wildlife Department of the Victorian State Government for help with the collection of fish. 931
932
J. R. JOHNSTONE AND R. F. MARK
t h a t a s i m i l a r m e c h a n i s m m a y c o n t r i b u t e to p e r c e p t u a l s t a b i l i t y d u r i n g e y e m o v e m e n t s in m a n . D i r e c t p h y s i o l o g i c a l e v i d e n c e is l a c k i n g a n d in t h i s p a p e r w e describe neurophysiological data consistent with the idea that some commissural n e u r o n e s o f t h e fish o p t i c l o b e d o c a r r y c o r o l l a r y d i s c h a r g e for eye m o v e m e n t . A p r e l i m i n a r y a c c o u n t o f this w o r k has a p p e a r e d e l s e w h e r e ( J o h n s t o n e & M a r k , 1968). MATERIALS AND METHODS Goldfish or carp (Carassius auratus or Carassius carassius) were anaesthetized with MS-222 (Sandoz) and a small hole was made in the skull to expose the brain. In some cases the spinal cord was cut through just behind the medulla. T h e fish was wrapped in sponge, supported in a U-shaped block and placed in a Perspex tank which was filled with water to just above eye level. Usually the fish was perfused with water through a cannula in the mouth. Recovery from the anaesthetic required about 10 min. When necessary Flaxedil (10 -4 M) was given intramuscularly to cause paralysis. Experiments were done on thirtynine fish. Glass-coated tungsten microelectrodes were made according to the method of Baldwin et al. (1965) and connected to a high-input impedance preamplifier, oscilloscope and chart recorder. Electrical activity from the tectal commissure could be averaged with a half-wave rectifier and low-pass filter (time constant 1-10 msec). Eye movements were measured by an optical method. A photoresistor (Clairex 705HL or Philips B8731 03) in the back focal plane of a binocular microscope varied in resistance as the image of the fish pupil moved across it, and a corresponding change in voltage was recorded on the chart recorder. T h e change in resistance with eye movement was not linear, but when necessary the recording could be calibrated by simultaneously observing movement of the eye across a graticule placed in the second eye-piece of the binocular microscope. The time at which eye movements started could be measured to + 2 msec. When required an Elliott-Tandberg F M tape recorder was used to record eye movements and single unit discharge. RESULTS
Eye Movements U n d e r t h e c o n d i t i o n s o f t h i s e x p e r i m e n t t h e r e s t r a i n e d fish m a d e a series o f r e g u l a r e y e m o v e m e n t s , b a c k a n d f o r t h in t h e h o r i z o n t a l p l a c e (Fig. 1) i n t e r r u p t e d Eye movements Forwords
F29
_
ioo~ Backwards
0
~
i
•
~'~
I I 0 sec
FIc. 1. Sample record of the continual back-and-forth movements of the left eye of a goldfish, restrained but unanaesthetized. T h e right eye moves in the same way at the same time but in the opposite direction. The number on the top right refers to the number of the experiment in this and subsequent figures. This and all subsequent chart recordings are curvilinear.
EVIDENCE FOR EFFERENCE COPY FOR EYE MOVEMENTS IN FISH
933
occasionally by fixation. Movements of the left and right eyes occurred synchronously to within + 10 msec (Figs. 5 and 6). The two eyes always moved in opposite directions, one forwards as the other moved backwards.
Microelectrode Recordings (a) Optic lobes Recordings could be made in the tectum presumably from optic nerve terminals as described by other authors (e.g. Jacobsen & Gaze, 1964). Bursts of activity occurred just after eye movements, the latency being about 30 msec. This activity was not studied further.
(b) Tectal commissure An electrode in the tectal commissure recorded two kinds of activity synchronous with eye movements. The first was that described previously by Mark & Davidson (1966), consisting of units that discharged fairly regularly and were inhibited by light. The discharge pattern of these units often changed when the eye moved but no detailed results will be presented here. The second type of activity, the description of which is the main purpose of this paper, could be recorded from the same regions as the first but had quite different properties. It consisted of bursts of high-frequency spikes, clearly audible on the loudspeaker as the summed activity of several units and which were obviously in time with the flick movements of the eyes. In order to facilitate analysis of this activity the signals from the microeleetrode were fed into a half-wave rectifier and low-pass filter and the resulting signal written out on a chart recorder. Figure 2 compares a filmed sample of the raw activity and the same record after being processed in this way. The relationship of these bursts to eye movement is shown in Fig. 3. Each quick movement of the eye is associated with a burst of impulses in the tectal commissure. The commissure discharge was usually largest at the beginning of each set of Commissure activity 5°F-vI
.~,,~,,~,!~=.,~, ~ ~ ; ~ ;
~_~~,.
F33 ~
..............................
I
"~ . . . . . . . .
~'= .......................
! I ~c
FIG. 2. P e r i o d i c activity r e c o r d e d b y a m i c r o e l e c t r o d e in t h e tectal c o m m i s s u r e o f a goldfish. T h e top tracing s h o w s t h e filmed r e c o r d f r o m the oscilloscope a n d t h e b o t t o m tracing is t h e rectified signal as seen o n a c h a r t recorder.
J. R. JOHNSTONEAND R. F. MAl~K
934
forwards or backwards movements. The origin of this periodic activky was examined in the following experiments. 1. Latency measurements. The time of occurrence of eye movements and the beginning of the rise of rectified signal were measured and the interval between them calculated. The error in measurement of the commissure discharge was + 5 msec, that of eye movement + 2 msec. Within these limits both signals occurred simultaneously. F29
E,e moveme Forwards ~/
,s
: ---'/
L
Backwards
Commissure
/
j
I
/
I
I sec
FIG. 3. Records of movement of the left eye of a restrained goldfish compared with tracings of the rectified activity from a microelectrode in the tectal commissure. Note that each quick change of eye position is accompanied by a burst of activity from the commissure.
2. Response to light. Theperiodicdischargeofcommissuralfibreswasunaffected by light levels in the experimental room and would continue uninterrupted in the same rhythm in complete darkness. 3. Effect ofparalysing eye muscles. The same regular bursts of activity continued when eye movement was stopped by neuromuscular blockade. In Fig. 4 a record of commissure activity is shown before and after injection of Flaxedil to abolish eye movement. The apparent increase in amplitude of the rectified signal after paralysis is probably not significant because the electrode was inadvertently moved during injection of the drug. 4. Brain lesions. Eye movements continued during and after complete section of the tectal commissure and the normal synchrony of movements of the two eyes was not changed (Fig. 5). Eye movements also continued essentially unchanged after removal of both optic lobes. Figure 6 shows simultaneous records of the movements of both eyes of one fish before and after total removal of the tectum. 5. Unit recordings. It is very difficult to make records of single fibres showing this periodic activity. None have yet been encountered in the tectum and so far we have managed to record from only four units in the commissure. Once isolated, however, recordings could be made for periods of up to 15 min. All the fibres we
EVIDENCE FOR EFFERENCECOPY FOR EYE MOVEMENTS IN FISH Before floxedil
935
FI6
Eye movements
Forwards
Backwards
Commissure
After f Ioxedil Eye movements
Commissure
I sec
FIG. 4. C o m m i s s u r e activity and m o v e m e n t of the left eye of a restrained u n anaesthetized goldfish before and after the administration of Flaxedil (10 -~ M). N o t e that periodic bursts in the commissure are still very p r o m i n e n t even w h e n eye m o v e m e n t is p r e v e n t e d b y paralysis of the ocular muscles.
FI9 After commissurotomy
Before commissurotomy
f
Left
Right
~,~
eye, I
I
I sec FIG. 5. Simultaneous records of m o v e m e n t of the left and right eyes of a goldfish before and after cutting the tectal commissure. T h e synchrony of eye m o v e m e n t s was not changed.
936
J. R. JOHNSTONE AND R. F. MARK
have encountered discharged for movements of the eye in one direction only and were silent for all movements in the opposite direction (Fig. 7). They discharged for every movement in the preferred direction although the number of spikes per burst was variable. Discharge always began just before the eye started to move. FI9 Before removing latium
After removing rectum Forwards
eye
ckwards
Right eye
¢_._J t0 sec
FIG. 6. Simultaneous recordings of m o v e m e n t of both eyes of a goldfish before and after complete removal of the tecturn. After the lesion the m o v e m e n t s are still regular, periodic and coordinated. T h e apparent increase in amplitude is due to a change in recording conditions.
There was no tonic firing between movements and none of these units were light sensitive, in contrast to the other class of commissural units previously described as slowly adapting "off" fibres (Mark & Davidson, 1966). We will present a full account of unit recordings from the tectal commissure in a later paper. F3"7 Commissure
,-~',,",w
~
~-v.Tr,-vlr,r-p,re-iTv~
"r'T~""~'
e- -
- ~ , ....... ~
~
~
Eye movements
I Forwards
~ ,.-r,q,~..r~,.~-~.,m-.,1,~-~,-.r-
,.
#"-'-'-------_--_.~
I I O0 msec
Backwards
FI6. 7. Excerpts from the filmed record of a unit from the commissure that responded only with forward m o v e m e n t s of the left eye. T h e burst discharge begins 16 msec before the eye begins to m o v e and stops when the eye has reached the n e w position. T h e r e was no response for m o v e m e n t in the opposite direction, Eye m o v e m e n t s were recorded with capacitative coupling in this experiment but were the same step-like m o v e m e n t s seen in other animals. Spikes retouched.
EVIDENCE FOR EFFERENCE COPY FOR EYE MOVEMENTS I N F I S H
937
DISCUSSION The movements studied here do not require tectal motoneurones or coordinating interneurones because they continue after removal of the tectum. The discharges are not the result of sensory impulses, either somatic afferent or from the retina, because the activity goes on when the eye is totally paralysed. Why then is a burst of activity recorded in the commissure with every eye movement ? We suggest that it is due to impulses in interneurones that are concerned with cancelling the behavioural effects of the burst of afferent activity generated by each quick eye movement. Should this prove to be so, these cells may form part of the system thought to account for perceptual stability during movement of the eye. Several arrangements for cancelling self-generated stimulation of sense organs by efference copy have been described in invertebrates, for example the peripheral inhibition of stretch receptor discharge from the crayfish abdomen during active tail-flicks (Eckert, 1961). In higher animals, an account of neurones that might be related to this function has been made by Bizzi (1967, 1968a, b) who recorded from single cortical cells of the frontal eye fields of unanaesthetized monkeys. Some neurones discharge during saccadic movement in a fixed direction and others are active for particular directions of gaze, yet they often do not begin to discharge until after the eye has taken up the new position. He suggests that these cells might be signalling a corollary discharge from eye movement systems to make information on eye position available to sensory mechanisms. However, the evidence that these neurones are not motor or sensory instead is by no means clear. Better evidence for efference copy activity has been found by Bizzi (1966a, b) in the lateral geniculate where he recorded waves that corresponded in time with eye movements. The geniculate waves are probably caused by presynaptic inhibition of ganglion cell terminals and this could be a result of efference copy arriving in the geniculate to block or reduce the transmission of sensory information. There remains the possibility that the fibres we have tentatively identified as carrying efference copy in the fish optic lobes are from simple co-ordinating neurones. At the neurophysiological level, however, the distinction may not be clear. For example, eye movements in the fish should, by displacement of the retinal image, tend to produce an opto-kinetic response in the reverse direction. Presumably this does not happen because of the blanking effect of efference copy. But it often happens that eye movements are followed by head and body movements for further scanning of the visual field and such movements would require coordinating interneurones. Both functions, blanking the response to visual input and co-ordinating subsequent orienting movements, may be served by the same neurone system or even by the same nerve cells. Direct interaction between motor commands and sensory input is only one physiological mechanism available for distinguishing between self and object movement. Palka (1968, 1969) has described interneurones in the cervical connectives of crickets that make the distinction by responding to movements within
938
J.R. JOHNSTONE AND R. F. MARK
the visual field but not to coherent displacements of the whole field. T h i s property apparently depends on the arrangement of interconnexions of neurones in the neuropil behind the c o m p o u n d eye and not on any interaction with m o t o r systems or other afferent channels. Some interneurones of crayfish, on the other hand, integrate information f r o m the eye and from the statocyst and this results in a directional constancy for visual input maintained, in the face of changes of body posture (Wiersma & Yamaguchi, 1967). All three mechanisms, motor-sensory, intra-sensory and inter-sensory integration, m a y contribute in varying degrees to the distinction between stimuli arising outside an animal and stimuli generated by active m o v e m e n t . We interpret the results of the experiments described in this p a p e r as p r e s u m p tive evidence that efference copy for eye m o v e m e n t s arrives in the optic lobe. Further experiments on the interaction between this activity and the self-induced sensory input to the optic lobe are needed in order to decide whether the burst of impulses that we record has an action corresponding to the efference copy postulated b y other workers. SUMMARY C o m m o n goldfish at rest m o v e their eyes back and forth in the horizontal plane in a series of regular saccadic steps, three or four forward and the same n u m b e r back. Microelectrode recordings from the tectal commissure show two kinds of response in time with eye movement, one of which is a sensory-evoked response, while the other appears to be neither sensory nor motor. T h i s p a p e r discusses the latter response in relation to the general p r o b l e m of distinguishing m o v e m e n t in the visual environment f r o m apparent m o v e m e n t generated by displacement of the eye. REFERENCES BALDWIN H. A., FRENK S. & LETVIN J. Y. (1965) Glass-coated tungsten microelectrodes. Science 148, 1462-1464. BIZZI E. (1966a) Changes in the orthodromic and antidromic response of optic tract during the eye movements of sleep. 07. Neurophysiol. 29, 861-870. Btzzl E. (1966b) Discharge patterns of single geniculate neurones during the rapid eye movements of sleep. 07. Neurophysiol. 29, 1087-1095. BIzzI E. (1967) Discharge of frontal eye field neurones during eye movements in unanaesthetized monkeys. Science 157, 1588-1590. Bizzl E. (1968a) Discharge of frontal eye field neurones during saccadic and smooth pursuit eye movement in monkeys. Proc. Int. Union Physiol. Sci. Volume VII, Abstract No. 138, p. 46. BlzZI E. (1968b) Discharge of frontal eye field neurones during saccadic and following eye movements in unanaesthetized monkeys. Exp. Brain Res. 6, 69-80. BRINDLEYG. S. & MERTONP. A. (1960) The absence of position sense in the human eye. 07. Physiol. (Lond.) 153, 127-130. ECKERTR. O. (1961) Reflex relationships of the abdominal stretch receptors of the crayfish-II. Stretch receptor involvement during the swimming reflex. 07. cell. comp. Physiol. 57, 163-174.
EVIDENCE FOR EFFERENCE COPY F O R EYE MOVEMENTS I N F I S H
939
VON HELMHOLTZ H. (1867) Handbuch der physiologischen Optik, 1st edn. Section 29, pp. 599-601. Voss, Leipzig. English translation by SOUTHALLJ. P. C. (1925) Helmholtz's Treatise on Physiological Optics, Vol. 3. Section 29, pp. 243-245. Optical Society of America, Menasha, Wisconsin. VON HOLST E. (1954) Relations between the central nervous system and the peripheral organs. Br.J. Anim. Behav. 2, 89-94. YON HOLST E. & MITTELSTAEDTH. (1950) Das Reafferenzprinzip. Naturwissenschaften 37, 46 A, A.76. JACOBSEN M. & GAZE R. M. (1964) Types of visual response from single units in the optic rectum and optic nerve of the goldfish. Quart.J. exp. Physiol. 49, 199-209. JOHNSTONE J. R. & R. F. MARK (1968) Do efference copy neurons exist ? Aust.J. exp. Biol. med. Sci. 46, 10. MARK R. F. & DAVIDSON T. M. (1966) Unit responses from commissural fibers of optic lobes offish. Science 152, 797-799. PAmLARD J. (1960) The patterning of skilled movement. In Handbook of Physiology (Edited by FIELD J., MAGOUN H. W. & HALL V. E.), Section I, Volume III, pp. 1679-1708. American Phsyiological Society, Washington. PALKA J. (1968) Discrimination between eye movement and object movement by insect neurones. Proc. Int. Union Physiol. Sci. Volume V I I , Abstract No. 1003, p. 335. PALKA J. (1969) Complex visual interneurones in insects--I. Discrimination between eye and object movement by cricket neurones. J. exp. Biol. (In press.) SHERRINGTON C. S. (1918) Observations on the sensual role of the proprioceptive nerve supply of the extrinsic ocular muscles. Brain 41,332-343. SPERRY R. W. (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482-489. TEUEER H.-L. (1966) The frontal lobes and their function: further observations on rodents, carnivores, subhuman primates, and man. Int.J. Neurol. 5, 282-300. WIERSMA C. A. G. & YAMAGUCHIT. (1967) Integration of visual stimuli by the crayfish central nervous system. J. exp. Biol. 47, 409-431.
Key Word Index--Goldfish; eye movements; efference copy; optic lobe; control of muscles.
eye
EVIDENCE FOR EFFERENCE COPY FOR EYE M O V E M E N T S IN FISH* J. R. J O H N S T O N E
and R. F. M A R K
Department of Physiology, Monash University, Clayton, Victoria 3168, Australia (Received 27 ffanuary 1969)
Abstract--1. Common goldfish at rest move their eyes back and forth in the horizontal plane in a series of regular saccadic steps, three or four forward and the same number back. 2. Microelectrode recordings from the tectal commissure show two kinds of response in time with eye movement, one of which is a sensory evoked response, while the other appears to be neither sensory nor motor. 3. This paper discusses the latter response in relation to the general problem of distinguishing movement in the visual environment from apparent movement generated by displacement of the eye. INTRODUCTION MANY authors have recognized that central nervous mechanisms for the control of muscular contraction must take account of the change in sensory inflow that accompanies movement (Paillard, 1960). This need is nowhere more apparent than in the scanning movements of vertebrate eyes because displacement of the retinal image has a different significance depending on whether it is caused by moving objects in the visual field or by movement of the eye in an otherwise stable environment. T h e perceptual stability that persists in the face of a constantly changing retinal image led in the nineteenth century to two different theories. Sherrington (1918) suggested that changing eye position could be signalled by peripheral receptors; yon Helmholtz (1867) favoured a purely internal representation of eye position corresponding to the effort of will needed to change the direction of gaze. More recent work in man supports yon Helmholtz. Brindley & Merton (1960) have shown that he was right to assume that judgement of eye position did not depend on peripheral receptors but on some internal monitoring of motor commands. Sperry (1950) and yon Holst & Mittelstaedt (1950), studying the orientation of various animals including fish, found it necessary to postulate that active movement was accompanied by neural messages that were destined to interact with the resulting sensory inflow and prevent any behavioural response to self-induced stimulation. These messages were called "corollary discharge" by Sperry and "efference copy" by yon Holst (1954). It has since been argued (Teuber, 1966) * This work was supported by a grant from the Australian Research Grants Committee. We thank the Fisheries and Wildlife Department of the Victorian State Government for help with the collection of fish. 931
932
J. R. JOHNSTONE AND R. F. MARK
t h a t a s i m i l a r m e c h a n i s m m a y c o n t r i b u t e to p e r c e p t u a l s t a b i l i t y d u r i n g e y e m o v e m e n t s in m a n . D i r e c t p h y s i o l o g i c a l e v i d e n c e is l a c k i n g a n d in t h i s p a p e r w e describe neurophysiological data consistent with the idea that some commissural n e u r o n e s o f t h e fish o p t i c l o b e d o c a r r y c o r o l l a r y d i s c h a r g e for eye m o v e m e n t . A p r e l i m i n a r y a c c o u n t o f this w o r k has a p p e a r e d e l s e w h e r e ( J o h n s t o n e & M a r k , 1968). MATERIALS AND METHODS Goldfish or carp (Carassius auratus or Carassius carassius) were anaesthetized with MS-222 (Sandoz) and a small hole was made in the skull to expose the brain. In some cases the spinal cord was cut through just behind the medulla. T h e fish was wrapped in sponge, supported in a U-shaped block and placed in a Perspex tank which was filled with water to just above eye level. Usually the fish was perfused with water through a cannula in the mouth. Recovery from the anaesthetic required about 10 min. When necessary Flaxedil (10 -4 M) was given intramuscularly to cause paralysis. Experiments were done on thirtynine fish. Glass-coated tungsten microelectrodes were made according to the method of Baldwin et al. (1965) and connected to a high-input impedance preamplifier, oscilloscope and chart recorder. Electrical activity from the tectal commissure could be averaged with a half-wave rectifier and low-pass filter (time constant 1-10 msec). Eye movements were measured by an optical method. A photoresistor (Clairex 705HL or Philips B8731 03) in the back focal plane of a binocular microscope varied in resistance as the image of the fish pupil moved across it, and a corresponding change in voltage was recorded on the chart recorder. T h e change in resistance with eye movement was not linear, but when necessary the recording could be calibrated by simultaneously observing movement of the eye across a graticule placed in the second eye-piece of the binocular microscope. The time at which eye movements started could be measured to + 2 msec. When required an Elliott-Tandberg F M tape recorder was used to record eye movements and single unit discharge. RESULTS
Eye Movements U n d e r t h e c o n d i t i o n s o f t h i s e x p e r i m e n t t h e r e s t r a i n e d fish m a d e a series o f r e g u l a r e y e m o v e m e n t s , b a c k a n d f o r t h in t h e h o r i z o n t a l p l a c e (Fig. 1) i n t e r r u p t e d Eye movements Forwords
F29
_
ioo~ Backwards
0
~
i
•
~'~
I I 0 sec
FIc. 1. Sample record of the continual back-and-forth movements of the left eye of a goldfish, restrained but unanaesthetized. T h e right eye moves in the same way at the same time but in the opposite direction. The number on the top right refers to the number of the experiment in this and subsequent figures. This and all subsequent chart recordings are curvilinear.
EVIDENCE FOR EFFERENCE COPY FOR EYE MOVEMENTS IN FISH
933
occasionally by fixation. Movements of the left and right eyes occurred synchronously to within + 10 msec (Figs. 5 and 6). The two eyes always moved in opposite directions, one forwards as the other moved backwards.
Microelectrode Recordings (a) Optic lobes Recordings could be made in the tectum presumably from optic nerve terminals as described by other authors (e.g. Jacobsen & Gaze, 1964). Bursts of activity occurred just after eye movements, the latency being about 30 msec. This activity was not studied further.
(b) Tectal commissure An electrode in the tectal commissure recorded two kinds of activity synchronous with eye movements. The first was that described previously by Mark & Davidson (1966), consisting of units that discharged fairly regularly and were inhibited by light. The discharge pattern of these units often changed when the eye moved but no detailed results will be presented here. The second type of activity, the description of which is the main purpose of this paper, could be recorded from the same regions as the first but had quite different properties. It consisted of bursts of high-frequency spikes, clearly audible on the loudspeaker as the summed activity of several units and which were obviously in time with the flick movements of the eyes. In order to facilitate analysis of this activity the signals from the microeleetrode were fed into a half-wave rectifier and low-pass filter and the resulting signal written out on a chart recorder. Figure 2 compares a filmed sample of the raw activity and the same record after being processed in this way. The relationship of these bursts to eye movement is shown in Fig. 3. Each quick movement of the eye is associated with a burst of impulses in the tectal commissure. The commissure discharge was usually largest at the beginning of each set of Commissure activity 5°F-vI
.~,,~,,~,!~=.,~, ~ ~ ; ~ ;
~_~~,.
F33 ~
..............................
I
"~ . . . . . . . .
~'= .......................
! I ~c
FIG. 2. P e r i o d i c activity r e c o r d e d b y a m i c r o e l e c t r o d e in t h e tectal c o m m i s s u r e o f a goldfish. T h e top tracing s h o w s t h e filmed r e c o r d f r o m the oscilloscope a n d t h e b o t t o m tracing is t h e rectified signal as seen o n a c h a r t recorder.
J. R. JOHNSTONEAND R. F. MAl~K
934
forwards or backwards movements. The origin of this periodic activky was examined in the following experiments. 1. Latency measurements. The time of occurrence of eye movements and the beginning of the rise of rectified signal were measured and the interval between them calculated. The error in measurement of the commissure discharge was + 5 msec, that of eye movement + 2 msec. Within these limits both signals occurred simultaneously. F29
E,e moveme Forwards ~/
,s
: ---'/
L
Backwards
Commissure
/
j
I
/
I
I sec
FIG. 3. Records of movement of the left eye of a restrained goldfish compared with tracings of the rectified activity from a microelectrode in the tectal commissure. Note that each quick change of eye position is accompanied by a burst of activity from the commissure.
2. Response to light. Theperiodicdischargeofcommissuralfibreswasunaffected by light levels in the experimental room and would continue uninterrupted in the same rhythm in complete darkness. 3. Effect ofparalysing eye muscles. The same regular bursts of activity continued when eye movement was stopped by neuromuscular blockade. In Fig. 4 a record of commissure activity is shown before and after injection of Flaxedil to abolish eye movement. The apparent increase in amplitude of the rectified signal after paralysis is probably not significant because the electrode was inadvertently moved during injection of the drug. 4. Brain lesions. Eye movements continued during and after complete section of the tectal commissure and the normal synchrony of movements of the two eyes was not changed (Fig. 5). Eye movements also continued essentially unchanged after removal of both optic lobes. Figure 6 shows simultaneous records of the movements of both eyes of one fish before and after total removal of the tectum. 5. Unit recordings. It is very difficult to make records of single fibres showing this periodic activity. None have yet been encountered in the tectum and so far we have managed to record from only four units in the commissure. Once isolated, however, recordings could be made for periods of up to 15 min. All the fibres we
EVIDENCE FOR EFFERENCECOPY FOR EYE MOVEMENTS IN FISH Before floxedil
935
FI6
Eye movements
Forwards
Backwards
Commissure
After f Ioxedil Eye movements
Commissure
I sec
FIG. 4. C o m m i s s u r e activity and m o v e m e n t of the left eye of a restrained u n anaesthetized goldfish before and after the administration of Flaxedil (10 -~ M). N o t e that periodic bursts in the commissure are still very p r o m i n e n t even w h e n eye m o v e m e n t is p r e v e n t e d b y paralysis of the ocular muscles.
FI9 After commissurotomy
Before commissurotomy
f
Left
Right
~,~
eye, I
I
I sec FIG. 5. Simultaneous records of m o v e m e n t of the left and right eyes of a goldfish before and after cutting the tectal commissure. T h e synchrony of eye m o v e m e n t s was not changed.
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J. R. JOHNSTONE AND R. F. MARK
have encountered discharged for movements of the eye in one direction only and were silent for all movements in the opposite direction (Fig. 7). They discharged for every movement in the preferred direction although the number of spikes per burst was variable. Discharge always began just before the eye started to move. FI9 Before removing latium
After removing rectum Forwards
eye
ckwards
Right eye
¢_._J t0 sec
FIG. 6. Simultaneous recordings of m o v e m e n t of both eyes of a goldfish before and after complete removal of the tecturn. After the lesion the m o v e m e n t s are still regular, periodic and coordinated. T h e apparent increase in amplitude is due to a change in recording conditions.
There was no tonic firing between movements and none of these units were light sensitive, in contrast to the other class of commissural units previously described as slowly adapting "off" fibres (Mark & Davidson, 1966). We will present a full account of unit recordings from the tectal commissure in a later paper. F3"7 Commissure
,-~',,",w
~
~-v.Tr,-vlr,r-p,re-iTv~
"r'T~""~'
e- -
- ~ , ....... ~
~
~
Eye movements
I Forwards
~ ,.-r,q,~..r~,.~-~.,m-.,1,~-~,-.r-
,.
#"-'-'-------_--_.~
I I O0 msec
Backwards
FI6. 7. Excerpts from the filmed record of a unit from the commissure that responded only with forward m o v e m e n t s of the left eye. T h e burst discharge begins 16 msec before the eye begins to m o v e and stops when the eye has reached the n e w position. T h e r e was no response for m o v e m e n t in the opposite direction, Eye m o v e m e n t s were recorded with capacitative coupling in this experiment but were the same step-like m o v e m e n t s seen in other animals. Spikes retouched.
EVIDENCE FOR EFFERENCE COPY FOR EYE MOVEMENTS I N F I S H
937
DISCUSSION The movements studied here do not require tectal motoneurones or coordinating interneurones because they continue after removal of the tectum. The discharges are not the result of sensory impulses, either somatic afferent or from the retina, because the activity goes on when the eye is totally paralysed. Why then is a burst of activity recorded in the commissure with every eye movement ? We suggest that it is due to impulses in interneurones that are concerned with cancelling the behavioural effects of the burst of afferent activity generated by each quick eye movement. Should this prove to be so, these cells may form part of the system thought to account for perceptual stability during movement of the eye. Several arrangements for cancelling self-generated stimulation of sense organs by efference copy have been described in invertebrates, for example the peripheral inhibition of stretch receptor discharge from the crayfish abdomen during active tail-flicks (Eckert, 1961). In higher animals, an account of neurones that might be related to this function has been made by Bizzi (1967, 1968a, b) who recorded from single cortical cells of the frontal eye fields of unanaesthetized monkeys. Some neurones discharge during saccadic movement in a fixed direction and others are active for particular directions of gaze, yet they often do not begin to discharge until after the eye has taken up the new position. He suggests that these cells might be signalling a corollary discharge from eye movement systems to make information on eye position available to sensory mechanisms. However, the evidence that these neurones are not motor or sensory instead is by no means clear. Better evidence for efference copy activity has been found by Bizzi (1966a, b) in the lateral geniculate where he recorded waves that corresponded in time with eye movements. The geniculate waves are probably caused by presynaptic inhibition of ganglion cell terminals and this could be a result of efference copy arriving in the geniculate to block or reduce the transmission of sensory information. There remains the possibility that the fibres we have tentatively identified as carrying efference copy in the fish optic lobes are from simple co-ordinating neurones. At the neurophysiological level, however, the distinction may not be clear. For example, eye movements in the fish should, by displacement of the retinal image, tend to produce an opto-kinetic response in the reverse direction. Presumably this does not happen because of the blanking effect of efference copy. But it often happens that eye movements are followed by head and body movements for further scanning of the visual field and such movements would require coordinating interneurones. Both functions, blanking the response to visual input and co-ordinating subsequent orienting movements, may be served by the same neurone system or even by the same nerve cells. Direct interaction between motor commands and sensory input is only one physiological mechanism available for distinguishing between self and object movement. Palka (1968, 1969) has described interneurones in the cervical connectives of crickets that make the distinction by responding to movements within
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J.R. JOHNSTONE AND R. F. MARK
the visual field but not to coherent displacements of the whole field. T h i s property apparently depends on the arrangement of interconnexions of neurones in the neuropil behind the c o m p o u n d eye and not on any interaction with m o t o r systems or other afferent channels. Some interneurones of crayfish, on the other hand, integrate information f r o m the eye and from the statocyst and this results in a directional constancy for visual input maintained, in the face of changes of body posture (Wiersma & Yamaguchi, 1967). All three mechanisms, motor-sensory, intra-sensory and inter-sensory integration, m a y contribute in varying degrees to the distinction between stimuli arising outside an animal and stimuli generated by active m o v e m e n t . We interpret the results of the experiments described in this p a p e r as p r e s u m p tive evidence that efference copy for eye m o v e m e n t s arrives in the optic lobe. Further experiments on the interaction between this activity and the self-induced sensory input to the optic lobe are needed in order to decide whether the burst of impulses that we record has an action corresponding to the efference copy postulated b y other workers. SUMMARY C o m m o n goldfish at rest m o v e their eyes back and forth in the horizontal plane in a series of regular saccadic steps, three or four forward and the same n u m b e r back. Microelectrode recordings from the tectal commissure show two kinds of response in time with eye movement, one of which is a sensory-evoked response, while the other appears to be neither sensory nor motor. T h i s p a p e r discusses the latter response in relation to the general p r o b l e m of distinguishing m o v e m e n t in the visual environment f r o m apparent m o v e m e n t generated by displacement of the eye. REFERENCES BALDWIN H. A., FRENK S. & LETVIN J. Y. (1965) Glass-coated tungsten microelectrodes. Science 148, 1462-1464. BIZZI E. (1966a) Changes in the orthodromic and antidromic response of optic tract during the eye movements of sleep. 07. Neurophysiol. 29, 861-870. Btzzl E. (1966b) Discharge patterns of single geniculate neurones during the rapid eye movements of sleep. 07. Neurophysiol. 29, 1087-1095. BIzzI E. (1967) Discharge of frontal eye field neurones during eye movements in unanaesthetized monkeys. Science 157, 1588-1590. Bizzl E. (1968a) Discharge of frontal eye field neurones during saccadic and smooth pursuit eye movement in monkeys. Proc. Int. Union Physiol. Sci. Volume VII, Abstract No. 138, p. 46. BlzZI E. (1968b) Discharge of frontal eye field neurones during saccadic and following eye movements in unanaesthetized monkeys. Exp. Brain Res. 6, 69-80. BRINDLEYG. S. & MERTONP. A. (1960) The absence of position sense in the human eye. 07. Physiol. (Lond.) 153, 127-130. ECKERTR. O. (1961) Reflex relationships of the abdominal stretch receptors of the crayfish-II. Stretch receptor involvement during the swimming reflex. 07. cell. comp. Physiol. 57, 163-174.
EVIDENCE FOR EFFERENCE COPY F O R EYE MOVEMENTS I N F I S H
939
VON HELMHOLTZ H. (1867) Handbuch der physiologischen Optik, 1st edn. Section 29, pp. 599-601. Voss, Leipzig. English translation by SOUTHALLJ. P. C. (1925) Helmholtz's Treatise on Physiological Optics, Vol. 3. Section 29, pp. 243-245. Optical Society of America, Menasha, Wisconsin. VON HOLST E. (1954) Relations between the central nervous system and the peripheral organs. Br.J. Anim. Behav. 2, 89-94. YON HOLST E. & MITTELSTAEDTH. (1950) Das Reafferenzprinzip. Naturwissenschaften 37, 46 A, A.76. JACOBSEN M. & GAZE R. M. (1964) Types of visual response from single units in the optic rectum and optic nerve of the goldfish. Quart.J. exp. Physiol. 49, 199-209. JOHNSTONE J. R. & R. F. MARK (1968) Do efference copy neurons exist ? Aust.J. exp. Biol. med. Sci. 46, 10. MARK R. F. & DAVIDSON T. M. (1966) Unit responses from commissural fibers of optic lobes offish. Science 152, 797-799. PAmLARD J. (1960) The patterning of skilled movement. In Handbook of Physiology (Edited by FIELD J., MAGOUN H. W. & HALL V. E.), Section I, Volume III, pp. 1679-1708. American Phsyiological Society, Washington. PALKA J. (1968) Discrimination between eye movement and object movement by insect neurones. Proc. Int. Union Physiol. Sci. Volume V I I , Abstract No. 1003, p. 335. PALKA J. (1969) Complex visual interneurones in insects--I. Discrimination between eye and object movement by cricket neurones. J. exp. Biol. (In press.) SHERRINGTON C. S. (1918) Observations on the sensual role of the proprioceptive nerve supply of the extrinsic ocular muscles. Brain 41,332-343. SPERRY R. W. (1950) Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43, 482-489. TEUEER H.-L. (1966) The frontal lobes and their function: further observations on rodents, carnivores, subhuman primates, and man. Int.J. Neurol. 5, 282-300. WIERSMA C. A. G. & YAMAGUCHIT. (1967) Integration of visual stimuli by the crayfish central nervous system. J. exp. Biol. 47, 409-431.
Key Word Index--Goldfish; eye movements; efference copy; optic lobe; control of muscles.
eye