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Differential responses of “simple” and “complex” cells of cat's striate cortex during saccadic eye movements
RESEARCH NOTE
DIFFERENTIAL RESPONSES OF “SIMPLE” AND “COMPLEX” CELLS OF CAT’S STRIATE CORTEX DURING SACCADIC EYE MOVEMENTS M. KWJRA’, Y. KOMATSUand K. TOY&MA Department of Physiology. Faculty of Medicine. University of Tokyo and Department of Physiology, Nagoya University, School of Medicine, Japan (Receired
The stability of visual images during eye movement has long been a subject of psychophysics (Jung, 1973). It has been hypothesized that a visual image is ‘perceived” as stable by subtraction of the motor signals for an eye movement from the reagerent retinal signals resulting from that eye movement (Hoist, 1950; Sperry, 1950). It has also been suggested that visual perception involves two independent processes, one perceiving an image and the other evaluating the coordinates of the perceived image in connection with the concurrent eye movement (MacKay, 1973). Both of these hypotheses incorporate motor signals into the process of image stabilization or coordinate evaluation. Efforts have been devoted to finding neuronal correlates to these hypotheses in the visual cortex of an alert animal, but the results have been rather controversial (Wurtz. 1969; Corazza et al., 1972; Duffy and Burchfiel, 1975; Noda er al., 1972: Kasamatsu, 1976). The main difficulties in these studies have been in keeping an animal fully alert and in motivating eye movements in darkness in a reproducible manner. In the present experiment these difficulties were removed by using eye movements evoked by reinforcement. Responses of striate cortex neurons of waterdeprived cats were studied during saccadic eye movements rewarded with water (Schlag et al., 1974) and also during eye fixation caused by withdrawal of the reward or by retrobulbar paralysis. The results suggest that the “simple” cells are related to the initial image perception, and the “complex’* cells to evaluation of the coordinates. Several days prior to the experiment, preparatory surgery was made on a cat under anaesthesia with Ketamine (40 mg/kg). The surgery involved (1) placement of a recording chamber over the striate cortex, (2) installation of holders on the skull for fixation of the cat’s head. (3) implantation of Ag-AgCl electrodes at the external canthi of both orbits for recording electrooculograms (EOGs) and (4) installation of injection needles for retrobulbar paralysis of both * Present address: Jichi Medical School Minamikawachi-Machi. T&higi 329-04. Japan.
30 Jttfy 1979)
eyes (Crewther et al., 1978). After recovery from the surgery, the cat was deprived of water and was trained to stay quietly with the head fixed on the stereotaxic frame and to make saccadic eye movements. During the training the EOGs were continuously monitored and a reward (a drop of water, 0.05 ml) was given for every qualified eye movement (horizontal saccades greater than 10” and faster than 4Odeg/sec). Within a few days. cats performed saccadie eye movements as frequently as 60 times/min, and could fulfill their daily demand of water (about 100 ml) in an hour. Cats were further trained to adapt to temporal withdrawal of the reward and to stay quietly on the stereotaxic frame with much less frequent saccadic eye movements (l-3 times/min). The trained cat was fixed on the frame. Patterned light stimuli (l-l.5 log units brighter than the background illumination of 3.5 cd/m’) such as light slits (0.5-2” wide and 2-40” long) or a checker pattern (periodicity, 3-5’) were projected on a translucent screen placed in front of the animal (distance. 57 cm). Impulse discharges were recorded extracellularly from striate neurons with a glass-coated stainless steel microelectrode while the cat was performing the trained task. The recording session, during which the task was partially reinforced (a reward for every few saccadie eye movements), was continued for a few hours. and was repeated once a day for about two weeks. Electrolytic marking was performed for the last ceil sampled in every track and the location of the celt in area 17 was confirmed histologically. One hundred and fifty-seven neurons were sampled from three cats under the above described conditions. When a checker pattern was displayed on the screen, almost all of these cells (149 of the 157 cells) exhibited a change of their spike activity in connection with saccadic eye movements. There was a distinct dichotomy in their response patterns; an excitation in one group of cells (n = 108) and an inhibition in the other (a = 41). The saccade-excited neurons discharged spontaneously at a relatively low frequency (less than 10 impulses/set) in the absence of saccadic eye movements. but they responded briskly to a saccadic move553
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Fig. I. Responses to saccadic eye movements. fA)-(D). responses of a saccade-excited cell during display of checker. (A). upper trace. a specimen record of impulse discharges and lower trace. electrooculogram (EOG) for horizontal eye movement. Upward deflection in EOG represents leftward movement. (ES).dot displays of impulse discharges. Horizontal dotted line demarcates responses for leftward (upper half) and rightward (lower haI0 movements. (C), an average response histogram for responses shown in (B). (DL traces of EOG. Time axis is common to (AHD). Zero in the axis represents the onset of the saccadic eye movements. (E)-(H), similar to (A)-(D), but in darkness. (I)-(L). similar to (A)-(D). but for a saccadeinhibited cell. Calibration for EOGs is common to (A). (D). (E). (H), (I) and (L), and voltage calibration of 0.5 mV to (A). (E) and (I).
ment (Fig. IA). As shown in the dot display of Fig. IB, the excitation occurred in both the Lftward (upper half of the dot display demarcated by a horizontal dotted line) and rightward movements (iower half ). Thus the excitation was not specific to the direction of the movements. Therefore, an average response histogram (C) was constructed by combining responses td horizontal movements both leftward and rightward (D). It indicates that the excitation starts as early as 2.5-50 msec after the onSet of saccadic movements, attains a maximum at 100 msec (when the eyes reach their final positions), and declines gradually during the succeeding several hundred milliseconds. Although most striate cells (n = 87) exhibited no strong directionality for saccade-excitation. a minority of celIs (n = 21) were strongly direction-specific, and excitation occurred only for eye movements in a preferred direction. In these cells the preferred direction agreed with that predicted from the directionat preference for movement of a light slit (see below). Responses of the saccade-excited neurons persisted in most cells (57/77 cells) even in absolute darkness (E-H in Fig. I), although their latencies were longer (about 150msec) and the number of discharged impulses was smaller than that with the checker pattern displayed (cf. with A-D). It is indicated that in carkness the initial part of the excitation diminish~. fience it is likely that the excitation evoked by saccadie movements during presentation of the checker pattern involves both visual and non-visual compo-
nents. The onset of the visual appears earlier than the non-visuaf component. The saccade-inhibited eelIs maintained spontaneous impulse discharges of a very low Frequency (less than 2 impuises/sec) in darkness. but they maintained discharges of 3&50impulses/sec in the presence of the checker ,pattern. A strong suppression of the discharges was caused by saccadic movements either leftward or rightward (I and J). The inhibition occurred at about 50msec after the onset of the movements and continued for the entire period of the movements (150msec). The saccade-inhibition disappeared completely in darkness. In 38 of the 157 neurons sampled, responsiveness to photic stimulation was also studied under withdrawal of the reward, which suppressed saccadic eye movements for several minutes, and in additional 27 cells under retrobulbar paralysis, which paralysed movements of both eyes for more than 2Omin (see EGG traces in Figs X3-D and F-G). Following withdrawal of the reward, location of receptive field, ocular and orientation preferences were roughly determined with a hand-moved light slit, and internal structures of the receptive field were systemati~aliy studied using a computer-controlled visual stimulator (Tanaka and Toyama. 1978). Under retrobulbar paralysis, other response properties such as orientation and velocity tunings were investigated as well. About one third of these cells (n = 19) exhibited a relatively narrow receptive field (0.5-3.0’). Presenta-
Research Note
A b C I0
D j
I
11 I-
Fig. 2. Responses to photic stimulation under retrobutbar paralysis. (A). schematic diagram illustrating the receptive field of a “simple” celi and a light stimulus. Stippled area area producing prominent on response (on area). Hatched area that for 08 response (off area). Thick solid line indicates stationary light slits presented at two different positioni (b and c) of the receptive field of the “simple” cetl. (B)-(D), responses of the “simple” cell. (B), that with a stationary light slit exposed at position (b). Uppermost trace, impulse discharges recorded with a pen-recorder. The impulses were shaped up through Schmitt trigger circuit. Lower two traces (H and V), EOGs for horizontal and vertical eye movements. (CL with the light slit at position (cl. The bottom trace indicates the onset (upward deflection) and offset (downward deflection) of the light stimulus. (D), with a moving light slit. The bottom trace represents movement of the light slit. (E)-(G), similar to (A)-(D) but for a “complex” cell. All records in (BHD) and (F)-(G) were obtained under retrobulbar paralysis of both eyes induced by injecting 0.3 ml of 5”; xylocaine to each eye. EOG calibration in (B) applies to all records. Time calibration of 0.5 set in (0) also applies to (B) and (CT).
tion of a stationary tive field (position
light slit in a region of their recep (b) in Fig. 2A) produced a sus-
tained on response (Fig. 2B), while an off response (Fig. 2C) was obtained in another region (position (c) in Fig. 2A). Systematic mapping revealed that the receptive field was composed of two sub-areas adjoining each other, one producing an on response (stippled area in Fig. 2A) and the other producing an o# response (hatched area). These cells also produced a short burst of impulses when a light slit moved across the border of the on and ofltesponse areas (Fig. 2D). They responded optimally to a tight stimulus moving at a relatively siow velocity (less than 2Odeg/sec). All of these response properties match characteristics of “simple” cells (Hubel and Wiesel, 1962; Bishop et al., 1973). Most of the remaining two thirds of cells (n = 37) exhibited a larger receptive field (2-14’) than the former group. In most parts of the receptive field (stippled and hatched area in Fig. 2E), a stationary light slit produced a transient on-off response (Fig. ZF), and their receptive field consisted of on and
offareas overlapping _. . each other (Fig. ZE). These cells were also responsive to a moving light slit. However the optimal stimulus velocity was greater (20-100 deg/ set) than for the former group of cells (Fig. 2G). Therefore the latter group of cells seems to correspond to “complex” cells. The remaining 9 ceils exhibited responsiveness intermediate between the “simple” and “complex” celis (n = 4) or weak responsiveness to photic stimulation (n = 5). Therefore, the classification of “simple” and ‘*complex” ceils which has been defined in anaesthet~ed cats appears to be applicable to alert cats. Of the 65 neurons in which responses both to saccadic eye movements and to photic stimulation were studied, 46 neurons were saccade-excited and involved all of the “complex” (n = 37). intermediate (n = 4) and weakly responsive cells (n = 5). By contrast, the saccade-inhibited neurons (n = 19) were all “simple” cells. These observations lead us to postulate that the “simple” and “complex” celIs provide parallel rather than serial channels of visual information (Stone and
Research
556
Dreher, 1973: Toyama rr ~11..19731,which are opened altemativef~. i.e. the “complex” cells during saccadic movements and the “simpte” cells during fixation of the eyes. This is similar to &he hypothesis that two processes of visual perceptions (McKay. 1973) operate alternatively. image perception during eye fixation and coordinate evaluation during saccadic eye movements. The inputs responsible for inhibition of the “simple” cells seem to be visual in origin (Noda. 1975). since it disappeared in darkness. while excitation of the “complex” cells involved visual and nonv*isualcomponents. The source of non-visual inputs to the “complex” cells is not clear at the present stage of investigation. Preliminary observation under retrobulbar block indicates that even during paralysis of eye movements the non-visual inputs still impinge on the *‘complex” cells in association with the ocuiomotor activities. Therefore it is tempting to assume that they are oculomotor in origin. It may be that the non-visual inputs convey rather crude information about the eye movements. The “complex” cells may assess the coordinates using crude motor information as a cue for discriminating the movement of the eyes and that of the image. .-lcXnorc(rdyr,nmr.s-The authors thank Professor M. Ito ror his helpful discussion and constant encouragement.
REFERE?iCES
Bishop P. 0..
Coombs J. S. and Henry G. H. (1973) Receptive fields of simple cells in the cat striate cortex. J. Phtsiol. 231, 3 l-60. Corazza R.. Lombroso C. f. and DutTy F. Ii. (1972) Time course of visual multi-neuronal discharges evoked by eye movements in light. Brain Res. 38, 109-l 16. Crewther D. P.. Crewther S. G. and Pettigrew J. D. (1978) ,A role for extraocular afferents in post-critical period
Note
reversal ISI-i9;.
of
monocular
deprt~arron.
J.
fh\-~1111. 282.
Duff? F.
H. and Burchnsl 1. L. ttY5t Eye morementrelated inhibition of primate \isu..rl neurons. Brum Rc*\ 89. 121-133. Hoist E. \on and Mittrlstaedt H. 11950) Das Realferenzprinzip 1W’echselwirkunpen zwischen Zentralner\ensystern und Prripheriel .~~rtrrr~,l.~sensrliufivn 37, -!6&476. Hubel D. H. and Wiesel T. N. 11962) Receptive iieids. binocular interaction and functional architecture in the cat’s visual cortex. J. Phvsi0l. 160, 106-l 51. Jung R. (I9731 Visual perception and neuroph>siolouv. In Handbook ofSm.sor~~ Phuioiouv. 1’01. VII 3. DD. 1?S?. Kasamatsu T.‘( 1976) cisu& cortical neurons in~uenced b\ the oculomotor input: Characterization of their rece& tive field properties. groin Rcs. 113. 271-292. MacKay D. M. (1973) Visual stabrlitk and voluntary e!e movements. In ~~~(~~o(~~ 0j Sen+~r!. ~~~~si~l~‘)~~!, Vol VII 3. pp. 307-332. Noda H. (19753 Discharges of relay cells in lateml geniculate nucleus of the cat during spontaneous e>e mo\rments in light and darkness. J. Ph~~~iol. 250. 579-595. Noda H.. Freeman R. B. and Creutzfeld 0. D. (19721 Neuronal correlates of eye morements in the visual cortex of the eat. Science 175. 661661. Schlag J.. Lehtinen I. and Schlag-Re! M (1974 Seuronal actirity before and during eye movements in thalamie internal mcdulfary lamina of the cat. J. .Verwoph,r~inl. 37. 982-995. Sperry R. W. (1950) Neuronal basis of the spontaneous optokinetic response produced ty visual inlcrsion. J. camp. ph.rriol. P,~~Cl?Ol.43, 4SZJS9. Stone J. and Dreher B. (1973) Projection of X- and Y-cells of the cat’s lateral geniculate nucleus to areas I7 and 18 of kisuai cortex. J. Neuroph~siol. 36. 551-567. Tanaka K. and Toyama K. (1978) Computer-controlled visual stimulator for electrophysioisgical experiments. C’:.vio~ Rrs. 18. 74%7JS. Toyama K.. .Maekawa K. and Takeds T. (l973! .An anal!sts of neuronal circuitry for two types of visual cortical neurones classifted on the basis oi their responses to photic stimuli. Brain RCF. 61. 395%). Wurtz R. H. (1969) Responses of striate stimuli during rapid eye movements :Vrw-ophFsio/. 32. 975-986.
cortex neurons in the monkey.
to J.
DIFFERENTIAL RESPONSES OF “SIMPLE” AND “COMPLEX” CELLS OF CAT’S STRIATE CORTEX DURING SACCADIC EYE MOVEMENTS M. KWJRA’, Y. KOMATSUand K. TOY&MA Department of Physiology. Faculty of Medicine. University of Tokyo and Department of Physiology, Nagoya University, School of Medicine, Japan (Receired
The stability of visual images during eye movement has long been a subject of psychophysics (Jung, 1973). It has been hypothesized that a visual image is ‘perceived” as stable by subtraction of the motor signals for an eye movement from the reagerent retinal signals resulting from that eye movement (Hoist, 1950; Sperry, 1950). It has also been suggested that visual perception involves two independent processes, one perceiving an image and the other evaluating the coordinates of the perceived image in connection with the concurrent eye movement (MacKay, 1973). Both of these hypotheses incorporate motor signals into the process of image stabilization or coordinate evaluation. Efforts have been devoted to finding neuronal correlates to these hypotheses in the visual cortex of an alert animal, but the results have been rather controversial (Wurtz. 1969; Corazza et al., 1972; Duffy and Burchfiel, 1975; Noda er al., 1972: Kasamatsu, 1976). The main difficulties in these studies have been in keeping an animal fully alert and in motivating eye movements in darkness in a reproducible manner. In the present experiment these difficulties were removed by using eye movements evoked by reinforcement. Responses of striate cortex neurons of waterdeprived cats were studied during saccadic eye movements rewarded with water (Schlag et al., 1974) and also during eye fixation caused by withdrawal of the reward or by retrobulbar paralysis. The results suggest that the “simple” cells are related to the initial image perception, and the “complex’* cells to evaluation of the coordinates. Several days prior to the experiment, preparatory surgery was made on a cat under anaesthesia with Ketamine (40 mg/kg). The surgery involved (1) placement of a recording chamber over the striate cortex, (2) installation of holders on the skull for fixation of the cat’s head. (3) implantation of Ag-AgCl electrodes at the external canthi of both orbits for recording electrooculograms (EOGs) and (4) installation of injection needles for retrobulbar paralysis of both * Present address: Jichi Medical School Minamikawachi-Machi. T&higi 329-04. Japan.
30 Jttfy 1979)
eyes (Crewther et al., 1978). After recovery from the surgery, the cat was deprived of water and was trained to stay quietly with the head fixed on the stereotaxic frame and to make saccadic eye movements. During the training the EOGs were continuously monitored and a reward (a drop of water, 0.05 ml) was given for every qualified eye movement (horizontal saccades greater than 10” and faster than 4Odeg/sec). Within a few days. cats performed saccadie eye movements as frequently as 60 times/min, and could fulfill their daily demand of water (about 100 ml) in an hour. Cats were further trained to adapt to temporal withdrawal of the reward and to stay quietly on the stereotaxic frame with much less frequent saccadic eye movements (l-3 times/min). The trained cat was fixed on the frame. Patterned light stimuli (l-l.5 log units brighter than the background illumination of 3.5 cd/m’) such as light slits (0.5-2” wide and 2-40” long) or a checker pattern (periodicity, 3-5’) were projected on a translucent screen placed in front of the animal (distance. 57 cm). Impulse discharges were recorded extracellularly from striate neurons with a glass-coated stainless steel microelectrode while the cat was performing the trained task. The recording session, during which the task was partially reinforced (a reward for every few saccadie eye movements), was continued for a few hours. and was repeated once a day for about two weeks. Electrolytic marking was performed for the last ceil sampled in every track and the location of the celt in area 17 was confirmed histologically. One hundred and fifty-seven neurons were sampled from three cats under the above described conditions. When a checker pattern was displayed on the screen, almost all of these cells (149 of the 157 cells) exhibited a change of their spike activity in connection with saccadic eye movements. There was a distinct dichotomy in their response patterns; an excitation in one group of cells (n = 108) and an inhibition in the other (a = 41). The saccade-excited neurons discharged spontaneously at a relatively low frequency (less than 10 impulses/set) in the absence of saccadic eye movements. but they responded briskly to a saccadic move553
Peszarch
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Fig. I. Responses to saccadic eye movements. fA)-(D). responses of a saccade-excited cell during display of checker. (A). upper trace. a specimen record of impulse discharges and lower trace. electrooculogram (EOG) for horizontal eye movement. Upward deflection in EOG represents leftward movement. (ES).dot displays of impulse discharges. Horizontal dotted line demarcates responses for leftward (upper half) and rightward (lower haI0 movements. (C), an average response histogram for responses shown in (B). (DL traces of EOG. Time axis is common to (AHD). Zero in the axis represents the onset of the saccadic eye movements. (E)-(H), similar to (A)-(D), but in darkness. (I)-(L). similar to (A)-(D). but for a saccadeinhibited cell. Calibration for EOGs is common to (A). (D). (E). (H), (I) and (L), and voltage calibration of 0.5 mV to (A). (E) and (I).
ment (Fig. IA). As shown in the dot display of Fig. IB, the excitation occurred in both the Lftward (upper half of the dot display demarcated by a horizontal dotted line) and rightward movements (iower half ). Thus the excitation was not specific to the direction of the movements. Therefore, an average response histogram (C) was constructed by combining responses td horizontal movements both leftward and rightward (D). It indicates that the excitation starts as early as 2.5-50 msec after the onSet of saccadic movements, attains a maximum at 100 msec (when the eyes reach their final positions), and declines gradually during the succeeding several hundred milliseconds. Although most striate cells (n = 87) exhibited no strong directionality for saccade-excitation. a minority of celIs (n = 21) were strongly direction-specific, and excitation occurred only for eye movements in a preferred direction. In these cells the preferred direction agreed with that predicted from the directionat preference for movement of a light slit (see below). Responses of the saccade-excited neurons persisted in most cells (57/77 cells) even in absolute darkness (E-H in Fig. I), although their latencies were longer (about 150msec) and the number of discharged impulses was smaller than that with the checker pattern displayed (cf. with A-D). It is indicated that in carkness the initial part of the excitation diminish~. fience it is likely that the excitation evoked by saccadie movements during presentation of the checker pattern involves both visual and non-visual compo-
nents. The onset of the visual appears earlier than the non-visuaf component. The saccade-inhibited eelIs maintained spontaneous impulse discharges of a very low Frequency (less than 2 impuises/sec) in darkness. but they maintained discharges of 3&50impulses/sec in the presence of the checker ,pattern. A strong suppression of the discharges was caused by saccadic movements either leftward or rightward (I and J). The inhibition occurred at about 50msec after the onset of the movements and continued for the entire period of the movements (150msec). The saccade-inhibition disappeared completely in darkness. In 38 of the 157 neurons sampled, responsiveness to photic stimulation was also studied under withdrawal of the reward, which suppressed saccadic eye movements for several minutes, and in additional 27 cells under retrobulbar paralysis, which paralysed movements of both eyes for more than 2Omin (see EGG traces in Figs X3-D and F-G). Following withdrawal of the reward, location of receptive field, ocular and orientation preferences were roughly determined with a hand-moved light slit, and internal structures of the receptive field were systemati~aliy studied using a computer-controlled visual stimulator (Tanaka and Toyama. 1978). Under retrobulbar paralysis, other response properties such as orientation and velocity tunings were investigated as well. About one third of these cells (n = 19) exhibited a relatively narrow receptive field (0.5-3.0’). Presenta-
Research Note
A b C I0
D j
I
11 I-
Fig. 2. Responses to photic stimulation under retrobutbar paralysis. (A). schematic diagram illustrating the receptive field of a “simple” celi and a light stimulus. Stippled area area producing prominent on response (on area). Hatched area that for 08 response (off area). Thick solid line indicates stationary light slits presented at two different positioni (b and c) of the receptive field of the “simple” cetl. (B)-(D), responses of the “simple” cell. (B), that with a stationary light slit exposed at position (b). Uppermost trace, impulse discharges recorded with a pen-recorder. The impulses were shaped up through Schmitt trigger circuit. Lower two traces (H and V), EOGs for horizontal and vertical eye movements. (CL with the light slit at position (cl. The bottom trace indicates the onset (upward deflection) and offset (downward deflection) of the light stimulus. (D), with a moving light slit. The bottom trace represents movement of the light slit. (E)-(G), similar to (A)-(D) but for a “complex” cell. All records in (BHD) and (F)-(G) were obtained under retrobulbar paralysis of both eyes induced by injecting 0.3 ml of 5”; xylocaine to each eye. EOG calibration in (B) applies to all records. Time calibration of 0.5 set in (0) also applies to (B) and (CT).
tion of a stationary tive field (position
light slit in a region of their recep (b) in Fig. 2A) produced a sus-
tained on response (Fig. 2B), while an off response (Fig. 2C) was obtained in another region (position (c) in Fig. 2A). Systematic mapping revealed that the receptive field was composed of two sub-areas adjoining each other, one producing an on response (stippled area in Fig. 2A) and the other producing an o# response (hatched area). These cells also produced a short burst of impulses when a light slit moved across the border of the on and ofltesponse areas (Fig. 2D). They responded optimally to a tight stimulus moving at a relatively siow velocity (less than 2Odeg/sec). All of these response properties match characteristics of “simple” cells (Hubel and Wiesel, 1962; Bishop et al., 1973). Most of the remaining two thirds of cells (n = 37) exhibited a larger receptive field (2-14’) than the former group. In most parts of the receptive field (stippled and hatched area in Fig. 2E), a stationary light slit produced a transient on-off response (Fig. ZF), and their receptive field consisted of on and
offareas overlapping _. . each other (Fig. ZE). These cells were also responsive to a moving light slit. However the optimal stimulus velocity was greater (20-100 deg/ set) than for the former group of cells (Fig. 2G). Therefore the latter group of cells seems to correspond to “complex” cells. The remaining 9 ceils exhibited responsiveness intermediate between the “simple” and “complex” celis (n = 4) or weak responsiveness to photic stimulation (n = 5). Therefore, the classification of “simple” and ‘*complex” ceils which has been defined in anaesthet~ed cats appears to be applicable to alert cats. Of the 65 neurons in which responses both to saccadic eye movements and to photic stimulation were studied, 46 neurons were saccade-excited and involved all of the “complex” (n = 37). intermediate (n = 4) and weakly responsive cells (n = 5). By contrast, the saccade-inhibited neurons (n = 19) were all “simple” cells. These observations lead us to postulate that the “simple” and “complex” celIs provide parallel rather than serial channels of visual information (Stone and
Research
556
Dreher, 1973: Toyama rr ~11..19731,which are opened altemativef~. i.e. the “complex” cells during saccadic movements and the “simpte” cells during fixation of the eyes. This is similar to &he hypothesis that two processes of visual perceptions (McKay. 1973) operate alternatively. image perception during eye fixation and coordinate evaluation during saccadic eye movements. The inputs responsible for inhibition of the “simple” cells seem to be visual in origin (Noda. 1975). since it disappeared in darkness. while excitation of the “complex” cells involved visual and nonv*isualcomponents. The source of non-visual inputs to the “complex” cells is not clear at the present stage of investigation. Preliminary observation under retrobulbar block indicates that even during paralysis of eye movements the non-visual inputs still impinge on the *‘complex” cells in association with the ocuiomotor activities. Therefore it is tempting to assume that they are oculomotor in origin. It may be that the non-visual inputs convey rather crude information about the eye movements. The “complex” cells may assess the coordinates using crude motor information as a cue for discriminating the movement of the eyes and that of the image. .-lcXnorc(rdyr,nmr.s-The authors thank Professor M. Ito ror his helpful discussion and constant encouragement.
REFERE?iCES
Bishop P. 0..
Coombs J. S. and Henry G. H. (1973) Receptive fields of simple cells in the cat striate cortex. J. Phtsiol. 231, 3 l-60. Corazza R.. Lombroso C. f. and DutTy F. Ii. (1972) Time course of visual multi-neuronal discharges evoked by eye movements in light. Brain Res. 38, 109-l 16. Crewther D. P.. Crewther S. G. and Pettigrew J. D. (1978) ,A role for extraocular afferents in post-critical period
Note
reversal ISI-i9;.
of
monocular
deprt~arron.
J.
fh\-~1111. 282.
Duff? F.
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