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Afferent visual pathways and receptive field properties of superior colliculus neurons in stroboscopically reared cats
Neuroscience Letters, 19 (1980) 283-288
283
© Elsevier/North-Holland Scientific Publishers Ltd.
A F F E R E N T V I S U A L P A T H W A Y S A N D R E C E P T I V E FIELD P R O P E R T I E S OF S U P E R I O R C O L L I C U L U S NEURONS IN S T R O B O S C O P I C A L L Y R E A R E D CATS
H. KENNEDY, J.M. FLANDRIN and B. AMBLARD Laboratoire de Neuropsychologie ExpOrimentale, INSERM U 94, 16 avenue Doyen L~pine, 69500 Bron (France)
and (B.A.) Institut de Neurophysiologie et Psychophysiologie CNRS, DOpartement de Psychophysiologie, 31 chemin J. Aiguier, 13009 Marseille (France)
(Received June 20th, 1980) (Revised version received June 30th, 1980) (Accepted June 30th, 1980)
SUMMARY Unit recordings were made in the superior colliculus of strobe-reared cats. Receptive field properties were studied and electrical stimulation in the chiasma and optic tract made it possible to characterize the visual input. The retinal Y-cell input and the cortical input were found to be deficient. The principal response deficit was the decrease of selective response to direction of movement, also shown to be largely absent in the corticotectal pathway. These results are compared to similar findings in dark-reared animals and discussed in connection with the importance of visual movement to the developing visual system.
Stroboscopic illumination allows experience of visual patterns but abolishes that of visual movement. Rearing animals ~n a stroboscopic illumination (strobe rearing) has been shown to produce marked deficits at the level of the visual cortex [2-4, 13, 14] as well as superior colliculus (SC) [1, 7]. The principal deficits in the SC include a reduced selectivity of the neuron to the direction of movement (directionality) and a decrease in the influence of the ipsilateral eye (binocularity). These deficits give rise to a SC which resembles that of the newborn animal [12, 18] and that of a darkreared animal [5, 10]. Visual decortication also produces the same effects [6, 16, 19]. The present study sets out to examine the visual afferents to the SC of strobe-reared
284 animals. Comparison of the types of visual afferents to the SC neurons and their functional deficits in dark-reared and in strobe-reared animals makes it possible to evaluate the importance of visual movement in the acquisition of normal adult function. There are three visual pathways to the SC of the normal cat [8]. A retinotectal Wdirect pathway which is afferent to 73% of SC neurons and originates from W retinal ganglion cells; a retinotectal Y-direct pathway which is afferent to 9°70 of SC neurons and originates from Y retinal ganglion cells; and a Y-indirect pathway which originates from Y retinal ganglion cells and is afferent to 18% of SC neurons after completing a geniculocortical loop involving a geniculate Y-cell and a cortical complex cell [8]. We have studied the receptive field (RF) characteristics of SC neurons and, using H o f f m a n n ' s protocol [8], have analyzed their afferent visual connections. Three cats were used. They were exposed to stroboscopic illumination for 12 h / d a y at a frequency of 2/sec and a flash duration of 0.2 msec. Duration of strobe rearing was 10 months from birth. Prior to testing the cats were anesthetized with Imalgene (ketamine base, 15 m g / k g intramuscular), so as to allow a tracheal cannula and an intravenous catheter to be placed. The animal was positioned in a stereotaxic frame and paralyzed by an intravenous injection of Flaxedil (20 mg/kg) and artificially ventilated. Throughout the experiment, the animal was paralyzed with a continuous intravenous infusion of 5 m g / k g / h of Flaxedil. 'Care was taken that the cat did not suffer during the experiment. Points of contact and wounds caused by the placement of the cannula and the catheter were frequently injected with 5°70 Xylocaine. The animal was maintained between 37 and 38°C by means of a warming blanket. The lids were maintained retracted by 15°70 Neosynephrine and pupils dilated by 1% atropine. Corneas were prevented from drying by corrective corneal lenses. The skull was opened after local injection of Xylocaine, and the cortex above the SC exposed and protected by an agar film. Neurons were recorded by tungsten microelectrodes. Visual stimulation was made by means of manual displacement of dark edges and small light spots projected onto a screen, covering the visual field, placed 70 cm in front of the animal. Response to flashed diffuse lighting of the visual field was examined. By further use of a visual stimulator controlled by a P D P 8 computer, it was possible to obtain a topographical representation and a spatial histogram of the RF. This set-up enabled an exact mapping of the RF and a precise verification of its directionality to be obtained when this was considered necessary. In these experiments the directionality, ocular dominance and response to diffuse flash were tested. We have classified as direction-selective all neurons giving an increased response for movement in a particular direction. Binocularity was estimated by means of the audible response. Alternative eye stimulation allowed the neurons to be classified in one of 5 groups ranging from purely contralateral (group 1) to purely ipsilateral (group 5). Bipolar stimulation electrodes (tip exposed 1 mm, tip separation 2 ram) were placed
285
stereotaxically. A first electrode was placed in the optic chiasma (OX) (14-15 m m anterior and 1 m m lateral). A second stimulation electrode was placed in the optic tract (OT) ( 8 - 9 m m anterior and 10 m m lateral). So as to optimally place the stimulation electrodes they were initially connected to the recording equipment and the final position was determined by the optimal response to a light flash. Electrical stimuli were 50-100 /zsec pulses o f up to 15 V amplitude. Latencies of spike discharge were taken from the oscilloscope screen. A total of 110 neurons were recorded and 63 (57o70) could be driven by electrical stimulation in the OX and OT. SC neurons receiving an input from retinal W-cells responded to OX stimulation with a mean latency of 6.9 msec. With a shift of the stimulation site to the O T this latency decreased to a mean value of 4.3 msec (Fig. 1). This decrease in latency corresponds to the time required for the axon
IY
25 " A
/W
/ 20
/ /
15
OX
10
'-
E
0
15
,
,~
B
~
'
,
1
E
10
o,
/ / m
i
0
t, 2
j~ 4
l,
,
i
I
6 rflsec
8
lO
12
Fig. 1. Diagram showing the distribution of response latencies in 110 SC neurons following stimulation of O X in A and O T in B. Vertical axis: n u m b e r of units; horizontal axis: latency in msec. The input to each neuron was identified according to the latency to OX stimulation and its conduction velocity (see text). Black bars: Y-cell direct input; hatched bars: Y-cell indirect input; open bars: W-cell input. Arrows indicate mean latency values. Forty-eight neurons which did not respond to OX stimulation are not shown.
286 TABLE 1 A F F E R E N T VISUAL P A T H W A Y S TO T H E SUPERIOR C O L L I C U L U S OF STROBE-REARED, N O R M A L A N D B I N O C U L A R L Y DEPRIVED CATS Cell proportions for both groups of deprived cats differ significantly (P < 0.001, x 2 test) from the normal. Figures in brackets refer to number o f cells. Afferent pathway Y-direct input
Y-indirect input
W-direct input
Undetermined
9%
18%
73%
0%
Strobe-reared (110)
2.7%
4.5%
50%
43%
Binocularly deprived b (84)
2.0%
0%
67%
31%
Normal" (170)
aData taken from ref. 8. bData taken from ref. 10.
conductance between OX and OT, the mean value of which was approximately 4.6 m/sec. SC neurons receiving direct and indirect input from retinal Y-cells showed a mean latency difference of 0.53 msec following OX and OT stimulation which corresponds to a conduction velocity of approximately 19.5 m/sec. The Y-indirect input to SC showed much longer OT and OX latencies due to the cortical loop. In fact the mean OX and OT latencies are not very different from those of W-cell input. To differentiate between W-cell and Y-indirect input it is necessary to compare the latency in response to OX and OT stimulation. Whereas the shift in latency is large for W-cell input due to the slow conductance of W-cell axons, the shift in latency for the Y-indirect input is much shorter due to the higher conduction velocities of the Y-cell axons. This is made clear in Fig. 1 where the slope of the line connecting the mean latency for the Y-direct input is very similar to that for the Yindirect input. In Table I are shown the proportions of Y-direct, Y-indirect and Wdirect inputs for normal, strobe-reared and binocularly deprived animals. (Data for the normal cat were taken from ref. 8 and for the binocularly deprived cat from ref. 10.) We found that in the strobe-reared animal 55 cells (50%) had W-direct input, 3 cells (2.7%) had Y-direct input and 5 cells (4.5%) had Y-indirect input. Forty-eight cells could not be driven by stimulation from OX. This is statistically* different (P < 0.001) from the normal animal and shows that strobe rearing results in: (1) a severe loss of Y-direct and Y-indirect inputs to SC; (2) no change in W-direct input; and (3) a large number of neurons which cannot be driven from the OX. Concomitant with the change in visual afference was a change in RF characteristics of SC neurons in strobe reared cats (see Table II). Strobe rearing results in a drastic reduction of direction-selective units (84% in the normal animal and only 12°70 in the strobe-reared). This is accompanied by a less dramatic but nevertheless * x2-test is used for all statistical analysis in this paper.
287 T A B L E 11 T H E P R O P O R T I O N OF D I R E C T I O N SELECTIVE CELLS A N D CELLS B E L O N G I N G TO O C U L A R D O M I N A N C E G R O U P S 2, 3 A N D 4 IN N O R M A L , S T R O B E - R E A R E D A N D B I N O C U L A R L Y DEPRIVED CATS Direction-selective ceils
Binocular driven cells
Normal a
84% (87)
85°7o (54)
Strobe-reared (110)
1207o (110)
38070 (110)
Binocularly deprived b
17o70 (42)
51% (118)
aData from ref. 5. bData from ref. 10.
significant reduction in the number of neurons which can be influenced by both eyes (85% in ocular dominance groups 2, 3 and 4 in the adult and 42% in the strobereared animal). The interpretation of the effects of strobe rearing makes it necessary to distinguish between firstly the failure to develop normal adult-like neuron response characteristics due to an absence of a type of visual input (i.e. visual movement), and secondly the development of abnormal neuron response properties due to an aberrant visual input. Comparison of the effects of dark-rearing and strobe-rearing make this possible. Binocularly deprived animals have been shown by H o f f m a n n and Sherman to have impaired visual input to SC [10]. Their results are shown in Table I. Binocularly deprived animals appear very similar to strobe-reared animals in that the W-direct input to the SC appears to be spared. In their study H o f f m a n n and Sherman found an absence of SC neurons which received a Y-indirect input. There is a decrease in the proportion of cells receiving a Y-indirect input in strobe animals. However, the difference between the decrease in the proportion of cells receiving Yindirect and Y-direct inputs is not statistically significant. Animals deprived of visual experience from birth also show certain RF deficits in c o m m o n with strobereared animals. Both rearing procedures give rise to a similar decrease in direction selectivity and the proportion of SC cells in ocular dominance groups 2, 3 and 4 (see Table II). The similarity of the proportion of direction-selective neurons in both groups of animals indicates that experience of visual movement is the essential criterion for the acquisition of this RF property. Binocular deprivation of visual pattern a n d / o r movement appears to be of much less importance in the retention of a normal ocular dominance distribution. This contrasts with the well established finding that monocular deprivation results in a profound modification of the ocular dominance distribution in both the cortex and superior colliculus [9, 20]. Our results support the claim that it is the absence of movement, in both dark-reared and strobe-reared animals, that results in an absence of direction selectivity. Corticotectal cells are the last link in the Y-indirect pathway. In the normal adult, over 70% of these cells are direction-selective and binocular [8, 15]. O f the 5 neurons in the SC of the strobe animal which were found to receive a Y-indirect
288
input, only one showed selectivity for the direction of motion although 4 could be driven by both eyes. These results support the notion [7] that the absence of direction selectivity of SC neurons of strobe-reared animals reflects a cortical deficit. Selectivity to direction of movement in the cortex has been shown to be dependent on intracortical inhibition [17] and to be absent in young animals [11]. It would seem, therefore, that movement of the retinal image, resulting either from saccadic eye movements or from movement of the visual stimuli, is essential for the development of this visual cortical response property. REFERENCES 1
2 3 4 5 6 7 8 9 10 I1 12 13 14 15 16 17 18 19 20
Chalupa, L.M. and Rhoades, R.W., Modification of visual response properties in the superior colliculus of the golden hamster following stroboscopic rearing, J. Physiol. (Lond.), 274 (1978) 571-592. Cynader, M., Berman, N. and Hein, A., Cats reared in stroboscopic illumination: effects on receptive fields in visual cortex, Proc. nat. Acad. Sci. (Wash.), 70 (1973) 1353-1354. Cynader, M., Berman, N. and Hein, A., Recovery of function in cat visual cortex following prolonged deprivation, Exp. Brain Res., 25 (1976) 139-156. Cynader, M. and Chernenko, G., Abolition of direction selectivity in the visual cortex of the cat, Science, 193 (1976) 504-505. Flandrin, J.M. and Jeannerod, M., Superior colliculus: environmental influences on the development of directional responses in the kitten, Brain Res., 89 (1975) 348-352. Flandrin, J.M. and Jeannerod, M., Lack of recovery in collicular neurons from the effects of early deprivation or neonatal cortical lesion in kitten, Brain Res., 120 (1977) 362 366. Flandrin, J.M., Kennedy, H. and Amblard, B., Effects of stroboscopic rearing on the binocularity and directionality of cat superior colliculus neurons, Brain Res., 101 (1976) 576-581. Hoffmann, K.P., Conduction velocity in pathways from retina to superior colliculus in the cat: a correlation with receptive-field properties, J. Neurophysiol., 36 (1973) 409-424. Hoffmann, K.P. and Sherman, S.M., Effects of early monocular deprivation on visual inpuLto cat superior colliculus, J. Neurophysiol., 37 (1974) 1276-1286. Hoffmann, K.P. and Sherman, S.M., Effects of early binocular deprivation on visual input to cat superior colliculus, J. Neurophysiol., 38 (1975) 1049-1059. Kennedy, H., Martin, K.A.C. and Whitteridge, D., Receptive field characteristics in area 17 of adult and newborn sheep, J. Physiol. (Lond.), 300 (1980) 55P. Norton, T.T., Receptive fields properties of superior colliculus cells and development of visual behavior in kittens, J. Neurophysiol., 37 (1974) 674-690. Olson, C.R. and Pettigrew, J.D., Single units in visual cortex of kittens reared in stroboscopic illumination, Brain Res., 70 (1974) 189-204. Orban, G.A., Kennedy, H., Maes, H. and Amblard, B., Cats reared in stroboscopic illumination: velocity characteristics of area 18 neurons, Arch. ital. Biol., 116 (1978) 413-419. Palmer, L.A. and Rosenquist, A.C., Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat, Brain Res., 67 (1974) 27-42. Rosenquist, A.C. and Palmer, L.A., Visual receptive field properties of cells of the superior colliculus after cortical lesions in the cat. Exp. Neurol., 33 (1971) 629-652. Sillito, A.M., Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex, J. Physiol. (Lond.), 271 (1977) 699-720. Stein, B.E., Labos, E. and Kr~iger, L., Sequence of changes in properties of neurons of superior colliculus of the kitten during maturation, J. Neurophysiol., 36 (1973) 667-679. Wickelgren, B.G. and Sterling, P., Influence of visual cortex on receptive fields in the superior colliculus of the cat, J. Neurophysiol., 32 (1969) 16-23. Wiesel, T.N. and Hubel, D.H., Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens, J. Neurophysiol., 28 (1965) 1029-1040.
283
© Elsevier/North-Holland Scientific Publishers Ltd.
A F F E R E N T V I S U A L P A T H W A Y S A N D R E C E P T I V E FIELD P R O P E R T I E S OF S U P E R I O R C O L L I C U L U S NEURONS IN S T R O B O S C O P I C A L L Y R E A R E D CATS
H. KENNEDY, J.M. FLANDRIN and B. AMBLARD Laboratoire de Neuropsychologie ExpOrimentale, INSERM U 94, 16 avenue Doyen L~pine, 69500 Bron (France)
and (B.A.) Institut de Neurophysiologie et Psychophysiologie CNRS, DOpartement de Psychophysiologie, 31 chemin J. Aiguier, 13009 Marseille (France)
(Received June 20th, 1980) (Revised version received June 30th, 1980) (Accepted June 30th, 1980)
SUMMARY Unit recordings were made in the superior colliculus of strobe-reared cats. Receptive field properties were studied and electrical stimulation in the chiasma and optic tract made it possible to characterize the visual input. The retinal Y-cell input and the cortical input were found to be deficient. The principal response deficit was the decrease of selective response to direction of movement, also shown to be largely absent in the corticotectal pathway. These results are compared to similar findings in dark-reared animals and discussed in connection with the importance of visual movement to the developing visual system.
Stroboscopic illumination allows experience of visual patterns but abolishes that of visual movement. Rearing animals ~n a stroboscopic illumination (strobe rearing) has been shown to produce marked deficits at the level of the visual cortex [2-4, 13, 14] as well as superior colliculus (SC) [1, 7]. The principal deficits in the SC include a reduced selectivity of the neuron to the direction of movement (directionality) and a decrease in the influence of the ipsilateral eye (binocularity). These deficits give rise to a SC which resembles that of the newborn animal [12, 18] and that of a darkreared animal [5, 10]. Visual decortication also produces the same effects [6, 16, 19]. The present study sets out to examine the visual afferents to the SC of strobe-reared
284 animals. Comparison of the types of visual afferents to the SC neurons and their functional deficits in dark-reared and in strobe-reared animals makes it possible to evaluate the importance of visual movement in the acquisition of normal adult function. There are three visual pathways to the SC of the normal cat [8]. A retinotectal Wdirect pathway which is afferent to 73% of SC neurons and originates from W retinal ganglion cells; a retinotectal Y-direct pathway which is afferent to 9°70 of SC neurons and originates from Y retinal ganglion cells; and a Y-indirect pathway which originates from Y retinal ganglion cells and is afferent to 18% of SC neurons after completing a geniculocortical loop involving a geniculate Y-cell and a cortical complex cell [8]. We have studied the receptive field (RF) characteristics of SC neurons and, using H o f f m a n n ' s protocol [8], have analyzed their afferent visual connections. Three cats were used. They were exposed to stroboscopic illumination for 12 h / d a y at a frequency of 2/sec and a flash duration of 0.2 msec. Duration of strobe rearing was 10 months from birth. Prior to testing the cats were anesthetized with Imalgene (ketamine base, 15 m g / k g intramuscular), so as to allow a tracheal cannula and an intravenous catheter to be placed. The animal was positioned in a stereotaxic frame and paralyzed by an intravenous injection of Flaxedil (20 mg/kg) and artificially ventilated. Throughout the experiment, the animal was paralyzed with a continuous intravenous infusion of 5 m g / k g / h of Flaxedil. 'Care was taken that the cat did not suffer during the experiment. Points of contact and wounds caused by the placement of the cannula and the catheter were frequently injected with 5°70 Xylocaine. The animal was maintained between 37 and 38°C by means of a warming blanket. The lids were maintained retracted by 15°70 Neosynephrine and pupils dilated by 1% atropine. Corneas were prevented from drying by corrective corneal lenses. The skull was opened after local injection of Xylocaine, and the cortex above the SC exposed and protected by an agar film. Neurons were recorded by tungsten microelectrodes. Visual stimulation was made by means of manual displacement of dark edges and small light spots projected onto a screen, covering the visual field, placed 70 cm in front of the animal. Response to flashed diffuse lighting of the visual field was examined. By further use of a visual stimulator controlled by a P D P 8 computer, it was possible to obtain a topographical representation and a spatial histogram of the RF. This set-up enabled an exact mapping of the RF and a precise verification of its directionality to be obtained when this was considered necessary. In these experiments the directionality, ocular dominance and response to diffuse flash were tested. We have classified as direction-selective all neurons giving an increased response for movement in a particular direction. Binocularity was estimated by means of the audible response. Alternative eye stimulation allowed the neurons to be classified in one of 5 groups ranging from purely contralateral (group 1) to purely ipsilateral (group 5). Bipolar stimulation electrodes (tip exposed 1 mm, tip separation 2 ram) were placed
285
stereotaxically. A first electrode was placed in the optic chiasma (OX) (14-15 m m anterior and 1 m m lateral). A second stimulation electrode was placed in the optic tract (OT) ( 8 - 9 m m anterior and 10 m m lateral). So as to optimally place the stimulation electrodes they were initially connected to the recording equipment and the final position was determined by the optimal response to a light flash. Electrical stimuli were 50-100 /zsec pulses o f up to 15 V amplitude. Latencies of spike discharge were taken from the oscilloscope screen. A total of 110 neurons were recorded and 63 (57o70) could be driven by electrical stimulation in the OX and OT. SC neurons receiving an input from retinal W-cells responded to OX stimulation with a mean latency of 6.9 msec. With a shift of the stimulation site to the O T this latency decreased to a mean value of 4.3 msec (Fig. 1). This decrease in latency corresponds to the time required for the axon
IY
25 " A
/W
/ 20
/ /
15
OX
10
'-
E
0
15
,
,~
B
~
'
,
1
E
10
o,
/ / m
i
0
t, 2
j~ 4
l,
,
i
I
6 rflsec
8
lO
12
Fig. 1. Diagram showing the distribution of response latencies in 110 SC neurons following stimulation of O X in A and O T in B. Vertical axis: n u m b e r of units; horizontal axis: latency in msec. The input to each neuron was identified according to the latency to OX stimulation and its conduction velocity (see text). Black bars: Y-cell direct input; hatched bars: Y-cell indirect input; open bars: W-cell input. Arrows indicate mean latency values. Forty-eight neurons which did not respond to OX stimulation are not shown.
286 TABLE 1 A F F E R E N T VISUAL P A T H W A Y S TO T H E SUPERIOR C O L L I C U L U S OF STROBE-REARED, N O R M A L A N D B I N O C U L A R L Y DEPRIVED CATS Cell proportions for both groups of deprived cats differ significantly (P < 0.001, x 2 test) from the normal. Figures in brackets refer to number o f cells. Afferent pathway Y-direct input
Y-indirect input
W-direct input
Undetermined
9%
18%
73%
0%
Strobe-reared (110)
2.7%
4.5%
50%
43%
Binocularly deprived b (84)
2.0%
0%
67%
31%
Normal" (170)
aData taken from ref. 8. bData taken from ref. 10.
conductance between OX and OT, the mean value of which was approximately 4.6 m/sec. SC neurons receiving direct and indirect input from retinal Y-cells showed a mean latency difference of 0.53 msec following OX and OT stimulation which corresponds to a conduction velocity of approximately 19.5 m/sec. The Y-indirect input to SC showed much longer OT and OX latencies due to the cortical loop. In fact the mean OX and OT latencies are not very different from those of W-cell input. To differentiate between W-cell and Y-indirect input it is necessary to compare the latency in response to OX and OT stimulation. Whereas the shift in latency is large for W-cell input due to the slow conductance of W-cell axons, the shift in latency for the Y-indirect input is much shorter due to the higher conduction velocities of the Y-cell axons. This is made clear in Fig. 1 where the slope of the line connecting the mean latency for the Y-direct input is very similar to that for the Yindirect input. In Table I are shown the proportions of Y-direct, Y-indirect and Wdirect inputs for normal, strobe-reared and binocularly deprived animals. (Data for the normal cat were taken from ref. 8 and for the binocularly deprived cat from ref. 10.) We found that in the strobe-reared animal 55 cells (50%) had W-direct input, 3 cells (2.7%) had Y-direct input and 5 cells (4.5%) had Y-indirect input. Forty-eight cells could not be driven by stimulation from OX. This is statistically* different (P < 0.001) from the normal animal and shows that strobe rearing results in: (1) a severe loss of Y-direct and Y-indirect inputs to SC; (2) no change in W-direct input; and (3) a large number of neurons which cannot be driven from the OX. Concomitant with the change in visual afference was a change in RF characteristics of SC neurons in strobe reared cats (see Table II). Strobe rearing results in a drastic reduction of direction-selective units (84% in the normal animal and only 12°70 in the strobe-reared). This is accompanied by a less dramatic but nevertheless * x2-test is used for all statistical analysis in this paper.
287 T A B L E 11 T H E P R O P O R T I O N OF D I R E C T I O N SELECTIVE CELLS A N D CELLS B E L O N G I N G TO O C U L A R D O M I N A N C E G R O U P S 2, 3 A N D 4 IN N O R M A L , S T R O B E - R E A R E D A N D B I N O C U L A R L Y DEPRIVED CATS Direction-selective ceils
Binocular driven cells
Normal a
84% (87)
85°7o (54)
Strobe-reared (110)
1207o (110)
38070 (110)
Binocularly deprived b
17o70 (42)
51% (118)
aData from ref. 5. bData from ref. 10.
significant reduction in the number of neurons which can be influenced by both eyes (85% in ocular dominance groups 2, 3 and 4 in the adult and 42% in the strobereared animal). The interpretation of the effects of strobe rearing makes it necessary to distinguish between firstly the failure to develop normal adult-like neuron response characteristics due to an absence of a type of visual input (i.e. visual movement), and secondly the development of abnormal neuron response properties due to an aberrant visual input. Comparison of the effects of dark-rearing and strobe-rearing make this possible. Binocularly deprived animals have been shown by H o f f m a n n and Sherman to have impaired visual input to SC [10]. Their results are shown in Table I. Binocularly deprived animals appear very similar to strobe-reared animals in that the W-direct input to the SC appears to be spared. In their study H o f f m a n n and Sherman found an absence of SC neurons which received a Y-indirect input. There is a decrease in the proportion of cells receiving a Y-indirect input in strobe animals. However, the difference between the decrease in the proportion of cells receiving Yindirect and Y-direct inputs is not statistically significant. Animals deprived of visual experience from birth also show certain RF deficits in c o m m o n with strobereared animals. Both rearing procedures give rise to a similar decrease in direction selectivity and the proportion of SC cells in ocular dominance groups 2, 3 and 4 (see Table II). The similarity of the proportion of direction-selective neurons in both groups of animals indicates that experience of visual movement is the essential criterion for the acquisition of this RF property. Binocular deprivation of visual pattern a n d / o r movement appears to be of much less importance in the retention of a normal ocular dominance distribution. This contrasts with the well established finding that monocular deprivation results in a profound modification of the ocular dominance distribution in both the cortex and superior colliculus [9, 20]. Our results support the claim that it is the absence of movement, in both dark-reared and strobe-reared animals, that results in an absence of direction selectivity. Corticotectal cells are the last link in the Y-indirect pathway. In the normal adult, over 70% of these cells are direction-selective and binocular [8, 15]. O f the 5 neurons in the SC of the strobe animal which were found to receive a Y-indirect
288
input, only one showed selectivity for the direction of motion although 4 could be driven by both eyes. These results support the notion [7] that the absence of direction selectivity of SC neurons of strobe-reared animals reflects a cortical deficit. Selectivity to direction of movement in the cortex has been shown to be dependent on intracortical inhibition [17] and to be absent in young animals [11]. It would seem, therefore, that movement of the retinal image, resulting either from saccadic eye movements or from movement of the visual stimuli, is essential for the development of this visual cortical response property. REFERENCES 1
2 3 4 5 6 7 8 9 10 I1 12 13 14 15 16 17 18 19 20
Chalupa, L.M. and Rhoades, R.W., Modification of visual response properties in the superior colliculus of the golden hamster following stroboscopic rearing, J. Physiol. (Lond.), 274 (1978) 571-592. Cynader, M., Berman, N. and Hein, A., Cats reared in stroboscopic illumination: effects on receptive fields in visual cortex, Proc. nat. Acad. Sci. (Wash.), 70 (1973) 1353-1354. Cynader, M., Berman, N. and Hein, A., Recovery of function in cat visual cortex following prolonged deprivation, Exp. Brain Res., 25 (1976) 139-156. Cynader, M. and Chernenko, G., Abolition of direction selectivity in the visual cortex of the cat, Science, 193 (1976) 504-505. Flandrin, J.M. and Jeannerod, M., Superior colliculus: environmental influences on the development of directional responses in the kitten, Brain Res., 89 (1975) 348-352. Flandrin, J.M. and Jeannerod, M., Lack of recovery in collicular neurons from the effects of early deprivation or neonatal cortical lesion in kitten, Brain Res., 120 (1977) 362 366. Flandrin, J.M., Kennedy, H. and Amblard, B., Effects of stroboscopic rearing on the binocularity and directionality of cat superior colliculus neurons, Brain Res., 101 (1976) 576-581. Hoffmann, K.P., Conduction velocity in pathways from retina to superior colliculus in the cat: a correlation with receptive-field properties, J. Neurophysiol., 36 (1973) 409-424. Hoffmann, K.P. and Sherman, S.M., Effects of early monocular deprivation on visual inpuLto cat superior colliculus, J. Neurophysiol., 37 (1974) 1276-1286. Hoffmann, K.P. and Sherman, S.M., Effects of early binocular deprivation on visual input to cat superior colliculus, J. Neurophysiol., 38 (1975) 1049-1059. Kennedy, H., Martin, K.A.C. and Whitteridge, D., Receptive field characteristics in area 17 of adult and newborn sheep, J. Physiol. (Lond.), 300 (1980) 55P. Norton, T.T., Receptive fields properties of superior colliculus cells and development of visual behavior in kittens, J. Neurophysiol., 37 (1974) 674-690. Olson, C.R. and Pettigrew, J.D., Single units in visual cortex of kittens reared in stroboscopic illumination, Brain Res., 70 (1974) 189-204. Orban, G.A., Kennedy, H., Maes, H. and Amblard, B., Cats reared in stroboscopic illumination: velocity characteristics of area 18 neurons, Arch. ital. Biol., 116 (1978) 413-419. Palmer, L.A. and Rosenquist, A.C., Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat, Brain Res., 67 (1974) 27-42. Rosenquist, A.C. and Palmer, L.A., Visual receptive field properties of cells of the superior colliculus after cortical lesions in the cat. Exp. Neurol., 33 (1971) 629-652. Sillito, A.M., Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex, J. Physiol. (Lond.), 271 (1977) 699-720. Stein, B.E., Labos, E. and Kr~iger, L., Sequence of changes in properties of neurons of superior colliculus of the kitten during maturation, J. Neurophysiol., 36 (1973) 667-679. Wickelgren, B.G. and Sterling, P., Influence of visual cortex on receptive fields in the superior colliculus of the cat, J. Neurophysiol., 32 (1969) 16-23. Wiesel, T.N. and Hubel, D.H., Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens, J. Neurophysiol., 28 (1965) 1029-1040.