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Diminution of evoked neuronal activity in the visual cortex of pattern deprived rats
EXPERIMENTAL
Diminution Visual C. Vision
45, 42-49
NEUROLOGY
Rrseurch
(1974)
of Evoked Neuronal Activity in the Cortex of Pattern Deprived Rats SHAW,
Laboratory,
U.
YINON,
AND
E.
Hadassah University Jevusalent, Israel Received
May
AUEKBACH
Hospital
1
and Medical
School,
12,1974
The “deprived” cortex of monocularly deprived rats showed a considerable diminution in response to specific visual stimuli. Many neurons (57.7%) in the “deprived” cortex did not respond to any visual stimuli, and 29% reacted nonspecifically to any stimulus anywhere in the visual field t indefinite cells). In comparison, 7.4% neurons in the “nondeprived” cortex were not responsive to visual stimuli and 41.3% gave indefinite response. In the “normal” cortex 51.1% of the cells were motion, orientation, or direction selective while the number for the “deprived” cortex was 13.3%. Spontaneous activity of the “deprived” cells was of the same rate and pattern as was that of the “normal” cells. Receptive field properties of cells from the “deprived” cortex that were responsive, were similar to those of cells from the “normal” cortex. They were large and showed pure “on” “off” or “on-off” regions: others were of the complex type with mixed response regions. All responded optimally to moving stimuli.
INTRODUCTION Monocular deprivation of pattern vision has been shown to alter cell response properties in the cat, particularly the binocularity of cortical neurons (14. 19, 31-33). Behavior is also affected in cats (4, 5, 25) and in monkeys (24). Psychophysical correlates have been reported for visually deprived humans (13, 21). No physiological effect seems to occur after various types of visual deprivation in the rabbit, (3, 22). In contrast, monocular deprivation in the rat results in altered cortical structures (G-10, 12) and lowered amplitudes of visual evoked potentials in the cortex contralateral to the deprived 1 Supported by Stiftung Shaw’s present address is: Jerusalem, Israel.
Copyright All rights
Volkswagenwerk under Department of Zoology,
0 1974 by Academic Press, Inc. of reproduction in any form reserved
contract Hebrew
number University
11 1538. Mr. of Jerusalem,
VISUAL
CORTEX
43
eye (34 j The current paper reports on the effects of monncular deprivation on the rat visual cortex studied at the single unit level. Nest neurons of the visual cortex are binocularly innervated in the cat. It was therefore, suggested that the deprivation effect found in the cat lateral geniculate nucleus and visual cortex depends upon competition of inputs from the two eyes (17. 32). The rats in contrast, has almost complete decussation of optic nerve fibers (20 ) which allows each cortex to be studied in relative isolation; thus, we were also able to examine the effect of visual deprivation in the absence of the suggested binocular competition.
METHODS Sixteen monocularly deprived and sixteen normal adult rats were used; the normal rats were usually littermates of the deprived rats. Visual deprivation was carried out by suturing the eyelids for 4.5-405 days. Only those animals whose deprived eyes remained fully closed were used. Eyelid suturing reduces light intensity at the cat retina by 4-5 log units (31) and depends partially on light absorption in fur and skin pigments. In albino rats, light absorption is probably less affected at the deprived retinae in comparison to pigmented animals. Development and behavior of the deprived pups, however, seemed normal in all respects. All animals were housed in standard cages (15 x 25 X 35 cm ) screened only at the top. Artificial lighting was diurnal (approximately 14 hr/day) and the maximum light intensity in the cage ranged from 2-8 it-c. This intensity is well below the level of illumination which causes damage of the albino rats’ photoreceptors ( 11, 15, 16). Single unit recordings from the visual cortex were only made after at least partial recovery had occurred in the deprived eye after eye opening as measured by the electroretinogram (36). In most experiments the animals could be kept in good condition for two days. Details on preparation of the animals. including anesthesia (urethane) and surgical procedures as well as animal maintenance during- the experiments have heen described (26. 27, 36). Stainless steel microelectrodes were used. A penetration was made first in one cortex and then in a corresponding position of the other cortex. This allowed the “normal” cortex to serve as a control for the “deprived” cortex. Special considerations of unit recording, analysis, and stimulation (moving or stationary stimuli) were described previously (26, 27). The data were analyzed using poststimulus time histograms and time interval histograms.
44
SHAW,
YINON
AND
AUERBACII
RESULTS Assuming a negligible amount of transfer of impulses through commissural connections and based on the very small number of ipsilateral optic nerve fibers in the rat we consider the hemisphere contralateral to the deprived eye as the “deprived” hemisphere and the other one as the “normal” hemisphere. In the present study we gave data for 104 neurons of the “normal” visual cortex and 45 neurons of the “deprived” cortex that were tested sufficiently to be classified. All cells were driven only by the contralateral eye. The physiological distribution of all units is very similar to that obtained at the posterior side of cortical area 17 of the rat by Yinon and Auerbach (34)) recording the visual evoked potential. Cells of the “deprived” cortex were found at locations and depths in visual cortex essentially identical to those of the “normal” cortex (Fig. 1). It therefore, seems likely that no changes had occurred in the physiological mapping of the visual cortex anatomically connected with the deprived eye. However, fewer cells were cortex although recordings from corresponding found in the “deprived” points in both cortices were equally attempted. This is likely a result of the cortex in addition generally lower evoked visual activity in the “deprived” to the generally low spontaneous rate of most cells.
,’
lombdo
. +4
Normal
Imm
Deprfved
FIG. 1. Locations from which unit activity was recorded from the visual 17, 18, 18a and 36) of the rat (Yinon and Auerbach, 1973). More than found at many points. Position of all cells were computed to a standard their relation to bregma and lambda; the standard map was determined rats.
cortex areas one cell was based upon with normal
VISUAL
FIG. 1. Distrihution of receptive field and 45 neurons of “deprived” cortices “normal” cortices of deprived rats and
CORTEX
45
properties of 104 neurons of “normal” cortices of the rat. Normal cells were pooled from normal control rats.
Most neurons in the “normal” cortex (,area 17 and 18) of rats could be mapped with moving and stationary stimuli. They were classified as motion (37% ). orientation (11%). or direction (47c) selective and indefinite cells (41%‘) (35). The population of cells of the “deprived” cortex! however, showed a very considerable diminution in the response to specific visual stimuli including information on motion, orientation and direction of the image. The number of cells in the “deprived” cortex activated by these parameters of the stimulus was too small to see relationships within groups, in comparison with cells from the “normal” cortex. This is shown by the distribution of cell types in the “deprived” cortex compared to the “normal” cortex (Fig. 2). The lack of visual response of 57.7% of neurons in the “deprived” cortex (7.4% in the “normal” cortex j is strengthened by the fact that 29$’ of those which reacted were of the indefinite type, i.e., they showed no specificity regarding their response to stationary or moving stimuli. Similar results were obtained also in deprived cats ( 14, 32). Therefore, it is readily apparent that a major change has occurred as a result of pattern deprivation. Pure “on”, “off” or “on-off” receptive fields were found for some “normal” neurons ; others were of the complex type with mixed response regions in the receptive field (26). Furthermore, receptive field sizes were usually quite large for cells of the “normal” cortex; range of the major receptive field axes for the most common class of cells-motion selectivewas 15” to SO”. This is expected considering their sizes for retinal ganglion and lateral geniculate nucleus cells found in the rat by other investigators (2, 23). Keceptive field sizes and organization of responsive cells from the “deprived” cortex were similar to those of “normal” cells. Spontaneous activity was analyzed for most “deprived” cells and compared to the spontaneous activity of “normal” cells. Kate of firing for both groups was quite low and very similar: mean intervals and patterns of firing were also nearly equal for both groups (Fig. 3). From this we may
46
SHAW,
YINON
AND
AUERBACH
FIG. 3. Spontaneous activity of units from “normal” and “deprived” visual cortices of the rat. A. Mean rate of firing (spikes/set) . “Normal” cortex : 76 units ; “Deprived” cortex : 48 units. B. Mean interval of firing (set). “Normal” cortex : 46 units; “Deprived” cortex : 23 units.
assume that the results seen are not due to neuronal degeneration but probably due to an alteration in synaptic input from lower levels to cortical cells. DISCUSSION The diminution of neuronal activity reported here is consistent with the previous
electrophysiological
data on effects of pattern
deprivation
in the
rat visual cortex (34). Similarly, the present findings confirm results obtained with monocularly deprived cats (31, 32) in which a significant decrease of unit activation through the deprived eye was found, Recent work has shown that our findings in the visual cortex cannot be attributed to permanent retinal dysfunction (36). Similarly, it was shown that the responseproperties of retinal ganglion cells are not affected by deprivation (28). Whether the cortical changes obtained are due to changes in the lateral geniculate nucleus is not yet known. Apparently, the major effect of monocular pattern deprivation is to alter the synaptic
organization
of cortical
cells.
Studies
with
the cat have
sug-
VISUAL
CORTEX
4i
gested that competition occurs between afferents of each eye for synaptic sites on cortical neurons (17, 32). According to this scheme, neurons are innervated only by afferents from the nondeprived eye while most of the afferents from the deprived eye fail to function, resulting in monocular dominance. Such a scheme is not likely for the rat because of the relative isolation of each hemisphere and the almost complete crossing of the optic tracts, IVith almost no afferent input from the nondeprived eye to take over in the “deprived” hemisphere, most cells of the “deprived” cortex simply become nonfunctional for visual stimuli, although having apparently normal maintained activity. This shows that competition between inputs is not a necessary condition for the deprivation effect to take place. If our findings had been the result of neural degeneration a total absence of visual activity would have to be expected in the “deprived” hemisphere. However, the spontaneous activity obtained in our experiments and the response to visual stimuli of regular and indefinite cells was clearly demonstrable. In comparison, enucleation of the eye in the rat after birth leads to degeneration of optic nerve fibers and higher levels (30) within periods much shorter than those used by us for deprivation in the present study. This is supported by the experiment of Terry ct al. (29) who compared the effects of unilateral enucleation and deprivation in the mouse; they found extensive degeneration of the visual pathways in enucleation and no However, from Fifkova’s studies demonstrable change with deprivation. (7-9, 12) it is known that changes take place in deprived rats at the synaptic level. The results indicate that plasticity takes place as seen in cells which are influenced by deprivation during development. IVhether the plastic cells can recover function after ending deprivation in the rat is unknown. In the cat there is evidence that some recovery occurs ( 19. 33). Furthermore, whether neuronal plasticity in the rat can have as wide a range of adaptability to different selective deprivations, as they do in the cat (‘1, 18) has not been resolved. The relatively nonspecific response properties of cortical neurons of the normal rat (26, 35) make it unlikely that such wide plasticity is possible. REFERENCES 1. BLAKEMORE, C., and G. F. COOPEIL 1970. Development of the brain depends on the visual environment. Nature 228 : 477-478. 3. BROWN, J. E., and J. A. ROJAS. 196.5. Rat retinal ganglion cells receptive field organization and maintained activity. J. Newopltysiol. 28 : 1073-1090. 3. CHOW, K. L., and P. D. SPEAR. 1974. Morphological and functional effects of visual deprivation on the rabbit visual system. E.rp. Sezlvol. 42 : 429-447. 4. CHOW, K. L., and II. L. STEWART. 1972. Reversal of structure and functional effects of long-term visual deprivation in cats. Err. Sfrrsot. 34: 409-431.
48
SHAW,
YINON
AND
AUERBACH
5. DEWS, P. B., and T. N. WIESEL. 1970. Consequences of monocular deprivation on visual behavior in kittens. J. Physiol. 206: 431-455. 6. FIFKOVA, E. 1967. The influence of unilateral visual deprivation on optic centers, Brain.
Res. 6, 763-766.
7. FIFKOVA, E. 1968. Changes in the visual cortex of rats after unilateral Nature
deprivation.
220 : 379-380.
8. FIFKOVA, E. 1970. Changes of axosomatic synpases in the visual cortex of monocularly deprived rats. J. Neurobiol. 2 : 61-71. 9. FIFKOV& E. 1970. The effects of monocular deprivation on the synaptic contacts of the visual cortex. J. Neurobiol. 3: 285-294. 10. FIFKOV~, E. 1970. The effects of unilateral deprivation on visual centers in rats. J. Comp. Neural. 140 : 431-438. 11. FIFI~OV~, E. 1972. Effects of light and visual deprivation on the retina. Exp. Newel. 35 : 450-457. 12. FIFKOV~, E., and R. HASSLER. 1969. Quantitative morphological changes in visual centers in rats after unilateral deprivation. J. Comp. Neurol. 135: 167-178. 13. FREEMAN, R. D., and L. N. THIBOS. 1973. Electrophysiological evidence that abnormal early visual experience can modify the human brain. Science 180: 876-878. 14. GANZ, L., M. FITCH, and J. A. SATTERBERG. 1968. The selective effect of visual deprivation on receptive field shape determined neurophysiologically. Exp. Neural. 22 : 614-637. 15. GORN, R. A. and T. KUWABARA. 1967. Retinal damage by visual light. Arch. Ophthal. 77 : 115-118. 16. GRIGNOLA, A., N. ORZALUSE, R. CASTELLOZZO, and P. VITTONE. 1969. Retinal damage by visible light in albino rats: An electron microscope study. Opthalmologia.
157 : 43-59.
17. GUILLERY, R. W., 1973. The effect of lid suture upon the growth of cells in the dorsal lateral geniculate nucleus of kittens. J. Camp. Nezrrol. 148: 417-422. 18. HIRSCH, H. V. B., and D. N. SPINELLI. 1971. Modification of the distribution of receptive field orientation in cats by selective visual exposure during development. Exp. Brain Res. 13: 509-527. 19. HUBEL, D. H., and T. N. WIESEL. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206: 419-436. 20. LUND, R. D. (1965). Uncrossed visual pathways of hooded and albino rats. Science 149 : 1506-1507. 21. MITCHELL, D. E., R. D. FREEMAN, M. MILLODOT, and G. HAEGERSTROM. 1973. Meridional amblyopia: Evidence for modification of the human visual system by early visual experience. Vision Rcs. 13 : 535-558. 22. MIZE, R. R. and E. H. MURPHEY. 1973. Selective visual experience fails to modify receptive field properties of rabbit striate cortex. Srience 180: 320-323. 23. MONTERO, V. M., J. F. BRUGGE, and R. E. BEITEL. 1968. Relation of the visual field to the lateral geniculate body of the albino rat. J. Neurophysiol. 31 : 221256. 24. VON NOOFCDEN, G. K., J. E. DOWLING, and D. C. FERGUSON. 1970. Experimental amblyopia in monkeys. I. Behavioral studies of stimulus deprivation amblyopia. Arch. Ophthal. 84 : 206214. 25. RIZZOLATTI, G., and V. TRADARDI. 1971. Pattern discrimination in monocularly reared cats. Exp. Neural. 33 : 181-194. 26. SHAW, C., U. YINON, and E. AUERBACH. 1974. Receptive fields and response propertiesof neurons in the rat visual cortex. Vision Res. In press.
VISUAL 27.
SHAW,
cortex. -38.
30. 31. 32.
33. 34. 35.
36.
I:isiojl S. M., deprived
and E. AUEKBACH.
1974. Single
unit
activity
in the rat visual
Rrs. 14: 311-313.
and J. STONE. 1973. Physiological normality of the retina in cats. Bra&L Rrs. 60: 224230. TEKHY. R. J., A. L. ROLAND, and J. RACE. 1962. Effect of eye enucleation and eyelid closure upon the brain and associated visual structures in the mouse. I. A report on degenerative changes. J. Exp. Zool. 150: 165-183. TSANG, Y. 1937. Visual centers in blinded rats. J. Cor~zp. Nrztrol. 66: 211-261. WIESEL, T. N., and I). H. HUBEL. 1963. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. ~Vcr~voplzj’siol. 26 : 1003-1017. WIESEL, T. N., and D. H. HUBEL. 19685. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. h’c~~ropl~ysiol. 28 : 1029-1040. WIESEL. T. N., and D. H. HUBEL. 1965. Extent of recovery from the effects of visual deprivation in kittens. J. Nczrro~lzysiol. 28 : 1061-1072. YINON, U., and E. AUERBACH. 1973. Deprivation of pattern vision studied by visual evoked potentials in the rat cortex. Exp. h’rurol. 38: 231-2.51. YINOS, U., C. SHAW, E. AI-ERBACH. 1974. Retinal and cortical changes in the visual system of pattern deprived rats. ZIL “Sensory Physiology and Behavior,” “Oholo” 19th -4nn. Biol. Conference, Ma’alot, Israel. 1974. YINOK, U., C. SHAW, and E. AUERBACII. 1974. Transitional changes during stimulation in the electroretinogram of visually deprived rats. Exp. Xczwol. 43: 479-486. SHERMAN,
visually
29.
C.. U. YINON,
49
CORTEX
Diminution Visual C. Vision
45, 42-49
NEUROLOGY
Rrseurch
(1974)
of Evoked Neuronal Activity in the Cortex of Pattern Deprived Rats SHAW,
Laboratory,
U.
YINON,
AND
E.
Hadassah University Jevusalent, Israel Received
May
AUEKBACH
Hospital
1
and Medical
School,
12,1974
The “deprived” cortex of monocularly deprived rats showed a considerable diminution in response to specific visual stimuli. Many neurons (57.7%) in the “deprived” cortex did not respond to any visual stimuli, and 29% reacted nonspecifically to any stimulus anywhere in the visual field t indefinite cells). In comparison, 7.4% neurons in the “nondeprived” cortex were not responsive to visual stimuli and 41.3% gave indefinite response. In the “normal” cortex 51.1% of the cells were motion, orientation, or direction selective while the number for the “deprived” cortex was 13.3%. Spontaneous activity of the “deprived” cells was of the same rate and pattern as was that of the “normal” cells. Receptive field properties of cells from the “deprived” cortex that were responsive, were similar to those of cells from the “normal” cortex. They were large and showed pure “on” “off” or “on-off” regions: others were of the complex type with mixed response regions. All responded optimally to moving stimuli.
INTRODUCTION Monocular deprivation of pattern vision has been shown to alter cell response properties in the cat, particularly the binocularity of cortical neurons (14. 19, 31-33). Behavior is also affected in cats (4, 5, 25) and in monkeys (24). Psychophysical correlates have been reported for visually deprived humans (13, 21). No physiological effect seems to occur after various types of visual deprivation in the rabbit, (3, 22). In contrast, monocular deprivation in the rat results in altered cortical structures (G-10, 12) and lowered amplitudes of visual evoked potentials in the cortex contralateral to the deprived 1 Supported by Stiftung Shaw’s present address is: Jerusalem, Israel.
Copyright All rights
Volkswagenwerk under Department of Zoology,
0 1974 by Academic Press, Inc. of reproduction in any form reserved
contract Hebrew
number University
11 1538. Mr. of Jerusalem,
VISUAL
CORTEX
43
eye (34 j The current paper reports on the effects of monncular deprivation on the rat visual cortex studied at the single unit level. Nest neurons of the visual cortex are binocularly innervated in the cat. It was therefore, suggested that the deprivation effect found in the cat lateral geniculate nucleus and visual cortex depends upon competition of inputs from the two eyes (17. 32). The rats in contrast, has almost complete decussation of optic nerve fibers (20 ) which allows each cortex to be studied in relative isolation; thus, we were also able to examine the effect of visual deprivation in the absence of the suggested binocular competition.
METHODS Sixteen monocularly deprived and sixteen normal adult rats were used; the normal rats were usually littermates of the deprived rats. Visual deprivation was carried out by suturing the eyelids for 4.5-405 days. Only those animals whose deprived eyes remained fully closed were used. Eyelid suturing reduces light intensity at the cat retina by 4-5 log units (31) and depends partially on light absorption in fur and skin pigments. In albino rats, light absorption is probably less affected at the deprived retinae in comparison to pigmented animals. Development and behavior of the deprived pups, however, seemed normal in all respects. All animals were housed in standard cages (15 x 25 X 35 cm ) screened only at the top. Artificial lighting was diurnal (approximately 14 hr/day) and the maximum light intensity in the cage ranged from 2-8 it-c. This intensity is well below the level of illumination which causes damage of the albino rats’ photoreceptors ( 11, 15, 16). Single unit recordings from the visual cortex were only made after at least partial recovery had occurred in the deprived eye after eye opening as measured by the electroretinogram (36). In most experiments the animals could be kept in good condition for two days. Details on preparation of the animals. including anesthesia (urethane) and surgical procedures as well as animal maintenance during- the experiments have heen described (26. 27, 36). Stainless steel microelectrodes were used. A penetration was made first in one cortex and then in a corresponding position of the other cortex. This allowed the “normal” cortex to serve as a control for the “deprived” cortex. Special considerations of unit recording, analysis, and stimulation (moving or stationary stimuli) were described previously (26, 27). The data were analyzed using poststimulus time histograms and time interval histograms.
44
SHAW,
YINON
AND
AUERBACII
RESULTS Assuming a negligible amount of transfer of impulses through commissural connections and based on the very small number of ipsilateral optic nerve fibers in the rat we consider the hemisphere contralateral to the deprived eye as the “deprived” hemisphere and the other one as the “normal” hemisphere. In the present study we gave data for 104 neurons of the “normal” visual cortex and 45 neurons of the “deprived” cortex that were tested sufficiently to be classified. All cells were driven only by the contralateral eye. The physiological distribution of all units is very similar to that obtained at the posterior side of cortical area 17 of the rat by Yinon and Auerbach (34)) recording the visual evoked potential. Cells of the “deprived” cortex were found at locations and depths in visual cortex essentially identical to those of the “normal” cortex (Fig. 1). It therefore, seems likely that no changes had occurred in the physiological mapping of the visual cortex anatomically connected with the deprived eye. However, fewer cells were cortex although recordings from corresponding found in the “deprived” points in both cortices were equally attempted. This is likely a result of the cortex in addition generally lower evoked visual activity in the “deprived” to the generally low spontaneous rate of most cells.
,’
lombdo
. +4
Normal
Imm
Deprfved
FIG. 1. Locations from which unit activity was recorded from the visual 17, 18, 18a and 36) of the rat (Yinon and Auerbach, 1973). More than found at many points. Position of all cells were computed to a standard their relation to bregma and lambda; the standard map was determined rats.
cortex areas one cell was based upon with normal
VISUAL
FIG. 1. Distrihution of receptive field and 45 neurons of “deprived” cortices “normal” cortices of deprived rats and
CORTEX
45
properties of 104 neurons of “normal” cortices of the rat. Normal cells were pooled from normal control rats.
Most neurons in the “normal” cortex (,area 17 and 18) of rats could be mapped with moving and stationary stimuli. They were classified as motion (37% ). orientation (11%). or direction (47c) selective and indefinite cells (41%‘) (35). The population of cells of the “deprived” cortex! however, showed a very considerable diminution in the response to specific visual stimuli including information on motion, orientation and direction of the image. The number of cells in the “deprived” cortex activated by these parameters of the stimulus was too small to see relationships within groups, in comparison with cells from the “normal” cortex. This is shown by the distribution of cell types in the “deprived” cortex compared to the “normal” cortex (Fig. 2). The lack of visual response of 57.7% of neurons in the “deprived” cortex (7.4% in the “normal” cortex j is strengthened by the fact that 29$’ of those which reacted were of the indefinite type, i.e., they showed no specificity regarding their response to stationary or moving stimuli. Similar results were obtained also in deprived cats ( 14, 32). Therefore, it is readily apparent that a major change has occurred as a result of pattern deprivation. Pure “on”, “off” or “on-off” receptive fields were found for some “normal” neurons ; others were of the complex type with mixed response regions in the receptive field (26). Furthermore, receptive field sizes were usually quite large for cells of the “normal” cortex; range of the major receptive field axes for the most common class of cells-motion selectivewas 15” to SO”. This is expected considering their sizes for retinal ganglion and lateral geniculate nucleus cells found in the rat by other investigators (2, 23). Keceptive field sizes and organization of responsive cells from the “deprived” cortex were similar to those of “normal” cells. Spontaneous activity was analyzed for most “deprived” cells and compared to the spontaneous activity of “normal” cells. Kate of firing for both groups was quite low and very similar: mean intervals and patterns of firing were also nearly equal for both groups (Fig. 3). From this we may
46
SHAW,
YINON
AND
AUERBACH
FIG. 3. Spontaneous activity of units from “normal” and “deprived” visual cortices of the rat. A. Mean rate of firing (spikes/set) . “Normal” cortex : 76 units ; “Deprived” cortex : 48 units. B. Mean interval of firing (set). “Normal” cortex : 46 units; “Deprived” cortex : 23 units.
assume that the results seen are not due to neuronal degeneration but probably due to an alteration in synaptic input from lower levels to cortical cells. DISCUSSION The diminution of neuronal activity reported here is consistent with the previous
electrophysiological
data on effects of pattern
deprivation
in the
rat visual cortex (34). Similarly, the present findings confirm results obtained with monocularly deprived cats (31, 32) in which a significant decrease of unit activation through the deprived eye was found, Recent work has shown that our findings in the visual cortex cannot be attributed to permanent retinal dysfunction (36). Similarly, it was shown that the responseproperties of retinal ganglion cells are not affected by deprivation (28). Whether the cortical changes obtained are due to changes in the lateral geniculate nucleus is not yet known. Apparently, the major effect of monocular pattern deprivation is to alter the synaptic
organization
of cortical
cells.
Studies
with
the cat have
sug-
VISUAL
CORTEX
4i
gested that competition occurs between afferents of each eye for synaptic sites on cortical neurons (17, 32). According to this scheme, neurons are innervated only by afferents from the nondeprived eye while most of the afferents from the deprived eye fail to function, resulting in monocular dominance. Such a scheme is not likely for the rat because of the relative isolation of each hemisphere and the almost complete crossing of the optic tracts, IVith almost no afferent input from the nondeprived eye to take over in the “deprived” hemisphere, most cells of the “deprived” cortex simply become nonfunctional for visual stimuli, although having apparently normal maintained activity. This shows that competition between inputs is not a necessary condition for the deprivation effect to take place. If our findings had been the result of neural degeneration a total absence of visual activity would have to be expected in the “deprived” hemisphere. However, the spontaneous activity obtained in our experiments and the response to visual stimuli of regular and indefinite cells was clearly demonstrable. In comparison, enucleation of the eye in the rat after birth leads to degeneration of optic nerve fibers and higher levels (30) within periods much shorter than those used by us for deprivation in the present study. This is supported by the experiment of Terry ct al. (29) who compared the effects of unilateral enucleation and deprivation in the mouse; they found extensive degeneration of the visual pathways in enucleation and no However, from Fifkova’s studies demonstrable change with deprivation. (7-9, 12) it is known that changes take place in deprived rats at the synaptic level. The results indicate that plasticity takes place as seen in cells which are influenced by deprivation during development. IVhether the plastic cells can recover function after ending deprivation in the rat is unknown. In the cat there is evidence that some recovery occurs ( 19. 33). Furthermore, whether neuronal plasticity in the rat can have as wide a range of adaptability to different selective deprivations, as they do in the cat (‘1, 18) has not been resolved. The relatively nonspecific response properties of cortical neurons of the normal rat (26, 35) make it unlikely that such wide plasticity is possible. REFERENCES 1. BLAKEMORE, C., and G. F. COOPEIL 1970. Development of the brain depends on the visual environment. Nature 228 : 477-478. 3. BROWN, J. E., and J. A. ROJAS. 196.5. Rat retinal ganglion cells receptive field organization and maintained activity. J. Newopltysiol. 28 : 1073-1090. 3. CHOW, K. L., and P. D. SPEAR. 1974. Morphological and functional effects of visual deprivation on the rabbit visual system. E.rp. Sezlvol. 42 : 429-447. 4. CHOW, K. L., and II. L. STEWART. 1972. Reversal of structure and functional effects of long-term visual deprivation in cats. Err. Sfrrsot. 34: 409-431.
48
SHAW,
YINON
AND
AUERBACH
5. DEWS, P. B., and T. N. WIESEL. 1970. Consequences of monocular deprivation on visual behavior in kittens. J. Physiol. 206: 431-455. 6. FIFKOVA, E. 1967. The influence of unilateral visual deprivation on optic centers, Brain.
Res. 6, 763-766.
7. FIFKOVA, E. 1968. Changes in the visual cortex of rats after unilateral Nature
deprivation.
220 : 379-380.
8. FIFKOVA, E. 1970. Changes of axosomatic synpases in the visual cortex of monocularly deprived rats. J. Neurobiol. 2 : 61-71. 9. FIFKOV& E. 1970. The effects of monocular deprivation on the synaptic contacts of the visual cortex. J. Neurobiol. 3: 285-294. 10. FIFKOV~, E. 1970. The effects of unilateral deprivation on visual centers in rats. J. Comp. Neural. 140 : 431-438. 11. FIFI~OV~, E. 1972. Effects of light and visual deprivation on the retina. Exp. Newel. 35 : 450-457. 12. FIFKOV~, E., and R. HASSLER. 1969. Quantitative morphological changes in visual centers in rats after unilateral deprivation. J. Comp. Neurol. 135: 167-178. 13. FREEMAN, R. D., and L. N. THIBOS. 1973. Electrophysiological evidence that abnormal early visual experience can modify the human brain. Science 180: 876-878. 14. GANZ, L., M. FITCH, and J. A. SATTERBERG. 1968. The selective effect of visual deprivation on receptive field shape determined neurophysiologically. Exp. Neural. 22 : 614-637. 15. GORN, R. A. and T. KUWABARA. 1967. Retinal damage by visual light. Arch. Ophthal. 77 : 115-118. 16. GRIGNOLA, A., N. ORZALUSE, R. CASTELLOZZO, and P. VITTONE. 1969. Retinal damage by visible light in albino rats: An electron microscope study. Opthalmologia.
157 : 43-59.
17. GUILLERY, R. W., 1973. The effect of lid suture upon the growth of cells in the dorsal lateral geniculate nucleus of kittens. J. Camp. Nezrrol. 148: 417-422. 18. HIRSCH, H. V. B., and D. N. SPINELLI. 1971. Modification of the distribution of receptive field orientation in cats by selective visual exposure during development. Exp. Brain Res. 13: 509-527. 19. HUBEL, D. H., and T. N. WIESEL. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206: 419-436. 20. LUND, R. D. (1965). Uncrossed visual pathways of hooded and albino rats. Science 149 : 1506-1507. 21. MITCHELL, D. E., R. D. FREEMAN, M. MILLODOT, and G. HAEGERSTROM. 1973. Meridional amblyopia: Evidence for modification of the human visual system by early visual experience. Vision Rcs. 13 : 535-558. 22. MIZE, R. R. and E. H. MURPHEY. 1973. Selective visual experience fails to modify receptive field properties of rabbit striate cortex. Srience 180: 320-323. 23. MONTERO, V. M., J. F. BRUGGE, and R. E. BEITEL. 1968. Relation of the visual field to the lateral geniculate body of the albino rat. J. Neurophysiol. 31 : 221256. 24. VON NOOFCDEN, G. K., J. E. DOWLING, and D. C. FERGUSON. 1970. Experimental amblyopia in monkeys. I. Behavioral studies of stimulus deprivation amblyopia. Arch. Ophthal. 84 : 206214. 25. RIZZOLATTI, G., and V. TRADARDI. 1971. Pattern discrimination in monocularly reared cats. Exp. Neural. 33 : 181-194. 26. SHAW, C., U. YINON, and E. AUERBACH. 1974. Receptive fields and response propertiesof neurons in the rat visual cortex. Vision Res. In press.
VISUAL 27.
SHAW,
cortex. -38.
30. 31. 32.
33. 34. 35.
36.
I:isiojl S. M., deprived
and E. AUEKBACH.
1974. Single
unit
activity
in the rat visual
Rrs. 14: 311-313.
and J. STONE. 1973. Physiological normality of the retina in cats. Bra&L Rrs. 60: 224230. TEKHY. R. J., A. L. ROLAND, and J. RACE. 1962. Effect of eye enucleation and eyelid closure upon the brain and associated visual structures in the mouse. I. A report on degenerative changes. J. Exp. Zool. 150: 165-183. TSANG, Y. 1937. Visual centers in blinded rats. J. Cor~zp. Nrztrol. 66: 211-261. WIESEL, T. N., and I). H. HUBEL. 1963. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. ~Vcr~voplzj’siol. 26 : 1003-1017. WIESEL, T. N., and D. H. HUBEL. 19685. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. h’c~~ropl~ysiol. 28 : 1029-1040. WIESEL. T. N., and D. H. HUBEL. 1965. Extent of recovery from the effects of visual deprivation in kittens. J. Nczrro~lzysiol. 28 : 1061-1072. YINON, U., and E. AUERBACH. 1973. Deprivation of pattern vision studied by visual evoked potentials in the rat cortex. Exp. h’rurol. 38: 231-2.51. YINOS, U., C. SHAW, E. AI-ERBACH. 1974. Retinal and cortical changes in the visual system of pattern deprived rats. ZIL “Sensory Physiology and Behavior,” “Oholo” 19th -4nn. Biol. Conference, Ma’alot, Israel. 1974. YINOK, U., C. SHAW, and E. AUERBACII. 1974. Transitional changes during stimulation in the electroretinogram of visually deprived rats. Exp. Xczwol. 43: 479-486. SHERMAN,
visually
29.
C.. U. YINON,
49
CORTEX