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Brief monocular visual experience and kitten cortical binocularity
Brain Research, 109 (1976) 165-168
165
© ElsevierScientificPublishingCompany,Amsterdam- Printed in The Netherlands
Brief monocular visual experience and kitten cortical binocularity
P. B. SCHECHTERANDE. H. MURPHY Department of Behavioral Sciences, Committee on Biopsychology, The University of Chicago, Chicago, Ill. 60637 (U.S.A.)
(Accepted February 19th, 1976)
In the normal adult cat, about 80 ~o of the cells in the visual cortex are responsive to visual stimuli presented to both eyes; about 10 % are monocularly driven by each eyet. This ocular dominance pattern may be changed by altering the animal's visual environment during a 'critical period' in its early life. If a cat is raised without pattern vision in one eye only (monocular pattern deprivation), nearly all of the cells in its visual cortex are monocularly driven by the experienced eye5,6. If a cat is raised with normal pattern vision in both eyes, but with a divergent strabismus such that corresponding points in visual space do not fall on corresponding retinal elements (binocular non-correspondence), nearly all cortical cells are monocular, but the ocular dominance distribution does not abnormally favor either eye2. There is some indication that monocular deprivation may cause a reduction in the percentage of binocularly driven cells before it causes a shift in ocular domina nce to favor the experienced eyea,4. In order to examine this possibility, we have examined the effects of brief periods of monocular visual experience on kitten cortical binocularity. We raised kittens in complete darkness from their 10th day of life--the approximate age at eye opening. On their 30th day, they were divided into 3-, 12- and 20-h groups. Kittens were anesthetized with a mixture of halothane (Fluothane; Ayerst), oxygen and nitrous oxide; the 3-h kittens had one eyelid sutured and were exposed to a bright visual environment for 3 h. The 12-h kittens were monocularly experienced for 4 h/day on their 30th, 31st and 32rid days of life; the 20-h kittens were monocularly experienced for 5 h/day on their 30th through 33rd days of life. Visual experience was limited to 5 h/day in order to minimize the amount of time the kittens spent sleeping. For the same reason, kittens were removed from their mothers during visual experience, were placed with older kittens during that time, and were periodically 'stimulated' by the experimenters. The kittens were returned to the dark between periods of monocular experience, and were maintained in the dark from the end of their visual experience period until electrophysiological recording. We also examined completely dark reared kittens, normal kittens, and normal kittens with one eye sutured from their 3rd day of life until several hours prior to recording. All kittens were between 42 and 48 days old at the time of recording.
166 TABLE
1
OCULAR DOMINANCE AND VISUAl. EXPERIENCE IN 7-WEEK-OLD KITTENS
Visual experience
Number o f cells
Monocular
3-h monocular 12-h monocular 20-h monocular Long-term monocular Dark-reared Normal binocular
Experienced eye
Nafve eye
20 (29 %) 33 (42 %) 33 (63 %) 25 (86 ~)
l6 (23 ~) 19 (24 ~) 4 (8 %) 1 (3 ~) 4 (9 ~) 2 (6 ~)
Binocular
Unresponsive
17 (24 ~) 13 (16 %) 1 (2 %) I (3 ~) 36 (78 ~) 26 (79 ~)
17 (24 %) 14 (18 ~) 14 (27 ~) 2 (7 %) 6 (13 ~) 5 (15 ~)
Several days prior to recording, kittens were anesthetized with an intraperitoneal (i.p.) injection of 35 mg/kg sodium pentobarbital (Nembutal; Abbott) and placed in a stereotaxic instrument. Two screws were cemented to their skulls, allowing them to be held in stereotaxic planes--with a special holder--without obstruction of the visual fields, and without the use of pressure devices. On the day of recording, the animal was again anesthetized with 35 mg/kg i.p. sodium pentobarbital. A tracheotomy was performed, and the trachea was intubated. A small area of skull over the visual cortex was removed bilaterally, the dura was reflected, and the cortex was covered with agar gel. All wounds were infiltrated with a long-lasting local anesthetic (Anucaine; Calvin Chemical). During the recording session, the animal was paralyzed with a continuous intramuscular infusion of gallamine triethiodide (Flaxedil; Davis and Geck) and artificially ventilated. End-tidal COs was continuously monitored (LB-2; Beckman Instruments) and maintained between 3.5 and 4.0 ~o- E C G was monitored, and rectal temperature was maintained between 37 and 39 °C. The animal faced a tangent screen placed 57 cm in front of its eyes. Maximal mydriasis and cycloplegia were induced with topical atropine sulfate (Atropisol 1 ~,; SMP International). The nictitating membranes were retracted with topical phenylephrine hydrochtoride (Neo-Synephrine 10 ~ ; Winthrop), and the eyes were covered with -F 1 diopter contact lenses. Additional spectacle lenses were used to focus the eyes on the tangent screen. Stimuli were projected on the back of the screen with a hand-held ophthalmoscope. Penetrations were made with varnish-insulated tungsten microelectrodes at stereotaxic coordinates L - - 2 , P--3, near the center of gaze. Extracellular action potentials were conventionally amplified, displayed on an oscilloscope, monitored over a loudspeaker, and stored on magnetic tape. Small electrolytic lesions were made at
167 100 ll
i
80
Z I&l
60
U
gg I&l O.
40 20
i j.
e: BINOCULAR
J
0
• : EXPERIENCED
o:NAIVE
, MONOCULAR
EYE
EYE
I/
VISION (HRS)
Fig. 1. Percentages of binocular (O) and monocular (n, experienced eye; O, naive eye) ceils are plotted as a function of number of hours of monocular visual experience.The '0'-h point is for darkreared kittens - - to whom it is not possible to assign a naive or experienced eye. The '400'-hour points are for kittens monocularly sutured from 3 days of age until just prior to recording.
the end of some penetrations, and cresyl violet stained serial sections were examined to verify electrode placement. A blind procedure was used, so that no kitten's visual history was known at the time of recording. We have examined the ocular dominance of 309 visual cortical units in 21 kittens. We examined other receptive field properties for some of the neurons; these results will be presented elsewhere. Most receptive fields were between 4 and 25 ° from the visual axes; receptive field eccentricity did not differ systematically among groups. In both the normal (n = 3) and dark-reared (n -- 3) kittens, about 80 ~o of the units examined were binocularly responsive (Table I). In the 3-h group (n = 5), however, only about 24 ~ of the cells were binocular; approximately equal percentages were monocularly driven by the experienced eye and by the naive eye. In the 12-h group (n -- 5) there is a further reduction in binocularity (to 16 ~o), but nearly no change in the percentage of cells monocularly driven by the naive eye. The 20-h group ( n = 3) had almost no binocularly driven cells, and showed a severe reduction in the percentage of cells driven by the naive eye only. The ocular dominance of the animals monocularly deprived from shortly after birth (n = 2) resembles that reported by other investigators for animals similarly raisedS, ~. Nearly all cells are driven by the experienced eye only. Fig. 1 presents some of these results graphically. A dramatic decrease in binocularity is found after only 3 h of monocular visual experience, and that decrease continues with increasing monocular experience, until the cortex appears to have virtually no binocular cells. The percentage of cells monocularly driven by the naive eye, on the other hand, does not appear to decrease until kittens have received 20 or more hours of monocular deprivation. The percentage of cells monocularly re-
168 sponsive to the experienced eye increases with increasing monocular experience, across all experimental groups. Our major finding is that 3 h of monocular visual experience is sufficient to cause a reduction in cortical binocularity, but is insufficient to cause a shift in ocular dominance favoring the experienced eye. It thus appears that the cortical effects of long-term monocular deprivation occur in two phases. First, there is a loss of binocularity that is similar to that seen in animals raised with binocular non-correspondence. Then, with longer periods of monocular deprivation, cortical ocular dominance begins to favor the experienced eye. It seems that the visual system responds to shortterm monocular deprivation primarily as binocular non-correspondence - - which it also is, of course. The physiological and anatomical mechanisms underlying these two phases of the long-term monocular deprivation effect are unclear; their elucidation awaits further investigation. We thank Ms. Beverly Brown for histological assistance. This work was supported by N I H Grant EY 01122 to E.H.M., and by NSF predoctoral fellowship HES 7507224 to P.B.S.
1 HUBEL,D. H., AND WIESEL, T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, J. Physiol. (Lond.), 160 (1962) 106-154. 2 HUBEL,D. H., AND WIESEL, T. N., Binocular interaction in striate cortex of kittens reared with artificial squint, J. NeurophysioL, 28 (1965) 1041-1059. 3 HUBEL,D. H., AND WIF.~EL, Z. N., The period of susceptibility to the physiological effects of urnlateral eye closure in kittens, J. Physiol. (Load.), 206 (1970) 419436. 40LSON, C. R., ANDFREEMAN,R. D., Progressive changes in kitten striate cortex during monocular vision, J. Neurophysiol., 38 (1975) 26--32. 5 WI~SEL,T. N., AND HUBEL,D. H., Single-cell responses in striate cortex of kittens deprived of vision in one eye, J. Neurophysiol., 26 (1963) 1003-1017. 6 WIESEL,T. N., ANDHUaEL,D. H., Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens, J. Neurophysiol., 28 (1965) 1029-1040.
165
© ElsevierScientificPublishingCompany,Amsterdam- Printed in The Netherlands
Brief monocular visual experience and kitten cortical binocularity
P. B. SCHECHTERANDE. H. MURPHY Department of Behavioral Sciences, Committee on Biopsychology, The University of Chicago, Chicago, Ill. 60637 (U.S.A.)
(Accepted February 19th, 1976)
In the normal adult cat, about 80 ~o of the cells in the visual cortex are responsive to visual stimuli presented to both eyes; about 10 % are monocularly driven by each eyet. This ocular dominance pattern may be changed by altering the animal's visual environment during a 'critical period' in its early life. If a cat is raised without pattern vision in one eye only (monocular pattern deprivation), nearly all of the cells in its visual cortex are monocularly driven by the experienced eye5,6. If a cat is raised with normal pattern vision in both eyes, but with a divergent strabismus such that corresponding points in visual space do not fall on corresponding retinal elements (binocular non-correspondence), nearly all cortical cells are monocular, but the ocular dominance distribution does not abnormally favor either eye2. There is some indication that monocular deprivation may cause a reduction in the percentage of binocularly driven cells before it causes a shift in ocular domina nce to favor the experienced eyea,4. In order to examine this possibility, we have examined the effects of brief periods of monocular visual experience on kitten cortical binocularity. We raised kittens in complete darkness from their 10th day of life--the approximate age at eye opening. On their 30th day, they were divided into 3-, 12- and 20-h groups. Kittens were anesthetized with a mixture of halothane (Fluothane; Ayerst), oxygen and nitrous oxide; the 3-h kittens had one eyelid sutured and were exposed to a bright visual environment for 3 h. The 12-h kittens were monocularly experienced for 4 h/day on their 30th, 31st and 32rid days of life; the 20-h kittens were monocularly experienced for 5 h/day on their 30th through 33rd days of life. Visual experience was limited to 5 h/day in order to minimize the amount of time the kittens spent sleeping. For the same reason, kittens were removed from their mothers during visual experience, were placed with older kittens during that time, and were periodically 'stimulated' by the experimenters. The kittens were returned to the dark between periods of monocular experience, and were maintained in the dark from the end of their visual experience period until electrophysiological recording. We also examined completely dark reared kittens, normal kittens, and normal kittens with one eye sutured from their 3rd day of life until several hours prior to recording. All kittens were between 42 and 48 days old at the time of recording.
166 TABLE
1
OCULAR DOMINANCE AND VISUAl. EXPERIENCE IN 7-WEEK-OLD KITTENS
Visual experience
Number o f cells
Monocular
3-h monocular 12-h monocular 20-h monocular Long-term monocular Dark-reared Normal binocular
Experienced eye
Nafve eye
20 (29 %) 33 (42 %) 33 (63 %) 25 (86 ~)
l6 (23 ~) 19 (24 ~) 4 (8 %) 1 (3 ~) 4 (9 ~) 2 (6 ~)
Binocular
Unresponsive
17 (24 ~) 13 (16 %) 1 (2 %) I (3 ~) 36 (78 ~) 26 (79 ~)
17 (24 %) 14 (18 ~) 14 (27 ~) 2 (7 %) 6 (13 ~) 5 (15 ~)
Several days prior to recording, kittens were anesthetized with an intraperitoneal (i.p.) injection of 35 mg/kg sodium pentobarbital (Nembutal; Abbott) and placed in a stereotaxic instrument. Two screws were cemented to their skulls, allowing them to be held in stereotaxic planes--with a special holder--without obstruction of the visual fields, and without the use of pressure devices. On the day of recording, the animal was again anesthetized with 35 mg/kg i.p. sodium pentobarbital. A tracheotomy was performed, and the trachea was intubated. A small area of skull over the visual cortex was removed bilaterally, the dura was reflected, and the cortex was covered with agar gel. All wounds were infiltrated with a long-lasting local anesthetic (Anucaine; Calvin Chemical). During the recording session, the animal was paralyzed with a continuous intramuscular infusion of gallamine triethiodide (Flaxedil; Davis and Geck) and artificially ventilated. End-tidal COs was continuously monitored (LB-2; Beckman Instruments) and maintained between 3.5 and 4.0 ~o- E C G was monitored, and rectal temperature was maintained between 37 and 39 °C. The animal faced a tangent screen placed 57 cm in front of its eyes. Maximal mydriasis and cycloplegia were induced with topical atropine sulfate (Atropisol 1 ~,; SMP International). The nictitating membranes were retracted with topical phenylephrine hydrochtoride (Neo-Synephrine 10 ~ ; Winthrop), and the eyes were covered with -F 1 diopter contact lenses. Additional spectacle lenses were used to focus the eyes on the tangent screen. Stimuli were projected on the back of the screen with a hand-held ophthalmoscope. Penetrations were made with varnish-insulated tungsten microelectrodes at stereotaxic coordinates L - - 2 , P--3, near the center of gaze. Extracellular action potentials were conventionally amplified, displayed on an oscilloscope, monitored over a loudspeaker, and stored on magnetic tape. Small electrolytic lesions were made at
167 100 ll
i
80
Z I&l
60
U
gg I&l O.
40 20
i j.
e: BINOCULAR
J
0
• : EXPERIENCED
o:NAIVE
, MONOCULAR
EYE
EYE
I/
VISION (HRS)
Fig. 1. Percentages of binocular (O) and monocular (n, experienced eye; O, naive eye) ceils are plotted as a function of number of hours of monocular visual experience.The '0'-h point is for darkreared kittens - - to whom it is not possible to assign a naive or experienced eye. The '400'-hour points are for kittens monocularly sutured from 3 days of age until just prior to recording.
the end of some penetrations, and cresyl violet stained serial sections were examined to verify electrode placement. A blind procedure was used, so that no kitten's visual history was known at the time of recording. We have examined the ocular dominance of 309 visual cortical units in 21 kittens. We examined other receptive field properties for some of the neurons; these results will be presented elsewhere. Most receptive fields were between 4 and 25 ° from the visual axes; receptive field eccentricity did not differ systematically among groups. In both the normal (n = 3) and dark-reared (n -- 3) kittens, about 80 ~o of the units examined were binocularly responsive (Table I). In the 3-h group (n = 5), however, only about 24 ~ of the cells were binocular; approximately equal percentages were monocularly driven by the experienced eye and by the naive eye. In the 12-h group (n -- 5) there is a further reduction in binocularity (to 16 ~o), but nearly no change in the percentage of cells monocularly driven by the naive eye. The 20-h group ( n = 3) had almost no binocularly driven cells, and showed a severe reduction in the percentage of cells driven by the naive eye only. The ocular dominance of the animals monocularly deprived from shortly after birth (n = 2) resembles that reported by other investigators for animals similarly raisedS, ~. Nearly all cells are driven by the experienced eye only. Fig. 1 presents some of these results graphically. A dramatic decrease in binocularity is found after only 3 h of monocular visual experience, and that decrease continues with increasing monocular experience, until the cortex appears to have virtually no binocular cells. The percentage of cells monocularly driven by the naive eye, on the other hand, does not appear to decrease until kittens have received 20 or more hours of monocular deprivation. The percentage of cells monocularly re-
168 sponsive to the experienced eye increases with increasing monocular experience, across all experimental groups. Our major finding is that 3 h of monocular visual experience is sufficient to cause a reduction in cortical binocularity, but is insufficient to cause a shift in ocular dominance favoring the experienced eye. It thus appears that the cortical effects of long-term monocular deprivation occur in two phases. First, there is a loss of binocularity that is similar to that seen in animals raised with binocular non-correspondence. Then, with longer periods of monocular deprivation, cortical ocular dominance begins to favor the experienced eye. It seems that the visual system responds to shortterm monocular deprivation primarily as binocular non-correspondence - - which it also is, of course. The physiological and anatomical mechanisms underlying these two phases of the long-term monocular deprivation effect are unclear; their elucidation awaits further investigation. We thank Ms. Beverly Brown for histological assistance. This work was supported by N I H Grant EY 01122 to E.H.M., and by NSF predoctoral fellowship HES 7507224 to P.B.S.
1 HUBEL,D. H., AND WIESEL, T. N., Receptive fields, binocular interaction and functional architecture in the cat's visual cortex, J. Physiol. (Lond.), 160 (1962) 106-154. 2 HUBEL,D. H., AND WIESEL, T. N., Binocular interaction in striate cortex of kittens reared with artificial squint, J. NeurophysioL, 28 (1965) 1041-1059. 3 HUBEL,D. H., AND WIF.~EL, Z. N., The period of susceptibility to the physiological effects of urnlateral eye closure in kittens, J. Physiol. (Load.), 206 (1970) 419436. 40LSON, C. R., ANDFREEMAN,R. D., Progressive changes in kitten striate cortex during monocular vision, J. Neurophysiol., 38 (1975) 26--32. 5 WI~SEL,T. N., AND HUBEL,D. H., Single-cell responses in striate cortex of kittens deprived of vision in one eye, J. Neurophysiol., 26 (1963) 1003-1017. 6 WIESEL,T. N., ANDHUaEL,D. H., Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens, J. Neurophysiol., 28 (1965) 1029-1040.