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Squint affects striate cortex cells encoding horizontal image movements
182
Brain Research, 170 (1979) 182-186 ;© Elsevier/North-Holland Biomedical Press
Squint affects striate cortex cells encoding horizontal image movements
w. SINGER, J. RAUSCHECKER and M. von GRUENAU Max-Planck-lnstitut fiir Psych iatrie, Kraepelinstr. 2, 8000 Miinchen 40 ( G. F. R.)
(Accepted March 8th, 1979)
The incongruency between retinal coordinates and other sensory-motor maps, such as results from surgical eye rotation, causes a drastic reduction of light reactive cells in striate cortex of developing and mature cats 4. It has been concluded from these observations that a substantial fraction of neurons in primary visual cortex subserve specific functions in visuomotor and polymodal processing. With 180° inversion of the retinal coordinates there was in addition a selective loss of binocular cells preferring vertical stimulus orientations 5. Since these neurons encode preferentially image displacements with a prominent horizontal vector, it was suggested that they might be involved in the coordination of horizontal eye movements. In this context vergence movements were thought to be of particular interest since they occur only in the horizontal plane and since their coordination is likely to require binocular cells sensitive to horizontal image displacements. These considerations led to the hypothesis that squint also might lead to a reduction of cells with vertically oriented receptive fields since it disturbs binocular fusion and concomitant vergence movements. To test this hypothesis data were evaluated from two independent series of experiments in which squinting cats had been examined for other purposes. Thus, by the time of data acquisition, none of the experimenters knew about the working hypothesis of the present investigation. Data were taken from 6 squinting kittens. In two animals asymmetrical divergent squint had been induced by section of the medial rectus muscle of the right eye. In the remaining 4 kittens squint had been induced symmetrically: two of them had the lateral recti of both eyes cut (symmetrical convergent squint) and in the other two, the medial recti were severed (symmetrical divergent squint). All animals had been operated on when 28 days old. Until the operation they had been kept in complete darkness, thereafter they were raised in normal animal house environment. Survival time until the electrophysiological experiment varied between 5 and 11 months. Preparation and recording techniques for the analysis of cortical receptive fields were conventional and identical to those routinely applied in this laboratory ~. Single units were recorded extracellularly from striate cortex of both hemispheres with potassium citrate-filled micropipettes. During penetration, a weak positive c-urrent (2-5 hA) was applied through the pipette to activate cells lacking spontaneous activity.
183 Receptive fields were plotted with hand-held stimuli. In all cases where this procedure failed to yield clear characterization of ocular dominance and preferred orientation, response histograms were compiled after stimulation with an electromechanical light stimulator. To reduce the sampling bias imposed by the columnar organization of striate cortex, electrode penetrations were directed with an inclination of 30° to the cortical surface from posterior to anterior. In addition to common receptive field parameters (ocular dominance, orientation preference and tuning, direction selectivity, field size, velocity preference) the vigour of responses to optimally aligned stimuli was estimated and rated in a subjective scale of 5 classes. In the cats with asymmetrical squint, 93 % of 71 analyzed cells could be driven with light stimuli. In the animals with symmetrical squint the percentage of lightreactive cells was slightly less (convergent: 84% of 143 cells; divergent: 83% of 78 cells). In all cats the misalignment of the visual axes had led to a disruption of cortical binocularity. This effect was obvious in each of the 6 animals and as shown in Fig. 1 also quantitatively similar in the 3 different groups. Only a small fraction of the cells had remained binocular in the animals raised with asymmetrical squint (23 %), with symmetrical divergent squint (33 %) and with convergent squint (25 %). In the two cats with asymmetrical squint, the normal eye was slightly dominant while in the cats with symmetrical squint both eyes were equally effective in driving cortical cells (compare Fig. 1A-C). As far as the animals with asymmetric squint are concerned, the marked loss of binocularity is in perfect agreement with Hubel and Wiesel's finding z. In a recent study 2 it has been claimed, however, that symmetrical squint does not cause disruption of binocularity in spite of the misalignment of the visual axes. The reason for this discrepancy is still unknown but for the purpose of the present investigation this issue is not relevant. The evaluation of the neurons' orientation preference showed that the misalignment of the visual axes had not only reduced binocularity but had also interfered with
A
B
C
divergent asymmetrical sc~nt
diveegenl symmetrical squ~
convergent syrnmetriml squint
50,
5O" N ~66
5O N= 65
25
N= 120
25
25
1
2
3 Id'l r,ormal
right eye
left eye
right eye
left eye
Fig. 1. Ocular dominance (OD) distributions in kittens with asymmetrical divergent squint (A), symmetrical divergent squint (B) and symmetrical convergent squint (C). Ordinate: number of ceils in the 50D classes. OD classes 1 and 5 comprise monocular cells, OD class 3 contains binocular cells driven equally well from both eyes and OD classes 2 and 3 comprise binocular cells dominated from either the left (2) or the right (4) eye.
184 the distribution o f orientation preferences. Since c o n t o u r vision was u n i m p a i r e d during the critical period o f d e v e l o p m e n t the large m a j o r i t y ot cortical cells showed a clear preference for p a r t i c u l a r stimulus orientations; 9 ! ~ o f the responsive cells in the cats with a s y m m e t r i c a l squint, 93 ~ a n d 89 ~ in the cats with symmetrical divergent a n d convergent squint, respectively. As shown in Fig. 2, however, there was a significant u n d e r - r e p r e s e n t a t i o n o f neurons preferring orientations close to the vertical. This t r e n d was similar in the 3 groups o f squinting animals. W h e n tested with Z 2 against the null-hypothesis o f an even distribution o f orientations the under-representation o f
A
B
N : 225
135 °
112 5 °
90 °
N = 190
67.5 °
45 °
135 °
112.5 °
90 °
67.5 °
45 °
22.5 °
.5 °
Do
135 °
112.5 °
C
D
N =67
N = 287
90 °
67.5 °
45 °
135 °
.5 °
112.5 °
90 °
67.5 °
45 °
22.5 °
Do
Fig. 2. Polar diagrams for orientation preferences of cortical cells in kittens raised with squint. The 0 ~ vector corresponds to horizontally and the 90 ° vector to vertically oriented receptive fields. The lengths of the vectors within the shaded area indicate the percentages of cells with corresponding orientation preferences. A : distribution of preferred orientations of all cells analyzed in the 6 squinting animals. B: orientation distribution after deduction of the cells that reacted poorly to light and had been given the lowest index of response quality. C: orientation distribution of the fraction of cells that had remained binocular. D: orientation distribution of cells recorded from 6 monocularly deprived kittens.
185 cells with orientation preferences between 67 ° and 112° was significant at the P < 0.01 level. This distortion in the orientation distribution became even more significant (P < 0.001), when all cells (n=35) with extremely weak and sluggish responses (quality index = 1) were discarded from analysis (Fig. 2B). This indicates that cells with preferences for vertical orientations were not only encountered less frequently but were in addition less reactive to retinal stimulation than the average. As in the cats with inverted vision~ the loss of cells with vertically oriented receptive fields was more pronounced in binocular than in monocular cells (compare Fig. 2A and C). For the binocular cells, the ratio of horizontally (0 °, 22.5 °, 157°) vs vertically (67°, 90 °, 112°) oriented receptive fields was 2.73 as compared to 1.55 for the monocular cells. Because of the relatively small number of binocular cells (n--67), the under-representation of cells with preferences for 67°-112 ° is, however, only significant at the P < 0.03 level. As a control for our sampling and mapping procedures, orientation distributions were compiled from 6 cats that had undergone conventional monocular deprivation and had been investigated for other purposes. The distribution in Fig. 2D shows no clear bias for a particular orientation. There is a slight over-representation of vertically oriented receptive fields and a slight reduction of oblique orientations but this trend is not significant. Since these control data were obtained with exactly the same techniques and under similarly bias-free conditions as the data in the present study, the reduction of vertically oriented receptive fields in squinting animals can barely be attributed to sampling artefacts. At the present stage we ignore the fate of the missing cells in the squinting animals. Since squint was introduced at the beginning of the critical period and right after dark-rearing it is conceivable that a certain class of cells has failed to develop their appropriate receptive field characteristics; alternatively it might be considered that cells whose prespecified functional role is no longer required or inadequate have become unresponsive or unrecordable because of shrinkage. Irrespective of the mechanisms involved, the reduction of recordable cells with preferences for orientations close to the vertical suggests a distinct function of these cells. Because squint interferes specifically with binocular fusion and vergence movements it appears likely that the missing cells had been or would have been involved in those processes. The fact that the 'missing' cells would have been mainly binocular and encoding preferentially movements in the horizontal plane is in agreement with this hypothesis. A further conclusion can be drawn from the observation that cells with vertically oriented receptive fields were not under-represented in the control group although these animals, too, had no binocular vision because of monocular deprivation. This suggests that incongruent signals are more disruptive than the non-availability of binocular signals. Thus, in line with the data obtained from kittens with inverted monocular vision 5, the induction of specific incongruencies of sensory input can serve as a valuable tool for the dissection ot otherwise concealed neuronal subsystems.
186 1 Hubel, D. H. and Wiesel, T. N., Binocular interaction in striate cortex of kittens reared with artificial squint, J. NeurophysioL, 28 (1965) 1041-1059. 2 Bisti, S. and Maffei, L., Binocular interaction in bilateral strabismic kittens, Brain Research, in press. 3 Singer, W., Effects of monocular deprivation on excitatory and inhibitory pathways in cat striate cortex, Exp. Brain Res., 30 (1977) 2541. 4 Singer, W., Tretter, F. and Yinon, U., Inverted vision prevents ocular dominance shift in kittens an d i mpai rs function of mature visual cortex, Brain Research, 164 (1979) 294-299. 5 Singer, W., Tretter, F. and Yinon, U., Inverted vision causes selective loss of striate cortex neurons with binocular, vertically oriented receptive fields, Brain Research, 170 (1979) 177-181.
Brain Research, 170 (1979) 182-186 ;© Elsevier/North-Holland Biomedical Press
Squint affects striate cortex cells encoding horizontal image movements
w. SINGER, J. RAUSCHECKER and M. von GRUENAU Max-Planck-lnstitut fiir Psych iatrie, Kraepelinstr. 2, 8000 Miinchen 40 ( G. F. R.)
(Accepted March 8th, 1979)
The incongruency between retinal coordinates and other sensory-motor maps, such as results from surgical eye rotation, causes a drastic reduction of light reactive cells in striate cortex of developing and mature cats 4. It has been concluded from these observations that a substantial fraction of neurons in primary visual cortex subserve specific functions in visuomotor and polymodal processing. With 180° inversion of the retinal coordinates there was in addition a selective loss of binocular cells preferring vertical stimulus orientations 5. Since these neurons encode preferentially image displacements with a prominent horizontal vector, it was suggested that they might be involved in the coordination of horizontal eye movements. In this context vergence movements were thought to be of particular interest since they occur only in the horizontal plane and since their coordination is likely to require binocular cells sensitive to horizontal image displacements. These considerations led to the hypothesis that squint also might lead to a reduction of cells with vertically oriented receptive fields since it disturbs binocular fusion and concomitant vergence movements. To test this hypothesis data were evaluated from two independent series of experiments in which squinting cats had been examined for other purposes. Thus, by the time of data acquisition, none of the experimenters knew about the working hypothesis of the present investigation. Data were taken from 6 squinting kittens. In two animals asymmetrical divergent squint had been induced by section of the medial rectus muscle of the right eye. In the remaining 4 kittens squint had been induced symmetrically: two of them had the lateral recti of both eyes cut (symmetrical convergent squint) and in the other two, the medial recti were severed (symmetrical divergent squint). All animals had been operated on when 28 days old. Until the operation they had been kept in complete darkness, thereafter they were raised in normal animal house environment. Survival time until the electrophysiological experiment varied between 5 and 11 months. Preparation and recording techniques for the analysis of cortical receptive fields were conventional and identical to those routinely applied in this laboratory ~. Single units were recorded extracellularly from striate cortex of both hemispheres with potassium citrate-filled micropipettes. During penetration, a weak positive c-urrent (2-5 hA) was applied through the pipette to activate cells lacking spontaneous activity.
183 Receptive fields were plotted with hand-held stimuli. In all cases where this procedure failed to yield clear characterization of ocular dominance and preferred orientation, response histograms were compiled after stimulation with an electromechanical light stimulator. To reduce the sampling bias imposed by the columnar organization of striate cortex, electrode penetrations were directed with an inclination of 30° to the cortical surface from posterior to anterior. In addition to common receptive field parameters (ocular dominance, orientation preference and tuning, direction selectivity, field size, velocity preference) the vigour of responses to optimally aligned stimuli was estimated and rated in a subjective scale of 5 classes. In the cats with asymmetrical squint, 93 % of 71 analyzed cells could be driven with light stimuli. In the animals with symmetrical squint the percentage of lightreactive cells was slightly less (convergent: 84% of 143 cells; divergent: 83% of 78 cells). In all cats the misalignment of the visual axes had led to a disruption of cortical binocularity. This effect was obvious in each of the 6 animals and as shown in Fig. 1 also quantitatively similar in the 3 different groups. Only a small fraction of the cells had remained binocular in the animals raised with asymmetrical squint (23 %), with symmetrical divergent squint (33 %) and with convergent squint (25 %). In the two cats with asymmetrical squint, the normal eye was slightly dominant while in the cats with symmetrical squint both eyes were equally effective in driving cortical cells (compare Fig. 1A-C). As far as the animals with asymmetric squint are concerned, the marked loss of binocularity is in perfect agreement with Hubel and Wiesel's finding z. In a recent study 2 it has been claimed, however, that symmetrical squint does not cause disruption of binocularity in spite of the misalignment of the visual axes. The reason for this discrepancy is still unknown but for the purpose of the present investigation this issue is not relevant. The evaluation of the neurons' orientation preference showed that the misalignment of the visual axes had not only reduced binocularity but had also interfered with
A
B
C
divergent asymmetrical sc~nt
diveegenl symmetrical squ~
convergent syrnmetriml squint
50,
5O" N ~66
5O N= 65
25
N= 120
25
25
1
2
3 Id'l r,ormal
right eye
left eye
right eye
left eye
Fig. 1. Ocular dominance (OD) distributions in kittens with asymmetrical divergent squint (A), symmetrical divergent squint (B) and symmetrical convergent squint (C). Ordinate: number of ceils in the 50D classes. OD classes 1 and 5 comprise monocular cells, OD class 3 contains binocular cells driven equally well from both eyes and OD classes 2 and 3 comprise binocular cells dominated from either the left (2) or the right (4) eye.
184 the distribution o f orientation preferences. Since c o n t o u r vision was u n i m p a i r e d during the critical period o f d e v e l o p m e n t the large m a j o r i t y ot cortical cells showed a clear preference for p a r t i c u l a r stimulus orientations; 9 ! ~ o f the responsive cells in the cats with a s y m m e t r i c a l squint, 93 ~ a n d 89 ~ in the cats with symmetrical divergent a n d convergent squint, respectively. As shown in Fig. 2, however, there was a significant u n d e r - r e p r e s e n t a t i o n o f neurons preferring orientations close to the vertical. This t r e n d was similar in the 3 groups o f squinting animals. W h e n tested with Z 2 against the null-hypothesis o f an even distribution o f orientations the under-representation o f
A
B
N : 225
135 °
112 5 °
90 °
N = 190
67.5 °
45 °
135 °
112.5 °
90 °
67.5 °
45 °
22.5 °
.5 °
Do
135 °
112.5 °
C
D
N =67
N = 287
90 °
67.5 °
45 °
135 °
.5 °
112.5 °
90 °
67.5 °
45 °
22.5 °
Do
Fig. 2. Polar diagrams for orientation preferences of cortical cells in kittens raised with squint. The 0 ~ vector corresponds to horizontally and the 90 ° vector to vertically oriented receptive fields. The lengths of the vectors within the shaded area indicate the percentages of cells with corresponding orientation preferences. A : distribution of preferred orientations of all cells analyzed in the 6 squinting animals. B: orientation distribution after deduction of the cells that reacted poorly to light and had been given the lowest index of response quality. C: orientation distribution of the fraction of cells that had remained binocular. D: orientation distribution of cells recorded from 6 monocularly deprived kittens.
185 cells with orientation preferences between 67 ° and 112° was significant at the P < 0.01 level. This distortion in the orientation distribution became even more significant (P < 0.001), when all cells (n=35) with extremely weak and sluggish responses (quality index = 1) were discarded from analysis (Fig. 2B). This indicates that cells with preferences for vertical orientations were not only encountered less frequently but were in addition less reactive to retinal stimulation than the average. As in the cats with inverted vision~ the loss of cells with vertically oriented receptive fields was more pronounced in binocular than in monocular cells (compare Fig. 2A and C). For the binocular cells, the ratio of horizontally (0 °, 22.5 °, 157°) vs vertically (67°, 90 °, 112°) oriented receptive fields was 2.73 as compared to 1.55 for the monocular cells. Because of the relatively small number of binocular cells (n--67), the under-representation of cells with preferences for 67°-112 ° is, however, only significant at the P < 0.03 level. As a control for our sampling and mapping procedures, orientation distributions were compiled from 6 cats that had undergone conventional monocular deprivation and had been investigated for other purposes. The distribution in Fig. 2D shows no clear bias for a particular orientation. There is a slight over-representation of vertically oriented receptive fields and a slight reduction of oblique orientations but this trend is not significant. Since these control data were obtained with exactly the same techniques and under similarly bias-free conditions as the data in the present study, the reduction of vertically oriented receptive fields in squinting animals can barely be attributed to sampling artefacts. At the present stage we ignore the fate of the missing cells in the squinting animals. Since squint was introduced at the beginning of the critical period and right after dark-rearing it is conceivable that a certain class of cells has failed to develop their appropriate receptive field characteristics; alternatively it might be considered that cells whose prespecified functional role is no longer required or inadequate have become unresponsive or unrecordable because of shrinkage. Irrespective of the mechanisms involved, the reduction of recordable cells with preferences for orientations close to the vertical suggests a distinct function of these cells. Because squint interferes specifically with binocular fusion and vergence movements it appears likely that the missing cells had been or would have been involved in those processes. The fact that the 'missing' cells would have been mainly binocular and encoding preferentially movements in the horizontal plane is in agreement with this hypothesis. A further conclusion can be drawn from the observation that cells with vertically oriented receptive fields were not under-represented in the control group although these animals, too, had no binocular vision because of monocular deprivation. This suggests that incongruent signals are more disruptive than the non-availability of binocular signals. Thus, in line with the data obtained from kittens with inverted monocular vision 5, the induction of specific incongruencies of sensory input can serve as a valuable tool for the dissection ot otherwise concealed neuronal subsystems.
186 1 Hubel, D. H. and Wiesel, T. N., Binocular interaction in striate cortex of kittens reared with artificial squint, J. NeurophysioL, 28 (1965) 1041-1059. 2 Bisti, S. and Maffei, L., Binocular interaction in bilateral strabismic kittens, Brain Research, in press. 3 Singer, W., Effects of monocular deprivation on excitatory and inhibitory pathways in cat striate cortex, Exp. Brain Res., 30 (1977) 2541. 4 Singer, W., Tretter, F. and Yinon, U., Inverted vision prevents ocular dominance shift in kittens an d i mpai rs function of mature visual cortex, Brain Research, 164 (1979) 294-299. 5 Singer, W., Tretter, F. and Yinon, U., Inverted vision causes selective loss of striate cortex neurons with binocular, vertically oriented receptive fields, Brain Research, 170 (1979) 177-181.