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Cells of the striate cortex projecting to the Clare-Bishop area of the cat
154
Brain Research, 151 (1978) 154-158 © Elsevier/North-Holland Biomedical Press
Cells of the striate cortex projecting to the Clare-Bishop area of the cat
G. H. HENRY, J. S. LUND* and A. R. HARVEY Department o.f Physiology, John Curtin School of Medical Research, Australian National University, Canberra, A. C. T. 2601 (Australia)
(Accepted February 9th, 1978)
Distinctive features in striate neuron response patterns are more readily appreciated if there is information on the site of projection of the cell's axonS,9,15. Anatomical studies tracing the extrinsic projections of axons have shown that cells with a common destination are frequently grouped in a single lamina in the striate cortex (area 17). In the cat, striate neurons projecting to the Clare-Bishop cortex are confined to laminae 2-35 (commonly treated as a single lamina), although cells in these laminae also project to other cortical regions. The aim of the present study is to separate, through physiological identification, those striate cells sending axons to the Clare-Bishop area. At the same time, an attempt is made to establish the possible intralaminar linkages of these cells. Single cell activity in the striate cortex was monitored with tungsten in glass microelectrodes. With stimulating electrodes in the medial bank of the suprasylvian sulcus it was possible to determine if the striate neuron could be driven antidromically or orthodromically from the Clare-Bishop area. Antidromic activation was taken as evidence that the axon of the striate neuron projected to the Clare-Bishop cortex. Spike collision and the following of high frequency stimulation were adopted as criteria for antidromic activation 1. In most of the experiments the recording electrode was directed to pass within laminae 2-3 on the medial bank of the lateral gyrus, but additional tracks were made to pass through all layers of the striate cortex in order to survey the laminar distribution of different receptive field types. Reference will be made to this distribution, but a more detailed account will be presented in the future. Following procedures already describe&, the cat was anaesthetised (N20/O2) and paralyzed (Flaxedil and Toxiferin) and artificially respired. Craniotomies were performed for the insertion of the recording electrode in the striate cortex and for a line of 6 stimulating electrodes (each 2 m m apart) angled into the Clare-Bishop area (from H C coordinates, AP - - 2 to + 1 0 and M L 14). Generally, the recording electrode entered the striate cortex close to the H-C coordinates, AP - - 3 ; M L 1.5. To extend the traverse of laminae 2-3 the electrode was tilted so that its tip was angled forward 30 ° * Present address: Department of Ophthalmology, University of Washington, Seattle, U.S.A.
155 and medially 10°. Nissl-stained sections (40/~m in thickness) were prepared for the reconstruction of the electrode path, and relative depths in each track were assessed from electrolytic lesions spaced at intervals of approximately 1 mm. Only those cells from tracks in which lesions were unambiguously defined are included in the analysis. The laminar pattern in the Nissl preparations was identified by using criteria closely conforming to those of O'Leary 14. The receptive fields were classed as S, SH, C or C a according to established response characteristics 9, with the exception that subdivisions now appear to be emerging within the C class of neuron. In general terms we are in agreement with Gilbert 6 that there are basically two groups of C or complex cells, although we have not placed the same weight on length-wise summation (along the line of optimal orientation) as a classing property. Our C cell, which seems similar in many respects to Gilbert's 6 special complex cell and Palmer and Rosenquist's 15 complex cell, has a large receptive field (usually greater than 2° in length and width) of composite O N / O F F discharge that can also be driven by both a light and dark moving edge. We have labelled as B a cell 9 that seems identical with a complex cell described by Camarda and Rizzolattia, 4 and shows some resemblance to the standard complex cells of Gilbert. It shares the C cell's responses to flashing and moving stimuli but has a smaller receptive field (generally less than 2° in length and width), and differs further from the C cell in having a preference for more slowly moving stimuli, little or no spontaneous activity, and responds with a sustained response when a light bar is flashed on. The response profile to a moving edge also seems smoother in outline than that of the C cell. The exact duplication of Gilbert's subdivision appears to break down, however, in that cells of our C category may or may not respond to short bars, which apparently indicates that the length-response curve rises sharply in some C cells and not in others. Ultimately it may prove advisable to further subdivide the C category, but this possibility need not concern us at present, since these cells do not appear to project to the Clare-Bishop cortex. A feature of the recording from laminae 2-3 was that cells were less visually responsive than those isolated in lower laminae in the same preparation. A relatively high proportion of cells possessing the hypercomplex or H property may account for this apparent sluggishness. However, many cells without the H property were encountered, and Table I shows the distribution of different cell types found in the lamina 2-3 zone (including 25 cells at the border of laminae 3 and 4 which was taken as a region 100/zm thick) from a population of 169 cells found in 22 electrode penetrations in 13 cats. In total 302 cells (98 unclassed) were recorded from all laminae. Table I shows that units activated antidromically from the Clare-Bishop area were encountered only rarely (6.5 ~ of all units in the lamina 2-3 zone and none in any other lamina), but that one particular cell, the B group, makes a major contribution to this number. If grouped with BK cells (i.e. cells with the same basic response pattern as B but also showing end zone inhibition), then at least 20 ~o of the group as a whole appear to project to the Clare-Bishop area. No other type of cell has anything like this proportion of antidromic responses. A similar class distinction is not apparent in cells orthodromically activated from the Clare-Bishop area (18.9 ~ of the population of
156 TABLE
I
Distribution of different cell types found in lamina 2-3 zone Cell type
Number in laminae 2-3 (incl. 3/4 border)
Number (all in lamina 3) driven antidromically from C.B.
Number (in all laminae) driven orthodromieally from C.B.
S SH C
47 19 6
1 1 --
7 4 7
CH B BH Non-oriented Miscellaneous Unclassed
2 30 11 1 4 49
-5 3 -1 --
! 10 5 6 -17
302), although it is perhaps significant that a number of the B group receive an input from this area. Following the emergence of the B group of cells in laminae 2-3 as possible candidates for the striate cells projecting to the Clare-Bishop area, we looked for its presence in other laminae in the striate cortex. To remove the bias that came from directing the recording electrode towards laminae 2-3, we included the data from 20 additional cats (with no stimulating electrodes present in Clare-Bishop area) in deriving this lamina distribution. In this larger population the B group (including the B~) made up 31.5 of the 146 classified cells in the lamina 2-3 zone (including the 3/4 border). The only other location where the B cell type occurred in significant numbers was in lamina 5A (or 4/5 border zone), where the B groups made up 37.5 ~ of 16 classified cells. The similarity in the receptive field properties of cells in laminae 3 and 5A may be associated with a morphological link between these two laminae. From our own Golgi studies and those of others 2,11,14, lamina 5A was found to have a population of small pyramidal cells with recurrent axons that ascend to arborise profusely in laminae 2-3. In addition, lamina 5A and the lower reaches of lamina 3 share a common afferent supply in receiving a direct projection from the C laminae of the lateral geniculate nucleus 10. With similar afferent signals it is not surprising that the processing of information progresses to a similar stage of abstraction in cells in the two laminae. In addition to the lamina 5A/2-3 link, there is also evidence from studies in axon terminal degeneration of a strong projection from laminae 2-3 to lamina 5B 13. Golgi material indicates that this projection consists principally of axon collaterals of lamina 2-3 pyramids. We have also confirmed the existence of this lamina 2-3/5B link by injecting tritiated proline into laminae 2-3. After 24 h survival a cohesive band of radioactive uptake was found confined to lamina 5B (see Fig. 1). However, with this survival time we could find no evidence of uptake in the Clare-Bishop cortex. From physiological recording many cells in lamina 5B are shown to have C type receptive fields, which, from tests with electrical stimulation, appear to project to the superior colli-
157
L_
Fig. 1. A dark-field photomicrograph showing a coherent band of radioactive labeling in lamina 5 after injection of tritiated proline into laminae 2-3. In the line drawing, the arrow shows the path of the injecting pipette; the rectangle outlines the area photographed. Heavy labeling is apparent in the vicinity of some of the large pyramidal cell bodies in lamina 5B. Examination under high power reveals a tailing off in the labeling around the smaller pyramids of lamina 5A. Streaming in laminae 4 and 6 is consistent with axonal transport in lamina 2-3 cells.
culusS, 15. The presence of this lamina 2-3/5B link raises the prospect that cells in laminae 2-3 (possibly with B type receptive fields), as well as providing an input to the Clare-Bishop cortex, also contribute axon collaterals to influence the firing of the C cells in lamina 5B projecting to the superior colliculus. The present study has indicated that the level of processing of visual information attained in the striate cortex prior to transfer to the Clare-Bishop area is reflected in the receptive field properties of the B cells of laminae 2-3. From the pattern of intracortical linkages it is likely that the activity of these lamina 2-3 B cells is (1) collated with the firing of cells in lamina 5A, which have similar receptive fields, and also (2) influences the responses of the C cells in lamina 5B that project to the superior colliculus.
158
Supported by NIH Research Grants EY-01086 and HD02274, and by the Lions N.S.W.-A.C.T. Save Sight Foundation. We are most grateful for technical assistance from Mr. C. MacQueen and Ms. R. Wise (preparation of histological material), Mr. R. M. Tupper and Mr. K. Collins (aid in the physiological experiments) and Ms. J. M. Anderson (preparation of the manuscript).
1 Bishop, P. O., Burke, W. and Davis, R., Single-unit recording from antidromically activated optic radiation neurones, J. Physiol. (Lond.), 162 (1962) 432-450. 2 Cajal, S., Ram6n y, Histologie de Systdme Nerveux de l'Homme et des Vertebrds, Vol. 2, Paris, 191 l, pp. 599-618. 3 Camarda, R. and Rizzolatti, G.,Receptivefieldsofcellsinthesuperficiallayersofthecat'sarea 17, Exp. Brain Res., 24 (1976) 423-427. 4 Camarda, R., Personal communication. 5 Gilbert, C. D. and Kelly, J. P., The projections of cells in different layers of the cat's visual cortex, J. cornp. Neurol., 163 (1975) 81-106. 6 Gilbert, C. D., Laminar differences in receptive field properties of cells in cat primary visual cortex, J. Physiol. (Lond.), 268 (1977) 391-424. 7 Goodwin, A. W., Henry, G. H. and Bishop, P. O., Direction selectivity of simple striate cells: properties and mechanism, J. Neurophysiol., 38 (1975) 1500-1523. 8 Harvey, A. R., Characteristics of corticothalamic neurons in area 17 of the cat, Neurosci. Lett., in press. 9 Henry, G. H., Receptive field classes of cells in the striate cortex of the cat, Brain Research, 133 (1977) 1-28. 10 LeVay, S. and Gilbert, C. D., Laminar patterns of geniculocortical projection in the cat, Brain Research, 113 (1976) 1-19. 11 Lorente de N6, R., Cerebral cortex: architecture, intracortical connections, motor projections. In J. Fulton, Physiology of the Nervous System, Oxford Univ. Press, 1949, pp. 288-330. 12 Lund, J. S. and Booth, R. G., Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17 of the macaque monkey, J. comp. Neurol., 159 (1975) 305-334. 13 Nauta, H. J. W., Butler, A. W. and Jane, J. A., Some observations on axonal degeneration resulting from superficial lesions of the cerebral cortex, J. eomp. Neurol., 150 0973) 349-360. 14 O'Leary, J. L., Structure of the area striata of the cat, J. comp. NeuroL, 75 (1941 ) 131-16 I. 15 Palmer, L. A. and Rosenquist, A. C., Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat, Brain Research, 67 (1974) 27-42.
Brain Research, 151 (1978) 154-158 © Elsevier/North-Holland Biomedical Press
Cells of the striate cortex projecting to the Clare-Bishop area of the cat
G. H. HENRY, J. S. LUND* and A. R. HARVEY Department o.f Physiology, John Curtin School of Medical Research, Australian National University, Canberra, A. C. T. 2601 (Australia)
(Accepted February 9th, 1978)
Distinctive features in striate neuron response patterns are more readily appreciated if there is information on the site of projection of the cell's axonS,9,15. Anatomical studies tracing the extrinsic projections of axons have shown that cells with a common destination are frequently grouped in a single lamina in the striate cortex (area 17). In the cat, striate neurons projecting to the Clare-Bishop cortex are confined to laminae 2-35 (commonly treated as a single lamina), although cells in these laminae also project to other cortical regions. The aim of the present study is to separate, through physiological identification, those striate cells sending axons to the Clare-Bishop area. At the same time, an attempt is made to establish the possible intralaminar linkages of these cells. Single cell activity in the striate cortex was monitored with tungsten in glass microelectrodes. With stimulating electrodes in the medial bank of the suprasylvian sulcus it was possible to determine if the striate neuron could be driven antidromically or orthodromically from the Clare-Bishop area. Antidromic activation was taken as evidence that the axon of the striate neuron projected to the Clare-Bishop cortex. Spike collision and the following of high frequency stimulation were adopted as criteria for antidromic activation 1. In most of the experiments the recording electrode was directed to pass within laminae 2-3 on the medial bank of the lateral gyrus, but additional tracks were made to pass through all layers of the striate cortex in order to survey the laminar distribution of different receptive field types. Reference will be made to this distribution, but a more detailed account will be presented in the future. Following procedures already describe&, the cat was anaesthetised (N20/O2) and paralyzed (Flaxedil and Toxiferin) and artificially respired. Craniotomies were performed for the insertion of the recording electrode in the striate cortex and for a line of 6 stimulating electrodes (each 2 m m apart) angled into the Clare-Bishop area (from H C coordinates, AP - - 2 to + 1 0 and M L 14). Generally, the recording electrode entered the striate cortex close to the H-C coordinates, AP - - 3 ; M L 1.5. To extend the traverse of laminae 2-3 the electrode was tilted so that its tip was angled forward 30 ° * Present address: Department of Ophthalmology, University of Washington, Seattle, U.S.A.
155 and medially 10°. Nissl-stained sections (40/~m in thickness) were prepared for the reconstruction of the electrode path, and relative depths in each track were assessed from electrolytic lesions spaced at intervals of approximately 1 mm. Only those cells from tracks in which lesions were unambiguously defined are included in the analysis. The laminar pattern in the Nissl preparations was identified by using criteria closely conforming to those of O'Leary 14. The receptive fields were classed as S, SH, C or C a according to established response characteristics 9, with the exception that subdivisions now appear to be emerging within the C class of neuron. In general terms we are in agreement with Gilbert 6 that there are basically two groups of C or complex cells, although we have not placed the same weight on length-wise summation (along the line of optimal orientation) as a classing property. Our C cell, which seems similar in many respects to Gilbert's 6 special complex cell and Palmer and Rosenquist's 15 complex cell, has a large receptive field (usually greater than 2° in length and width) of composite O N / O F F discharge that can also be driven by both a light and dark moving edge. We have labelled as B a cell 9 that seems identical with a complex cell described by Camarda and Rizzolattia, 4 and shows some resemblance to the standard complex cells of Gilbert. It shares the C cell's responses to flashing and moving stimuli but has a smaller receptive field (generally less than 2° in length and width), and differs further from the C cell in having a preference for more slowly moving stimuli, little or no spontaneous activity, and responds with a sustained response when a light bar is flashed on. The response profile to a moving edge also seems smoother in outline than that of the C cell. The exact duplication of Gilbert's subdivision appears to break down, however, in that cells of our C category may or may not respond to short bars, which apparently indicates that the length-response curve rises sharply in some C cells and not in others. Ultimately it may prove advisable to further subdivide the C category, but this possibility need not concern us at present, since these cells do not appear to project to the Clare-Bishop cortex. A feature of the recording from laminae 2-3 was that cells were less visually responsive than those isolated in lower laminae in the same preparation. A relatively high proportion of cells possessing the hypercomplex or H property may account for this apparent sluggishness. However, many cells without the H property were encountered, and Table I shows the distribution of different cell types found in the lamina 2-3 zone (including 25 cells at the border of laminae 3 and 4 which was taken as a region 100/zm thick) from a population of 169 cells found in 22 electrode penetrations in 13 cats. In total 302 cells (98 unclassed) were recorded from all laminae. Table I shows that units activated antidromically from the Clare-Bishop area were encountered only rarely (6.5 ~ of all units in the lamina 2-3 zone and none in any other lamina), but that one particular cell, the B group, makes a major contribution to this number. If grouped with BK cells (i.e. cells with the same basic response pattern as B but also showing end zone inhibition), then at least 20 ~o of the group as a whole appear to project to the Clare-Bishop area. No other type of cell has anything like this proportion of antidromic responses. A similar class distinction is not apparent in cells orthodromically activated from the Clare-Bishop area (18.9 ~ of the population of
156 TABLE
I
Distribution of different cell types found in lamina 2-3 zone Cell type
Number in laminae 2-3 (incl. 3/4 border)
Number (all in lamina 3) driven antidromically from C.B.
Number (in all laminae) driven orthodromieally from C.B.
S SH C
47 19 6
1 1 --
7 4 7
CH B BH Non-oriented Miscellaneous Unclassed
2 30 11 1 4 49
-5 3 -1 --
! 10 5 6 -17
302), although it is perhaps significant that a number of the B group receive an input from this area. Following the emergence of the B group of cells in laminae 2-3 as possible candidates for the striate cells projecting to the Clare-Bishop area, we looked for its presence in other laminae in the striate cortex. To remove the bias that came from directing the recording electrode towards laminae 2-3, we included the data from 20 additional cats (with no stimulating electrodes present in Clare-Bishop area) in deriving this lamina distribution. In this larger population the B group (including the B~) made up 31.5 of the 146 classified cells in the lamina 2-3 zone (including the 3/4 border). The only other location where the B cell type occurred in significant numbers was in lamina 5A (or 4/5 border zone), where the B groups made up 37.5 ~ of 16 classified cells. The similarity in the receptive field properties of cells in laminae 3 and 5A may be associated with a morphological link between these two laminae. From our own Golgi studies and those of others 2,11,14, lamina 5A was found to have a population of small pyramidal cells with recurrent axons that ascend to arborise profusely in laminae 2-3. In addition, lamina 5A and the lower reaches of lamina 3 share a common afferent supply in receiving a direct projection from the C laminae of the lateral geniculate nucleus 10. With similar afferent signals it is not surprising that the processing of information progresses to a similar stage of abstraction in cells in the two laminae. In addition to the lamina 5A/2-3 link, there is also evidence from studies in axon terminal degeneration of a strong projection from laminae 2-3 to lamina 5B 13. Golgi material indicates that this projection consists principally of axon collaterals of lamina 2-3 pyramids. We have also confirmed the existence of this lamina 2-3/5B link by injecting tritiated proline into laminae 2-3. After 24 h survival a cohesive band of radioactive uptake was found confined to lamina 5B (see Fig. 1). However, with this survival time we could find no evidence of uptake in the Clare-Bishop cortex. From physiological recording many cells in lamina 5B are shown to have C type receptive fields, which, from tests with electrical stimulation, appear to project to the superior colli-
157
L_
Fig. 1. A dark-field photomicrograph showing a coherent band of radioactive labeling in lamina 5 after injection of tritiated proline into laminae 2-3. In the line drawing, the arrow shows the path of the injecting pipette; the rectangle outlines the area photographed. Heavy labeling is apparent in the vicinity of some of the large pyramidal cell bodies in lamina 5B. Examination under high power reveals a tailing off in the labeling around the smaller pyramids of lamina 5A. Streaming in laminae 4 and 6 is consistent with axonal transport in lamina 2-3 cells.
culusS, 15. The presence of this lamina 2-3/5B link raises the prospect that cells in laminae 2-3 (possibly with B type receptive fields), as well as providing an input to the Clare-Bishop cortex, also contribute axon collaterals to influence the firing of the C cells in lamina 5B projecting to the superior colliculus. The present study has indicated that the level of processing of visual information attained in the striate cortex prior to transfer to the Clare-Bishop area is reflected in the receptive field properties of the B cells of laminae 2-3. From the pattern of intracortical linkages it is likely that the activity of these lamina 2-3 B cells is (1) collated with the firing of cells in lamina 5A, which have similar receptive fields, and also (2) influences the responses of the C cells in lamina 5B that project to the superior colliculus.
158
Supported by NIH Research Grants EY-01086 and HD02274, and by the Lions N.S.W.-A.C.T. Save Sight Foundation. We are most grateful for technical assistance from Mr. C. MacQueen and Ms. R. Wise (preparation of histological material), Mr. R. M. Tupper and Mr. K. Collins (aid in the physiological experiments) and Ms. J. M. Anderson (preparation of the manuscript).
1 Bishop, P. O., Burke, W. and Davis, R., Single-unit recording from antidromically activated optic radiation neurones, J. Physiol. (Lond.), 162 (1962) 432-450. 2 Cajal, S., Ram6n y, Histologie de Systdme Nerveux de l'Homme et des Vertebrds, Vol. 2, Paris, 191 l, pp. 599-618. 3 Camarda, R. and Rizzolatti, G.,Receptivefieldsofcellsinthesuperficiallayersofthecat'sarea 17, Exp. Brain Res., 24 (1976) 423-427. 4 Camarda, R., Personal communication. 5 Gilbert, C. D. and Kelly, J. P., The projections of cells in different layers of the cat's visual cortex, J. cornp. Neurol., 163 (1975) 81-106. 6 Gilbert, C. D., Laminar differences in receptive field properties of cells in cat primary visual cortex, J. Physiol. (Lond.), 268 (1977) 391-424. 7 Goodwin, A. W., Henry, G. H. and Bishop, P. O., Direction selectivity of simple striate cells: properties and mechanism, J. Neurophysiol., 38 (1975) 1500-1523. 8 Harvey, A. R., Characteristics of corticothalamic neurons in area 17 of the cat, Neurosci. Lett., in press. 9 Henry, G. H., Receptive field classes of cells in the striate cortex of the cat, Brain Research, 133 (1977) 1-28. 10 LeVay, S. and Gilbert, C. D., Laminar patterns of geniculocortical projection in the cat, Brain Research, 113 (1976) 1-19. 11 Lorente de N6, R., Cerebral cortex: architecture, intracortical connections, motor projections. In J. Fulton, Physiology of the Nervous System, Oxford Univ. Press, 1949, pp. 288-330. 12 Lund, J. S. and Booth, R. G., Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17 of the macaque monkey, J. comp. Neurol., 159 (1975) 305-334. 13 Nauta, H. J. W., Butler, A. W. and Jane, J. A., Some observations on axonal degeneration resulting from superficial lesions of the cerebral cortex, J. eomp. Neurol., 150 0973) 349-360. 14 O'Leary, J. L., Structure of the area striata of the cat, J. comp. NeuroL, 75 (1941 ) 131-16 I. 15 Palmer, L. A. and Rosenquist, A. C., Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat, Brain Research, 67 (1974) 27-42.