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Geometry and orientation of thalamocortical arborizations in the cat somatosensory cortex as revealed by computer reconstruction
222
Brain Research, 237 (1982) 222-226
Elsevier Biomedical Press
Geometry and orientation of thalamocorti,cal arborizations in the cat somatosensory cortex as revealed by computer reconstruction
PIERRE LANDRY, JEAN VILLEMURE and MARTIN DESCHENES Laboratoire de Neurophysiologie, Ddpartement de Physiologie et Centre de Traitement de l'lnformation, Universitd Laval, Quebec, G1K 7P4 (Canada)
(Accepted December 17th, 1981) Key words: area S1 - - thalamocortical arbors - - cortical columns - - somatotopy
The geometry of the intracortical arborization of single neurons from the ventroposterolateral thalamic nucleus in cat was studied with computer reconstruction after intraaxonal injections of horseradish peroxidase in fibers whose receptive field had been identified. The terminal arbors of slowly (SA) and rapidly (RA) adapting thalamocortical neurons were often (60 ~) composed of two separated bushes of 300-600 pm in diameter separated by a region of about the same size containing much less terminal ramifications. The bushes were aligned mainly along the mediolateral axis of the brain. It is proposed that this structural feature underlies the RA-SA banding already described in the somatosensory areas by physiologicalexperiments. The fine retinotopic distribution of terminal arbors of geniculate afferents in the visual cortex determines the existence and topographical characteristics of ocular dominance bands 4. These bands altogether with the recently demonstrated glutamic acid decarboxylase columns 3 (GAD columns) appear to be the main structural features that underly the orientation properties of cortical cells. In the primary somatic sensory cortex of cat and monkey, segregation of submodalities have been demonstrated within the cutaneous receptive areas (areas 3b and 1) 1,9. Rapidly adapting (RA) units and slowly adapting (SA) units are grouped in distinct zones and the tangential distribution of these zones forms bands of submodality which are now referred to as RA and SA bands. This type of organization is believed to be the somatosensory counterpart of the ocular dominance bands of the visual areas 9. In a recent paper 7 we have reported that after injections of horseradish peroxidase (HRP) in thalamocortical axons, cells of the ventroposterolateral (VPL) nucleus in cat terminated in different cytoarchitectonic areas according to their receptive field modality. Moreover we have suggested on the basis of the distribution of terminal arbors that the RA-SA bands were generated by the selective cortical distribution of RA and SA thalamic units. In order to get additional observations on the geometry and orientation of the terminal arbors of RA and SA thalamocortical units we used computer reconstruction and rotation of these arborizations. Methods used for intraaxonal injections of HRP, identification of receptive 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
223 fields a n d c y t o a r c h i t e c t o n i c areas have been r e p o r t e d in detail p r e v i o u s l y L Once the t o t a l a r b o r i z a t i o n o f a fiber h a d been fully r e c o n s t r u c t e d from c a m e r a l u c i d a d r a w i n g s o f serial p a r a s a g i t t a l sections ( × 600) it was b r o k e n d o w n into smaller a r b o r s in which b r a n c h p o i n t s a n d e n d segments c o u l d be easily recognized. These small a r b o r s c o n t a i n e d a b o u t 150 b r a n c h p o i n t s a n d e n d segments. There were
\ A ~ 500 pm
V
M ~ 5001Jm
ILL
C
E 0 0 It1 ..1'
A
500~m
P
2,.,
Fig. 1. Computer reconstruction of the thalamocortical arborization of a single VPL neuron which was driven by hair displacement over the external surface of the contralateral forearm (D), A ~-~ P, anteroposterior axis; M ~-~L, mediolateral axis. For the top view representation in C only the terminal ramifications located in layers III and IV were used. The cut-offlevel is shown in A by the dashed line.
224 between 7 and 17 small arbors in the arborization of a single fiber. Each point was then give,n a depth coordinate (z) according to the section on which it was located. The zcoordinates were multiple of 80/~m (the thickness of histological sections). The x-axis corresponded to the antero-posterior plane of sectioning, the y-axis was the axis normal to the pial surface, and the z-axis corresponded to the medio-lateral dimension of the brain. Data were entered into a digital computer (IBM 370/3031) with the use of a large graphic tablet and a graphic terminal. The APL language was used for programming. Programs allowed rotation (around the x-, y- or z-axis) of the entire arborization or of any of its portion. This last possibility was especially useful for top view representations in which only bushes located in layer IV could be examined without the masking effect of ramifications located in layer VI. As reported previously 7 all thalamocortical RA and SA units arborized in areas 3b or 1 and gave terminals in layers VI, IV and in the lower part of layer III. In only 1 case (out of 12) a cutaneous afferent was seen sending a fine axonal branch that reached layer I. This fiber was excited directly by low current stimulation of the VPL nucleus and monosynaptically at a latency of _ 2 ms by stimulation of dorsal column nuclei. By all other aspects this fiber was very similar to those arborizing only in deeper cortical layers so we cannot yet specify which functional characteristics are typical of this superficially projecting fiber. Of these 12 fibers driven by cutaneous stimulation, 7 generated 2 bushes separated by an uninvaded gap. The spatial distribution of the bushes is shown in Figs. 1 and 2 respectively for a RA and a SA unit. These 2 fibers were chosen because their total arborization had been cut normal to the surface and because they represent typical examples of a patchy cortical projection issued from a single afferent axon. The RA fiber in Fig. 1 responded to hair displacement over most of the external surface of the contralateral forearm and projected in the rostral pole of area 1. The total arborization was composed of two plexuses of about 300 #m in layer IV spaced by a gap of about the same size. Both plexuses were aligned along the mediolateral axis of the brain. The SA fiber in Fig. 2 responded tonically with graded responses to light skin pressure on the dorsal and lateral part of the contralateral fifth digit. Computer rotation shows clearly the presence of 2 bushes of about 450 # m spaced by a region of about 350/~m containing much less terminal ramifications. Again both plexuses were aligned along the mediolateial axis of the brain. Other cutaneous afferent fibers having their receptive field localized on digits generated two patches of terminal ramifications. They arborized in the lateral part of the postcruciate sulcus where area 3b curves rostrally around the tip of the cruciate sulcus. In these instances bushes were obliquely oriented with respect to the rostrocaudal and medio-lateral axis of the brain as if they were attempting to maintain their orientation along the long curved axis of cytoarchitectonic areas. The production of 2 separate terminals bushes by a single VPL thalamocortical fiber is not an exceptional phenomenon since it was observed in 60 ~o of the fibers injected. This observation fits well with the patchy focal projections of electrophysiologically defined groupings of thalamic cells on the monkey somatic sensory cortexL Recent studies on the fine somatotopic organization of area S1 in cat 8 and monkeyS, 6 may allow interpretation of the above results. In both species the forelimb and digits
225
A
,
P~-
=A
500pm
.~
M ~
500vm
.
~L
D
ZL P
500vm
,lllllllniimililll'P"'--"ll~li A
2.°¢
Fig. 2. Computer reconstruction of the thalamocortical arborization of a single VPL neuron which was driven tonically by light pressure on the contralateral fifth digit (D). P ~ A, posteroanterior axis; M 4-~ L, mediolateral axis. For the top view representation in C only terminal ramifications located in layers III and IV were used. The cut-off level is shown in A by the dashed line. are represented in r o s t r o - c a u d a l b a n d s o f cortex lying o r t h o g o n a l the cytoarchitectonic b o u n d a r i e s . In a r e a 3b o f the owl m o n k e y , a fine m a p p i n g o f R A a n d S A units has disclosed, within the r e p r e s e n t a t i o n o f the digits, r o s t r o - c a u d a l l y o r i e n t e d b a n d s o f S A units flanked b y b a n d s o f R A units 9. The S A a n d R A b a n d widths v a r y f r o m 200 to 600/~m. Similar d i m e n s i o n s were observed for the t e r m i n a l bushes as well as for the
226 interbush gaps in our results (i.e. 300 to 600 #m). I n the cat a r e a 3b, segregation o f R A a n d S A units is present 1 b u t no m a p p i n g o f s u b m o d a l i t y d i s t r i b u t i o n within a fine grained s o m a t o t o p y has yet been published. I f the type o f o r g a n i z a t i o n observed in m o n k e y were to be extended to the cat it might be p o s t u l a t e d that the gap between the bushes o f R A fibers are occupied b y SA fibers a n d vice-versa. This i n t e r p r e t a t i o n w o u l d be s u p p o r t e d b y the close resemblance between the orientation, size, a n d spacing o f bushes a n d the t o p o g r a p h y o f R A - S A b a n d s disclosed b y physiological experiments. The a u t h o r s t h a n k Mr. M a r c e l Clercq for his technical help, Mr. G. O a k s o n for reading the m a n u s c r i p t a n d Mrs. M. C a r d i n a l for typing it. This study was s u p p o r t e d b y the M R C ( M A 5877). M . D . is a n M R C Scholar.
1 Dykes, R. W., Rasmusson, D. D. and Hoeltzell, P. B., Organization of primary somatosensory cortex in the cat, J. NeurophysioL, 43 (1980) 1527-1546. 2 Friedman, D. P. and Jones, E. G., Focal projection of electrophysiologicallydefined groupings of thalamic cells on the monkey somatic sensory cortex, Brain Research, 191 (1980) 249-252. 3 Hendrickson, A., Hunt, S. and Wu, J. Y., Localization of GABA in the monkey striate cortex, Abstr. Soc. for Neurosci. lOth Annual Meeting, 1980, p. 671. 4 Hubel, D. H. and Weisel, T. N., Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey, J. comp. Neurol., 146 (1972) 421-450. 5 Kaas, J. H., Nelson, R. S., Sur, M., Lin, C. S. and Merzenich, M. M., Multiple representations of the body within primary somatosensory cortex of primates, Science, 204 (1979) 521-523. 6 Kaas, J. H., Nelson, R. J., Sur, M. and Merzenich, M. M., Organization of somatosensory cortex in primates. In F. O. Schmitt, F. G. Werden, G. Adelman and S. G. Dennis (Eds.), The Organization of the Cerebral Cortex, MIT Press, Cambridge, MA, 1981, pp. 237-261. 7 Landry, P. and Desch6nes, M., Intracortical arborization and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat, J. comp. Neurol., t99 (1981) 345-371. 8 McKenna, T. M., Whitzel, B. L., Dreyer, D. A. and Metz, C. B., Organization of cat anterior parietal cortex: relations among cytoarchitecture, single neuron functional properties, and interhemispheric connectivity, J. Neurophysiol., 45 (1981) 667-697. 9 Sur, M., Wall, J. T. and Kaas, J. H., Modular segregation of functional cell classes within the postcentral somatosensory cortex of monkeys, Science, 212 (1981) 1059-1061.
Brain Research, 237 (1982) 222-226
Elsevier Biomedical Press
Geometry and orientation of thalamocorti,cal arborizations in the cat somatosensory cortex as revealed by computer reconstruction
PIERRE LANDRY, JEAN VILLEMURE and MARTIN DESCHENES Laboratoire de Neurophysiologie, Ddpartement de Physiologie et Centre de Traitement de l'lnformation, Universitd Laval, Quebec, G1K 7P4 (Canada)
(Accepted December 17th, 1981) Key words: area S1 - - thalamocortical arbors - - cortical columns - - somatotopy
The geometry of the intracortical arborization of single neurons from the ventroposterolateral thalamic nucleus in cat was studied with computer reconstruction after intraaxonal injections of horseradish peroxidase in fibers whose receptive field had been identified. The terminal arbors of slowly (SA) and rapidly (RA) adapting thalamocortical neurons were often (60 ~) composed of two separated bushes of 300-600 pm in diameter separated by a region of about the same size containing much less terminal ramifications. The bushes were aligned mainly along the mediolateral axis of the brain. It is proposed that this structural feature underlies the RA-SA banding already described in the somatosensory areas by physiologicalexperiments. The fine retinotopic distribution of terminal arbors of geniculate afferents in the visual cortex determines the existence and topographical characteristics of ocular dominance bands 4. These bands altogether with the recently demonstrated glutamic acid decarboxylase columns 3 (GAD columns) appear to be the main structural features that underly the orientation properties of cortical cells. In the primary somatic sensory cortex of cat and monkey, segregation of submodalities have been demonstrated within the cutaneous receptive areas (areas 3b and 1) 1,9. Rapidly adapting (RA) units and slowly adapting (SA) units are grouped in distinct zones and the tangential distribution of these zones forms bands of submodality which are now referred to as RA and SA bands. This type of organization is believed to be the somatosensory counterpart of the ocular dominance bands of the visual areas 9. In a recent paper 7 we have reported that after injections of horseradish peroxidase (HRP) in thalamocortical axons, cells of the ventroposterolateral (VPL) nucleus in cat terminated in different cytoarchitectonic areas according to their receptive field modality. Moreover we have suggested on the basis of the distribution of terminal arbors that the RA-SA bands were generated by the selective cortical distribution of RA and SA thalamic units. In order to get additional observations on the geometry and orientation of the terminal arbors of RA and SA thalamocortical units we used computer reconstruction and rotation of these arborizations. Methods used for intraaxonal injections of HRP, identification of receptive 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
223 fields a n d c y t o a r c h i t e c t o n i c areas have been r e p o r t e d in detail p r e v i o u s l y L Once the t o t a l a r b o r i z a t i o n o f a fiber h a d been fully r e c o n s t r u c t e d from c a m e r a l u c i d a d r a w i n g s o f serial p a r a s a g i t t a l sections ( × 600) it was b r o k e n d o w n into smaller a r b o r s in which b r a n c h p o i n t s a n d e n d segments c o u l d be easily recognized. These small a r b o r s c o n t a i n e d a b o u t 150 b r a n c h p o i n t s a n d e n d segments. There were
\ A ~ 500 pm
V
M ~ 5001Jm
ILL
C
E 0 0 It1 ..1'
A
500~m
P
2,.,
Fig. 1. Computer reconstruction of the thalamocortical arborization of a single VPL neuron which was driven by hair displacement over the external surface of the contralateral forearm (D), A ~-~ P, anteroposterior axis; M ~-~L, mediolateral axis. For the top view representation in C only the terminal ramifications located in layers III and IV were used. The cut-offlevel is shown in A by the dashed line.
224 between 7 and 17 small arbors in the arborization of a single fiber. Each point was then give,n a depth coordinate (z) according to the section on which it was located. The zcoordinates were multiple of 80/~m (the thickness of histological sections). The x-axis corresponded to the antero-posterior plane of sectioning, the y-axis was the axis normal to the pial surface, and the z-axis corresponded to the medio-lateral dimension of the brain. Data were entered into a digital computer (IBM 370/3031) with the use of a large graphic tablet and a graphic terminal. The APL language was used for programming. Programs allowed rotation (around the x-, y- or z-axis) of the entire arborization or of any of its portion. This last possibility was especially useful for top view representations in which only bushes located in layer IV could be examined without the masking effect of ramifications located in layer VI. As reported previously 7 all thalamocortical RA and SA units arborized in areas 3b or 1 and gave terminals in layers VI, IV and in the lower part of layer III. In only 1 case (out of 12) a cutaneous afferent was seen sending a fine axonal branch that reached layer I. This fiber was excited directly by low current stimulation of the VPL nucleus and monosynaptically at a latency of _ 2 ms by stimulation of dorsal column nuclei. By all other aspects this fiber was very similar to those arborizing only in deeper cortical layers so we cannot yet specify which functional characteristics are typical of this superficially projecting fiber. Of these 12 fibers driven by cutaneous stimulation, 7 generated 2 bushes separated by an uninvaded gap. The spatial distribution of the bushes is shown in Figs. 1 and 2 respectively for a RA and a SA unit. These 2 fibers were chosen because their total arborization had been cut normal to the surface and because they represent typical examples of a patchy cortical projection issued from a single afferent axon. The RA fiber in Fig. 1 responded to hair displacement over most of the external surface of the contralateral forearm and projected in the rostral pole of area 1. The total arborization was composed of two plexuses of about 300 #m in layer IV spaced by a gap of about the same size. Both plexuses were aligned along the mediolateral axis of the brain. The SA fiber in Fig. 2 responded tonically with graded responses to light skin pressure on the dorsal and lateral part of the contralateral fifth digit. Computer rotation shows clearly the presence of 2 bushes of about 450 # m spaced by a region of about 350/~m containing much less terminal ramifications. Again both plexuses were aligned along the mediolateial axis of the brain. Other cutaneous afferent fibers having their receptive field localized on digits generated two patches of terminal ramifications. They arborized in the lateral part of the postcruciate sulcus where area 3b curves rostrally around the tip of the cruciate sulcus. In these instances bushes were obliquely oriented with respect to the rostrocaudal and medio-lateral axis of the brain as if they were attempting to maintain their orientation along the long curved axis of cytoarchitectonic areas. The production of 2 separate terminals bushes by a single VPL thalamocortical fiber is not an exceptional phenomenon since it was observed in 60 ~o of the fibers injected. This observation fits well with the patchy focal projections of electrophysiologically defined groupings of thalamic cells on the monkey somatic sensory cortexL Recent studies on the fine somatotopic organization of area S1 in cat 8 and monkeyS, 6 may allow interpretation of the above results. In both species the forelimb and digits
225
A
,
P~-
=A
500pm
.~
M ~
500vm
.
~L
D
ZL P
500vm
,lllllllniimililll'P"'--"ll~li A
2.°¢
Fig. 2. Computer reconstruction of the thalamocortical arborization of a single VPL neuron which was driven tonically by light pressure on the contralateral fifth digit (D). P ~ A, posteroanterior axis; M 4-~ L, mediolateral axis. For the top view representation in C only terminal ramifications located in layers III and IV were used. The cut-off level is shown in A by the dashed line. are represented in r o s t r o - c a u d a l b a n d s o f cortex lying o r t h o g o n a l the cytoarchitectonic b o u n d a r i e s . In a r e a 3b o f the owl m o n k e y , a fine m a p p i n g o f R A a n d S A units has disclosed, within the r e p r e s e n t a t i o n o f the digits, r o s t r o - c a u d a l l y o r i e n t e d b a n d s o f S A units flanked b y b a n d s o f R A units 9. The S A a n d R A b a n d widths v a r y f r o m 200 to 600/~m. Similar d i m e n s i o n s were observed for the t e r m i n a l bushes as well as for the
226 interbush gaps in our results (i.e. 300 to 600 #m). I n the cat a r e a 3b, segregation o f R A a n d S A units is present 1 b u t no m a p p i n g o f s u b m o d a l i t y d i s t r i b u t i o n within a fine grained s o m a t o t o p y has yet been published. I f the type o f o r g a n i z a t i o n observed in m o n k e y were to be extended to the cat it might be p o s t u l a t e d that the gap between the bushes o f R A fibers are occupied b y SA fibers a n d vice-versa. This i n t e r p r e t a t i o n w o u l d be s u p p o r t e d b y the close resemblance between the orientation, size, a n d spacing o f bushes a n d the t o p o g r a p h y o f R A - S A b a n d s disclosed b y physiological experiments. The a u t h o r s t h a n k Mr. M a r c e l Clercq for his technical help, Mr. G. O a k s o n for reading the m a n u s c r i p t a n d Mrs. M. C a r d i n a l for typing it. This study was s u p p o r t e d b y the M R C ( M A 5877). M . D . is a n M R C Scholar.
1 Dykes, R. W., Rasmusson, D. D. and Hoeltzell, P. B., Organization of primary somatosensory cortex in the cat, J. NeurophysioL, 43 (1980) 1527-1546. 2 Friedman, D. P. and Jones, E. G., Focal projection of electrophysiologicallydefined groupings of thalamic cells on the monkey somatic sensory cortex, Brain Research, 191 (1980) 249-252. 3 Hendrickson, A., Hunt, S. and Wu, J. Y., Localization of GABA in the monkey striate cortex, Abstr. Soc. for Neurosci. lOth Annual Meeting, 1980, p. 671. 4 Hubel, D. H. and Weisel, T. N., Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey, J. comp. Neurol., 146 (1972) 421-450. 5 Kaas, J. H., Nelson, R. S., Sur, M., Lin, C. S. and Merzenich, M. M., Multiple representations of the body within primary somatosensory cortex of primates, Science, 204 (1979) 521-523. 6 Kaas, J. H., Nelson, R. J., Sur, M. and Merzenich, M. M., Organization of somatosensory cortex in primates. In F. O. Schmitt, F. G. Werden, G. Adelman and S. G. Dennis (Eds.), The Organization of the Cerebral Cortex, MIT Press, Cambridge, MA, 1981, pp. 237-261. 7 Landry, P. and Desch6nes, M., Intracortical arborization and receptive fields of identified ventrobasal thalamocortical afferents to the primary somatic sensory cortex in the cat, J. comp. Neurol., t99 (1981) 345-371. 8 McKenna, T. M., Whitzel, B. L., Dreyer, D. A. and Metz, C. B., Organization of cat anterior parietal cortex: relations among cytoarchitecture, single neuron functional properties, and interhemispheric connectivity, J. Neurophysiol., 45 (1981) 667-697. 9 Sur, M., Wall, J. T. and Kaas, J. H., Modular segregation of functional cell classes within the postcentral somatosensory cortex of monkeys, Science, 212 (1981) 1059-1061.