Brain Research, 90 (1975) 139-142
139
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
The laminar organization of certain afferent and efferent fiber systems in the rat somatosensory cortex
STEVEN P. WISE Department of Anatomy, Washington University, School of Medic#le, St. Louis, Mo. 63110 (U.S.A.)
(Accepted February 26th, 1975)
An investigation of the somatic sensory cortex of the albino rat was undertaken to determine the laminar distribution of certain of its afferent fibers and the cells of origin of some of its efferent projections. In the first part of the study, the terminal distributions of commissural and thalamocortical fibers were examined using the autoradiographic method 1. These afferent fiber systems have different laminar patterns of termination (Fig. 1). The commissural fibers enter the homotopic cortex in a bundle which ascends through all laminae and gives rise to large numbers of terminals in the supragranular layers and in a part of layer V, but gives very few terminals to the granular layer (layer IV, Fig. Ic). By contrast, the thalamocortical fibers terminate mostly in layer IV and to a lesser extent in a deep portion of layer V (Fig. ld). In the second part of the study, the laminar organization of the cells of the first (SI) and the second (SII) somatosensory areas which project to the contralateral cortex, to the ventrobasal complex of the thalamus, and to the dorsal column nuclei of the medulla were examined. Single or multiple injections of type VI horseradish peroxidase (HRP, Sigma) in concentrations of 500 #g/#l were made in SI, in the thalamus, or in the dorsal column nuclei. After 1-3 days, the animals were perfused with 0 a.-,--..u/;An'~ paraformaldehyde and 1.25~i glutaraldehyde in 0.1 M phosphate buffer and 50 p m frozen sections were treated according to the method of LaVail et al. 4. Commivsural projection. Injections of H R P in S1 lead to retrograde labeling of cells in a site homotopic to the injection. The cells of origin of the commissural fibers are found in all layers of the opposite SI with the exception of layer 1 (Fig. l b), but they are concentrated in layers III and V (see ref. 2). The cells most heavily labeled are medium to large pyramidal cells located throughout layers Ill and V. Fewer HRP-positive cells are found in layer II, although these are also heavily labeled. In all cases where heavily labeled cells are found, others with less intense staining are seen in close proximity to them. A few lightly labeled pyramidal cells are also found in layer IV and at the border of V and VI, but no labeled neurons appear in the rest of layer VI.
Fig. I. a: bright-field photomicl~ograph I~rom a palall~n s0ction o f SL T h i o n i n ~au~,
7t~
: ,[a/'~
field p h o t o m i c r o g r a p h of labeled cells in SI [*ollowing an in.jection of the couuuiatcral S I ~i) c: dark-field p h o t o m i c r o g r a p h from an a u t o r a d i o g r a p h s h o w i n g labeling ol c o m m i s s u r a l ~ii',c~,, and terminals in SI. Note the relative lack of ~,ilver grains over l~ycr IV and pa~i of la>el \ ;! d: p h o t o m i c r o g r a p h of an a u t o r a d i o g r a p h shox~ing the distribution of thalanlocn!'~ical lern.iii:~d,. :~ ~I
~/~i
d
it
a
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i
Fig. 2. a a n d b: bright- a n d dark-field p h o t o m i c r o g r a p h s s h o w i n g cells in layer VB of the face representation of S! following an injection of the contralateral trigeminal and dorsal c o l u m n nuclei. T h e blood vessel m a r k e d x is the s a m e in each p h o t o m i c r o g r a p h , a, ~'< 55, b, × 185. c: H R P labeled cells mainly in layer VI, but with a few in layer VB (arrows) of SII after injection in the ipsilateral t h a l a m u s . 130. d: H R P labeled cells in layer VB of SI, s a m e section from which Fig. 2c was t a k e n . . : 240.
142
Corticothalamic projection. I n j e c t i o n s o f H R P i n t o t h e t h a l a m u s w h i c h irlvolvc the ventrobasal complex result in labeling of many infragranular, but no supragranufar cells (see also retd. 3 and 5). The SI corticothalamic projection originates m~stly from the densely populated sublayer, layer VB (Figs. la and 2a). The cells in layer VB are heavily labeled and are medium to large pyramids. In many instances, especially near the border of SI and Sll, HRP-positive cells can also be seen in layer VL but they are always more lightly labeled than the cells in layer VB. By contrast, the corticothalamic projection from SII originates primarily in upper layer VI though a few labeled cells also appear in layer VB (Fig. 2c and d). The cells in layer VI of S]I are lightly labeled, but a strikingly large number of cells contain retrogradely tr:~ngported peroxidase (as many as 80'~ii in some areasl. Corlicomedullary projection. The projection of the somatosensory cortex upon the relay nuclei of the medulla has been examined by injection of HRP into lhe cuneate, gracile, and spinal trigeminal nuclei. The cells which project to these structures are found exclusively in a narrow band of layer VB (Fig. 2a and b). The labeled neurons are large pyramidal cells and there appears to be no difference between SI and Sll in their laminar distribution. It is not yet known whether single cells of the somatosensory cortex project only to one or, by means of axonal branches, to more than one location. However, certain possibilities seem to be excluded by these data. Few SI1 cells appear to project to both the thalamus and the medulla since most of these fibers originate from distinct cortical laminae. Further, none of the supragranular, commissurally projecting cells or those from layer VA seem to project to any of the subcortical loci examined. The other projections of the somatosensory cortex remain to be investigated, e.g., those to the pontine nuclei, superior colliculus, and spinal cord and to the contralateral SII. Furthermore, there may be considerable differences in the organization of these connections in different species. For example, preliminary data in the cat and squirrel monkey indicate that the commissural projection in these animals originates exclusively from one of the supragranular layers, layer IlIB, which is quite different from our findings in the rat in which the corresponding projection arises from layers 11, I l i A . and V, as well as layer IIIB. S u p p o r t e d by G r a n t s N S 10526 and 1 T0I E Y 0 0 0 2 4 f r o m t h e N a t i o n a l I n s t i t u t e s of Health, U.S.P.HS. 1 COWAN, W. M., GOTTLIEB, D. 1., HENDRICKSON, A. E., PRICE, J. L., AND WOOLSEY, T. A., The autoradiographic demonstration of axonal connections in the central nervous system, Brain Research, 37 (1972) 21 51. 2 JACOBSON, S., AND TROJANOWSKI, J. Q., The cells of origin of the corpus callosum in rat, cat, and rhesus monkey, Brain Research, 74 (1974) 149-155. 3 GILBERT, C., AND KELLY, J. P., The use of peroxidase transport to study the connections of the cat's visual system. In Proc. ofSoc. Neurosci., 4th Annual Meeting, St. Louis, 1974, p. 227. 4 LAVAIL, J. H., WINSTON, K. R., AND T1SH, A., A method based on retrograde intraaxonal transport of protein for identification of cell bodies of axons terminating within the CNS, Brain Research, 58 (1973) 470477. 5 LUND, R. D., LUND, J. S., BUNT, A. H., HENDRICKSON, A. E., AND FUCHS, A. f-., Cells in area 17 of monkey (Macaca mulatta) which give rise to corticotectal and corticogeniculate pathways. In Proc. ~!'Soc. Neurosci., 4th Annual Meethtg, St. Louis, 1974, p. 319.
139
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
The laminar organization of certain afferent and efferent fiber systems in the rat somatosensory cortex
STEVEN P. WISE Department of Anatomy, Washington University, School of Medic#le, St. Louis, Mo. 63110 (U.S.A.)
(Accepted February 26th, 1975)
An investigation of the somatic sensory cortex of the albino rat was undertaken to determine the laminar distribution of certain of its afferent fibers and the cells of origin of some of its efferent projections. In the first part of the study, the terminal distributions of commissural and thalamocortical fibers were examined using the autoradiographic method 1. These afferent fiber systems have different laminar patterns of termination (Fig. 1). The commissural fibers enter the homotopic cortex in a bundle which ascends through all laminae and gives rise to large numbers of terminals in the supragranular layers and in a part of layer V, but gives very few terminals to the granular layer (layer IV, Fig. Ic). By contrast, the thalamocortical fibers terminate mostly in layer IV and to a lesser extent in a deep portion of layer V (Fig. ld). In the second part of the study, the laminar organization of the cells of the first (SI) and the second (SII) somatosensory areas which project to the contralateral cortex, to the ventrobasal complex of the thalamus, and to the dorsal column nuclei of the medulla were examined. Single or multiple injections of type VI horseradish peroxidase (HRP, Sigma) in concentrations of 500 #g/#l were made in SI, in the thalamus, or in the dorsal column nuclei. After 1-3 days, the animals were perfused with 0 a.-,--..u/;An'~ paraformaldehyde and 1.25~i glutaraldehyde in 0.1 M phosphate buffer and 50 p m frozen sections were treated according to the method of LaVail et al. 4. Commivsural projection. Injections of H R P in S1 lead to retrograde labeling of cells in a site homotopic to the injection. The cells of origin of the commissural fibers are found in all layers of the opposite SI with the exception of layer 1 (Fig. l b), but they are concentrated in layers III and V (see ref. 2). The cells most heavily labeled are medium to large pyramidal cells located throughout layers Ill and V. Fewer HRP-positive cells are found in layer II, although these are also heavily labeled. In all cases where heavily labeled cells are found, others with less intense staining are seen in close proximity to them. A few lightly labeled pyramidal cells are also found in layer IV and at the border of V and VI, but no labeled neurons appear in the rest of layer VI.
Fig. I. a: bright-field photomicl~ograph I~rom a palall~n s0ction o f SL T h i o n i n ~au~,
7t~
: ,[a/'~
field p h o t o m i c r o g r a p h of labeled cells in SI [*ollowing an in.jection of the couuuiatcral S I ~i) c: dark-field p h o t o m i c r o g r a p h from an a u t o r a d i o g r a p h s h o w i n g labeling ol c o m m i s s u r a l ~ii',c~,, and terminals in SI. Note the relative lack of ~,ilver grains over l~ycr IV and pa~i of la>el \ ;! d: p h o t o m i c r o g r a p h of an a u t o r a d i o g r a p h shox~ing the distribution of thalanlocn!'~ical lern.iii:~d,. :~ ~I
~/~i
d
it
a
/. /-
.gJ
i
Fig. 2. a a n d b: bright- a n d dark-field p h o t o m i c r o g r a p h s s h o w i n g cells in layer VB of the face representation of S! following an injection of the contralateral trigeminal and dorsal c o l u m n nuclei. T h e blood vessel m a r k e d x is the s a m e in each p h o t o m i c r o g r a p h , a, ~'< 55, b, × 185. c: H R P labeled cells mainly in layer VI, but with a few in layer VB (arrows) of SII after injection in the ipsilateral t h a l a m u s . 130. d: H R P labeled cells in layer VB of SI, s a m e section from which Fig. 2c was t a k e n . . : 240.
142
Corticothalamic projection. I n j e c t i o n s o f H R P i n t o t h e t h a l a m u s w h i c h irlvolvc the ventrobasal complex result in labeling of many infragranular, but no supragranufar cells (see also retd. 3 and 5). The SI corticothalamic projection originates m~stly from the densely populated sublayer, layer VB (Figs. la and 2a). The cells in layer VB are heavily labeled and are medium to large pyramids. In many instances, especially near the border of SI and Sll, HRP-positive cells can also be seen in layer VL but they are always more lightly labeled than the cells in layer VB. By contrast, the corticothalamic projection from SII originates primarily in upper layer VI though a few labeled cells also appear in layer VB (Fig. 2c and d). The cells in layer VI of S]I are lightly labeled, but a strikingly large number of cells contain retrogradely tr:~ngported peroxidase (as many as 80'~ii in some areasl. Corlicomedullary projection. The projection of the somatosensory cortex upon the relay nuclei of the medulla has been examined by injection of HRP into lhe cuneate, gracile, and spinal trigeminal nuclei. The cells which project to these structures are found exclusively in a narrow band of layer VB (Fig. 2a and b). The labeled neurons are large pyramidal cells and there appears to be no difference between SI and Sll in their laminar distribution. It is not yet known whether single cells of the somatosensory cortex project only to one or, by means of axonal branches, to more than one location. However, certain possibilities seem to be excluded by these data. Few SI1 cells appear to project to both the thalamus and the medulla since most of these fibers originate from distinct cortical laminae. Further, none of the supragranular, commissurally projecting cells or those from layer VA seem to project to any of the subcortical loci examined. The other projections of the somatosensory cortex remain to be investigated, e.g., those to the pontine nuclei, superior colliculus, and spinal cord and to the contralateral SII. Furthermore, there may be considerable differences in the organization of these connections in different species. For example, preliminary data in the cat and squirrel monkey indicate that the commissural projection in these animals originates exclusively from one of the supragranular layers, layer IlIB, which is quite different from our findings in the rat in which the corresponding projection arises from layers 11, I l i A . and V, as well as layer IIIB. S u p p o r t e d by G r a n t s N S 10526 and 1 T0I E Y 0 0 0 2 4 f r o m t h e N a t i o n a l I n s t i t u t e s of Health, U.S.P.HS. 1 COWAN, W. M., GOTTLIEB, D. 1., HENDRICKSON, A. E., PRICE, J. L., AND WOOLSEY, T. A., The autoradiographic demonstration of axonal connections in the central nervous system, Brain Research, 37 (1972) 21 51. 2 JACOBSON, S., AND TROJANOWSKI, J. Q., The cells of origin of the corpus callosum in rat, cat, and rhesus monkey, Brain Research, 74 (1974) 149-155. 3 GILBERT, C., AND KELLY, J. P., The use of peroxidase transport to study the connections of the cat's visual system. In Proc. ofSoc. Neurosci., 4th Annual Meeting, St. Louis, 1974, p. 227. 4 LAVAIL, J. H., WINSTON, K. R., AND T1SH, A., A method based on retrograde intraaxonal transport of protein for identification of cell bodies of axons terminating within the CNS, Brain Research, 58 (1973) 470477. 5 LUND, R. D., LUND, J. S., BUNT, A. H., HENDRICKSON, A. E., AND FUCHS, A. f-., Cells in area 17 of monkey (Macaca mulatta) which give rise to corticotectal and corticogeniculate pathways. In Proc. ~!'Soc. Neurosci., 4th Annual Meethtg, St. Louis, 1974, p. 319.
