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The laminar arrangement of limbic thalamocortical neurons in the lateropulvinar nuclei of the cat thalamus
JVmmmx'imeeLetters. 38 (1983) 215-219 Ehevier Scieatific Publishers Ireland Ltd.
215
TilE LAMINAig AERANGEMENT OF LIMBIC THALAMOCORTICAL NEUEON$ IN THE LA'gEEOIqJLVINAR NUCLEI OF THE CAT TEIALAMUS
K. NIIMI, M. NIIMI, H. MATSUOKA, M. YANAGIHARA and T. KATAYAMA
Third Department of Anatomy, Okayama University Medical School, Okoyama 700 (Japan) (P___e~_'ved March 24th, 1983; Revised version received and accepted April 25th, 191~.~)
Key words: cat - horseradish peroxidase - lateropulvinar nuclei - limbic system - thalamus thalamocortical neurons
The topical orsanization of limbic conical projections of the lateropulvinar nuclei of the thalamus in the cat was studied with the horseradish peroxidase (HRP~ technique. The dorsal marsins of the dorsal lateral, medial pulvinar and lateral pulvinar nuclei project to the postsubicular and presubicular areas (presubiculum in a wide sense), the most dorsal paris of these nuclei projecting to the retrmplenial area, and the dorsal parts to the cinjular area. These three zones of limbic thalamocoriical neurons in the lateropulvinar nuclei are arranged in lamination from the surface inward, and may be called prembieular, retrmplenial and cingular zones.
The limbic cortex receives fibers largely from the anterior thalamic nuclei, but a few fibers come from the dorsal lateral, medial pulvinar and lateral pulvinar nuclei [ 10]. The present study attempts to clarify the topographical organization of the cortical projections of these lateropulvinar nuclei to the limbic cortex. In the limbic cortex of 22 cats, injections of 0.1 d of S0% HRP in 0.9% saline were made stereotaxically or manually with a Hamilton microsyringe under general anesthesia (Nembutal 35-40 mg/kg, i.p.) (Fig. I). After 48 h the animals were perfused transcardially with 2.5% glutaraldehyde and 0.5% paraformaldehyde. Frozen sections were treated for peroxidase reaction by either the diaminobenzidine method of LaVail et al. [2] or the tetramethylbenzidine method of Mesulam [4]. The limbic conical areas were defined, for the most part, according to the cytoarchitectural study of Rose and Woolsey [I I] in the cat. The thalamic nuclei were classified and named following Niimi and Kuwahara [7]. Injections of HRP into the anterior limbic region resulted in no labeling of cells in the lateropulvinar group of the thalamus. On the contrary, a considerable number of labeled cells were found in the dorsal lateral, medial pulvinar and lateral pulvinar nuclei following injections of HRP into the posterior limbic region (Figs. 2 and 3). Injections of HRP into the postsubicular and presubicular areas (presubiculum in 0~4-3940/S3/$ 0~.00 © 1983 Elsevier Scientific Publishers Ireland Lid.
216
a wide sense) led to abundam labeling o f cells in the anterior ¢xu'emby ,qd d z dorsal mmgin of tl~ lateral dorsal nuclcm and in tl~ dorsal border o.e d • medial and later~ ~ nuclei (cats 4R, 6R, SR and 20L). F o l l o w ~ injeetimm of HRP imo the nmmplmial area, many ~ ceBs w e ~ seen in the mint dorsal zones of the dmsal Immal, medial pulvinar and Imeml
pulvinar nuclei (cats 71., 7R, 18R, 191., 19R and 412L). In cat ISR scarcely any labeled cells were seen in the anterior thalami¢ nuclei, but a large numher o f labeled c¢11s were detected in the d o n m l m ~ pans of the above-memioned lateropulvin~ nuclei. Injections of H R P into the ¢ingular area, except for its antefim' portion, save rise to labeted cells in the dorsal zones o f the lateral donml nucleus and of the medial
and lateral pulvinar nuclei (cats 121., 21L0 21R0 25R, 494L, $15L and $15R). In cats 21L, 21R and 25R, where injections involved the lower bank and fundus of the splenial sulcus, a few labeled cells were found in the dorsal part of the posterior lateral nucleus. The above results show that the three transverse bands of labeled cells were arranged from the surface inward in the dorsal parts of the dorsal lateral nucleus and of the medial and lateral pulvinar nuclei. The dorsal maqgins of these nuclei project to the postsubicular and presubicular areas, the most dorsal zones to the retrosplenial area, and the domd zones to the cinlgular area. These three areas are arranged in layers and may be called the presubicular, retrmplcnial and cingular zones (a, b and c in F i p . 2 and 3).
It has been demonstrated by the Nauta method that the dorsal lateral nucleus projeers to the cinlgular and suprasylvian cortices, and the pulvinar nuclei to the
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Fig. I. Diagram to show the site of HRP injections drawn on a standardized oudine of the Icf! medial cortex in all the cats studied, in this figure cortical injections made in either or both left and right cerebral hemispher~ are all depicted on the left hemisphere to facilitate comparison. The numbers with L (left) or R (right) are cat numbers. The banks of sulci are indicated by areas lying close to the sulci. Cg, cingular area; LA, anterior limbic region; Pr, prcsubicular area; Ps, poslsubicular area; Rs, rctrosplenial area.
217
A
Fig. 2. The distribution of labeled cells in the dorsal lateral nucleus (B and C) of the thalamus following injections of HRP into the limbic cortex (A). In A, abbreviations of the limbic conex are same as in Fig. I. In C, three zones of limbic neurons in the dorsal lateral nucleus are indicated by a, b and c (presubicular, rctrosplenial and cinlgular zones). AD, amerodorsal nucleus; AM, anteromedial nucleus; AV, anterovcmral nucleus; CL, lateral central nucleus; LD, dorsal lateral nucleus; LP, posterior lateral nucleus; MD, dorsal medial nucleus. VA, ventral anterior nucleus; VL, ventral lateral nucleus.
2111
mprmylvim runes and the amex within the ~ mlcus 11, 3, ~, 61. N',im, m al. II0]. mini the HI~P method, ferruled that the Imslerior limbi¢ regiom reoeive fibem from the dorsal pans of the dorsal Imeral, medial pulvimmr and Imeml pulvimr nuclei. The presem study f u m ~ dmmomumed the ~ ~ of these projectimm, it is of interest to note that lhe cemml and vemml pints of these
lateropulvinar nuclei project to the anterior and middle mpmsylvin Ipjri and the anterior lateral gyms in a t ~ manner [8, 9J.
%.
rip. 9. The distribution ot labeled cells (A and B) in the medial and Zatcral pulvinar nuclei in the cat following injcctions of HRP inlo thc limbic c m l ~ (see Fig: 2A). Three zones of limbi¢ neurons in Ihe pulvinar nuclei are rq)r~,enlcd by a. b. and c (pmsubicular. r~rosplenial and cinl~,~r zones). CD. dor~l ccmral nucleus; CeM. centre m~'dian nucleus; CL. lazaal cemral nucleus; t';L. lataal geniculam nucleus; MI). dorsal medial nucleus; PL. lalcral pulvinar nuclms; PMD. nmdial p:llvinar nucleus, pars doro solatcralis; PMM. medial pulvinar nucleus, pars mcdialis; PMY. medial pulvinar nucleus, pars vcnIrolateralis; Sg, nucleus suprageniculalus.
219 I~ , A.M., Some ascendinig cotumctio~ of the puivinar and nucleus lateralis posterior of the ,halamus in the cat, Brain Res., 44 (1972) 99-12~. 2 LaVnd, J.H., W'umone, R.R. and "Fish, A., A m.-thod based on retrograde intra-axonal transport of protein for identification of cg~ bodies of oriLvn of axons terminating within the central ,tervous • j ~ m , Brain Itm., ~1 ( 1 9 ' ~ 4 7 0 - 4 ~ . 3 locke, S., And, vine, J.B., Jr. and Yakovlev, P.i., Limbic nuclei of thalamus and connections of limbig cortex. VI. Thalmsm-cmtiml projection of lateral dorsal nucleus in cat and monkey, Arch. Neurol., II (1964) 1-12. 4 Mesulam, M.-M,, Tetramethyl benzidi~ for horseradbh peroxidase neurohistochemistry: a noncarcinolgnic blue reaction-product with s u ~ sensibility for visualizing neural afferents and efferents, J. Histochem, Cytochem., 26 (1978) 106-11"/. 5 Niimi, K, and Inmihita, H., Cortical projections of the lateral thalamic nuclei in the cat, Proc. Jap. Acad., 47 (1971) 664-¢m9. 6 Miimi0 K,, Kadota, M. and Matsushita. Y., Conical projections of the pulvinar nuclear group of the thalamus in the cat, Brain Behav. Evol,, 9 (1974) 422-457. "/Niimi, K. and Kuwahma, E,, The dorsal thalamus of the cat and comparison with monkey and man, J. Himforsch., 14 (1973) 303 -326. 8 Niimi, K,, Matsuoka, H. and Matsumoto, H., Thalamic affcrents to the anterior part of the lateral fpjrus in the cat studied by retrograde axonal transport of horseraflish pcroxidase, Proc. ,lap, Acad., 55 (1979) I-$, 9 Niimi, K,, Matsuoka, 14,, Yamazaki, Y, and Katayama, T,, Thalamic afferents to the anterior and middle suprasylvian 8yri in the cat traced with horseradish peroxidase. J, Hirnforsch., in press. tO Niimi. K,, Niimi, M. and Okada, Y,, Thalamic afferent$ to the limbic cortex in the cat ~tudied with the method of retrolgrade axonal transport of horseradi.qh peroxidase, Brain Res., 145 (1971) 2~-231¢. t I Rose, J,E, and Woolx'y, C,N,. Structure and relations of limbic cortex and anterior thalami¢ nuclei in rabbit and cat, J. comp, Neurol,, 119 (1948) 2"/9-348,
215
TilE LAMINAig AERANGEMENT OF LIMBIC THALAMOCORTICAL NEUEON$ IN THE LA'gEEOIqJLVINAR NUCLEI OF THE CAT TEIALAMUS
K. NIIMI, M. NIIMI, H. MATSUOKA, M. YANAGIHARA and T. KATAYAMA
Third Department of Anatomy, Okayama University Medical School, Okoyama 700 (Japan) (P___e~_'ved March 24th, 1983; Revised version received and accepted April 25th, 191~.~)
Key words: cat - horseradish peroxidase - lateropulvinar nuclei - limbic system - thalamus thalamocortical neurons
The topical orsanization of limbic conical projections of the lateropulvinar nuclei of the thalamus in the cat was studied with the horseradish peroxidase (HRP~ technique. The dorsal marsins of the dorsal lateral, medial pulvinar and lateral pulvinar nuclei project to the postsubicular and presubicular areas (presubiculum in a wide sense), the most dorsal paris of these nuclei projecting to the retrmplenial area, and the dorsal parts to the cinjular area. These three zones of limbic thalamocoriical neurons in the lateropulvinar nuclei are arranged in lamination from the surface inward, and may be called prembieular, retrmplenial and cingular zones.
The limbic cortex receives fibers largely from the anterior thalamic nuclei, but a few fibers come from the dorsal lateral, medial pulvinar and lateral pulvinar nuclei [ 10]. The present study attempts to clarify the topographical organization of the cortical projections of these lateropulvinar nuclei to the limbic cortex. In the limbic cortex of 22 cats, injections of 0.1 d of S0% HRP in 0.9% saline were made stereotaxically or manually with a Hamilton microsyringe under general anesthesia (Nembutal 35-40 mg/kg, i.p.) (Fig. I). After 48 h the animals were perfused transcardially with 2.5% glutaraldehyde and 0.5% paraformaldehyde. Frozen sections were treated for peroxidase reaction by either the diaminobenzidine method of LaVail et al. [2] or the tetramethylbenzidine method of Mesulam [4]. The limbic conical areas were defined, for the most part, according to the cytoarchitectural study of Rose and Woolsey [I I] in the cat. The thalamic nuclei were classified and named following Niimi and Kuwahara [7]. Injections of HRP into the anterior limbic region resulted in no labeling of cells in the lateropulvinar group of the thalamus. On the contrary, a considerable number of labeled cells were found in the dorsal lateral, medial pulvinar and lateral pulvinar nuclei following injections of HRP into the posterior limbic region (Figs. 2 and 3). Injections of HRP into the postsubicular and presubicular areas (presubiculum in 0~4-3940/S3/$ 0~.00 © 1983 Elsevier Scientific Publishers Ireland Lid.
216
a wide sense) led to abundam labeling o f cells in the anterior ¢xu'emby ,qd d z dorsal mmgin of tl~ lateral dorsal nuclcm and in tl~ dorsal border o.e d • medial and later~ ~ nuclei (cats 4R, 6R, SR and 20L). F o l l o w ~ injeetimm of HRP imo the nmmplmial area, many ~ ceBs w e ~ seen in the mint dorsal zones of the dmsal Immal, medial pulvinar and Imeml
pulvinar nuclei (cats 71., 7R, 18R, 191., 19R and 412L). In cat ISR scarcely any labeled cells were seen in the anterior thalami¢ nuclei, but a large numher o f labeled c¢11s were detected in the d o n m l m ~ pans of the above-memioned lateropulvin~ nuclei. Injections of H R P into the ¢ingular area, except for its antefim' portion, save rise to labeted cells in the dorsal zones o f the lateral donml nucleus and of the medial
and lateral pulvinar nuclei (cats 121., 21L0 21R0 25R, 494L, $15L and $15R). In cats 21L, 21R and 25R, where injections involved the lower bank and fundus of the splenial sulcus, a few labeled cells were found in the dorsal part of the posterior lateral nucleus. The above results show that the three transverse bands of labeled cells were arranged from the surface inward in the dorsal parts of the dorsal lateral nucleus and of the medial and lateral pulvinar nuclei. The dorsal maqgins of these nuclei project to the postsubicular and presubicular areas, the most dorsal zones to the retrosplenial area, and the domd zones to the cinlgular area. These three areas are arranged in layers and may be called the presubicular, retrmplcnial and cingular zones (a, b and c in F i p . 2 and 3).
It has been demonstrated by the Nauta method that the dorsal lateral nucleus projeers to the cinlgular and suprasylvian cortices, and the pulvinar nuclei to the
~ee.-~. v C4 l m . , / . ~ . . a - . . . . S,Se iSa w /...---s,-~ . . . . . . . . . //
~s
T
---
L:.:'....:i-t'~,," --'" ! 3
.
~
".._.~',~,.._
~=.
~ , ~j~o ;
..... •
............... "', v
-
,
M t" -Db. e
-:
~ "..
:
N
Fig. I. Diagram to show the site of HRP injections drawn on a standardized oudine of the Icf! medial cortex in all the cats studied, in this figure cortical injections made in either or both left and right cerebral hemispher~ are all depicted on the left hemisphere to facilitate comparison. The numbers with L (left) or R (right) are cat numbers. The banks of sulci are indicated by areas lying close to the sulci. Cg, cingular area; LA, anterior limbic region; Pr, prcsubicular area; Ps, poslsubicular area; Rs, rctrosplenial area.
217
A
Fig. 2. The distribution of labeled cells in the dorsal lateral nucleus (B and C) of the thalamus following injections of HRP into the limbic cortex (A). In A, abbreviations of the limbic conex are same as in Fig. I. In C, three zones of limbic neurons in the dorsal lateral nucleus are indicated by a, b and c (presubicular, rctrosplenial and cinlgular zones). AD, amerodorsal nucleus; AM, anteromedial nucleus; AV, anterovcmral nucleus; CL, lateral central nucleus; LD, dorsal lateral nucleus; LP, posterior lateral nucleus; MD, dorsal medial nucleus. VA, ventral anterior nucleus; VL, ventral lateral nucleus.
2111
mprmylvim runes and the amex within the ~ mlcus 11, 3, ~, 61. N',im, m al. II0]. mini the HI~P method, ferruled that the Imslerior limbi¢ regiom reoeive fibem from the dorsal pans of the dorsal Imeral, medial pulvimmr and Imeml pulvimr nuclei. The presem study f u m ~ dmmomumed the ~ ~ of these projectimm, it is of interest to note that lhe cemml and vemml pints of these
lateropulvinar nuclei project to the anterior and middle mpmsylvin Ipjri and the anterior lateral gyms in a t ~ manner [8, 9J.
%.
rip. 9. The distribution ot labeled cells (A and B) in the medial and Zatcral pulvinar nuclei in the cat following injcctions of HRP inlo thc limbic c m l ~ (see Fig: 2A). Three zones of limbi¢ neurons in Ihe pulvinar nuclei are rq)r~,enlcd by a. b. and c (pmsubicular. r~rosplenial and cinl~,~r zones). CD. dor~l ccmral nucleus; CeM. centre m~'dian nucleus; CL. lazaal cemral nucleus; t';L. lataal geniculam nucleus; MI). dorsal medial nucleus; PL. lalcral pulvinar nuclms; PMD. nmdial p:llvinar nucleus, pars doro solatcralis; PMM. medial pulvinar nucleus, pars mcdialis; PMY. medial pulvinar nucleus, pars vcnIrolateralis; Sg, nucleus suprageniculalus.
219 I~ , A.M., Some ascendinig cotumctio~ of the puivinar and nucleus lateralis posterior of the ,halamus in the cat, Brain Res., 44 (1972) 99-12~. 2 LaVnd, J.H., W'umone, R.R. and "Fish, A., A m.-thod based on retrograde intra-axonal transport of protein for identification of cg~ bodies of oriLvn of axons terminating within the central ,tervous • j ~ m , Brain Itm., ~1 ( 1 9 ' ~ 4 7 0 - 4 ~ . 3 locke, S., And, vine, J.B., Jr. and Yakovlev, P.i., Limbic nuclei of thalamus and connections of limbig cortex. VI. Thalmsm-cmtiml projection of lateral dorsal nucleus in cat and monkey, Arch. Neurol., II (1964) 1-12. 4 Mesulam, M.-M,, Tetramethyl benzidi~ for horseradbh peroxidase neurohistochemistry: a noncarcinolgnic blue reaction-product with s u ~ sensibility for visualizing neural afferents and efferents, J. Histochem, Cytochem., 26 (1978) 106-11"/. 5 Niimi, K, and Inmihita, H., Cortical projections of the lateral thalamic nuclei in the cat, Proc. Jap. Acad., 47 (1971) 664-¢m9. 6 Miimi0 K,, Kadota, M. and Matsushita. Y., Conical projections of the pulvinar nuclear group of the thalamus in the cat, Brain Behav. Evol,, 9 (1974) 422-457. "/Niimi, K. and Kuwahma, E,, The dorsal thalamus of the cat and comparison with monkey and man, J. Himforsch., 14 (1973) 303 -326. 8 Niimi, K,, Matsuoka, H. and Matsumoto, H., Thalamic affcrents to the anterior part of the lateral fpjrus in the cat studied by retrograde axonal transport of horseraflish pcroxidase, Proc. ,lap, Acad., 55 (1979) I-$, 9 Niimi, K,, Matsuoka, 14,, Yamazaki, Y, and Katayama, T,, Thalamic afferents to the anterior and middle suprasylvian 8yri in the cat traced with horseradish peroxidase. J, Hirnforsch., in press. tO Niimi. K,, Niimi, M. and Okada, Y,, Thalamic afferent$ to the limbic cortex in the cat ~tudied with the method of retrolgrade axonal transport of horseradi.qh peroxidase, Brain Res., 145 (1971) 2~-231¢. t I Rose, J,E, and Woolx'y, C,N,. Structure and relations of limbic cortex and anterior thalami¢ nuclei in rabbit and cat, J. comp, Neurol,, 119 (1948) 2"/9-348,