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Projection of precentral motor cortex upon nucleus medialis dorsalis thalami in the monkey
Neuroscience Letters, 11 (1979) 103--106 © Elsevier/North-Holland Scientific Publishers Ltd.
103
PROJECTION OF PRECENTRAL MOTOR CORTEX UPON NUCLEUS MEDIALIS DORSALIS THALAMI IN THE MONKEY
K O N R A D AKERT, K U R T H A R T M A N N - V O N M O N A K O W
and HEINZ K U N Z L E
Brain Research Institute o f the University of Zi~'rich, August Fore!s~asse 1, CH-8029 Zh'rich (Switzerland)
(Received October 26th, 1978) . (Accepted November 2rid, 1978)
SUMMARY
The efferent connections of the lateral aspects of the precentral, premotor and granular frontal cortex were reexamined in 12 monkeys (Macaca fascicular/s) by means of anterograde labelling techniques using radioactive proline and leucine. A distinct projection of the precentral gyrus upon the psxalamellar portion of the nucleus medialis dorsalis (MD) was observed. The somatotopic arrangement within this projection is less well defined than within the ventrolateral thalamic complex. The facial division of area 4 has not only a marked ipsilateral but in contrast to the body representation also a distinct if much weaker contrala~ral projection. No label was found in MD after injections in the postcentral gyrus. Thus, MD represents a thalamic link between agranular (motor) and granular (association) cortex of the frontal lobe.
The relationships between medial thalamus and frontal cortex have been explored experimentally since the pioneering studies of Monakow [9] and Rutishauser [12], and with the advent of more powerful methods these relationships have been gradually refined by numerous subsequent investigators [2,11,13--15]. Akert [1] emphasized the 10xninar organization of thalamic afferents to agranular and granular frontal Brodmann fields with respect to their origin in ventrolateral and mediodorsal nuclear masses respectively. The latter findings have been recently confirmed and extended by Kievit and Kuypers [3] who applied the retrograde axonal flow technique for the demonstration of the remarkable laminar organisation of the thalamo-frontal connections particularly if examined in the horizontal plane. It is generally assumed that cortico-thalamic connections are organized in a reciprocal manner. An important exception to this rule was found recently in the course of systematic investigations of the afferent connections of area 4. In concerns the projections to the mediodorsal nucleus (MD) which heretofore has been
104
regm:ded as the domain of prefrontal connections. These findings will be briefly reported here. The present study was carried out in 12 monkeys (Macaca fascicularis) in which small, circumscribed injections into frontal cortical areas have been made
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Fig. 1. Projection of precentral motor cortex (precentral gyrus) upon the medial thalamic nuclei in the monkey. Note that face, arm and leg areas of the primary motor cortex project not only to centrum medianum (CM) and central lateralis (CL), but also to the adjacent portion of medialis dorsalis (MD). There is a shifting overlap with the face representation (above) extending more ventrally than the leg and arm areas (below). Mag. x15.
105
with radioactive leucine and proline. The procedures have been described in detail elsewhere [4 ] ..and the reconstructions of the injection and uptake sites are also displayed in detail in the same paper. Suffice it here to say that the injections specifically covered the lateral aspects of the precentral gyrus and the typical locations which, according to the electrophysiological maps of Woolsey et al. [16] represent the face, arm and leg areas of the primary motor cortex. Silver grains were traced to various thalamic nuclei, particulaHy to the ventrolateral group and centrum rnedianum [5]. This communication places its main emphasis on terminal and preterminal fields within the medial dorsal nucleus. The projection of area 4 to M D in the monkey 4s surprisingly dense. Its terminal and preterminal field occupies the lateral moiety of M D corresponding approximately to p. multiformis of Olszewski [10] (Fig. 1). The facial projection is particularly heavy and a faint contralateral mirror focus can also be seen (not illustrated). Face, arm and leg representations are characterized by a shifting overlap within a narrow sheath of cells with the face extending rr.ore ventrally than the leg and arm areas (Fig. 1). When compared with the rather distinct projections within the ventrolateral nuclei [5], it seems inevitable to conclude that the somatotopic arrangement in M D is not as clearly defined. Furthermore, an overlap with area 8 and area 6 projections [6,7] is also noted. All these precentral and prernotor areas seem to project within a relatively limited field of M D situated rather closely to the intralarninarnuclei which are additional recipients of frontal lobe connections [6]. This finding is all the more remarkable because reciprocal thalamocortical connections (i.e.from M D to area 4) have thus far not been observed [3 ]. The main and perhaps exclusive cortical target of M D seems to be the so
The skillful assistance of A. F~ih, E. Schneider, D. Savini and H. Hauser is gratefully acknowledged. This work was supported by the Swiss National Science Foundation, grant 3.636.75 and the Stiftung ffir wissenschaftliche Forschung an der Universit~it Zfirich. REFERENCES 1 Akert, K., Comparative anatomy of frontal cortex and thalamo-frontal In J.M. Warren and K. Akert (Eds.), The Frontal Granular Cortex and McGraw-Hill, New York, 1964, pp. 372--396. 2 Clark, W.E., Le Gros and Boggon, R.H., The thalamic connexions of the frontal lobes of the brain in the monkey. Philos. Trans. B., London, 224 359.
connections. Behavior, parietal and (1935) 3 1 3 -
i06 3 Kievit, J. and Kt~ypers, H.G.J.M., Organization of the thalamocortical connexions to the frontal l o r e in the Rhesus monkey. Exp. Brain Res. , 29 (1977) 299-322. 4 K/inzle, H., Bilateral projections from precentral motor cortex to the putamen and •other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis, Brain Res., 88(1975) 195--209. 5 Kiinzle, H., Thalamic projections from the precentral motor cortex in Macaca fascicularis, Brain Res., 105 (1976)253--267. 6 K~nzle, H., An autoradiographie analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 • and 9) in Macaca faseicularis, Brain Behav. Evol., 15 (1978) 185--234. 7 K/Inzle, H. and Akert, K., Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique, J. eomp. NeUrol., 173.(.1977) 147--164.. 8 Minkowski, M., Etude sur les connexions anatomiques des circonvolutions rolandiques, pa¢i~tales et frontales, Schweiz. Arch. Neurol. Neurochir. Psychiat., 12 (1923) 71--104. 9 Monakow, v., C., Ueher einige durch Exstirpation circumscripte:- Hirnrindenregionen bedingte Entwicklungshemmungen des Kaninchengehirns, Arch. f. Psychiat., 12 (1881) 141--156, 10 Olszewski, J., The thalamus of the macaca mulatta. An atlas for ~se with the stereotaxic instrument. Karger, Basel, 1952. 11 Pribram, K.H., Chow, K.L. and Semmes, J., Limit and organization of the cortical projection from the medial thalamic nucleus in the monkey. J. comp. Neurol., 98 (1953) 433--448. 12 Rutishauser, F., Experimenteller Beitrag zur Stabkranzfaserung im Frontalhirn des Affen. Monatschr. f. Psychiat. u. Neut., Bd. 5 (1899) 161--179. 13 Tanaka, D., Thalamic projections of the dorsomediai prefrontal cortex in the Rhesus monkey (Macaca mulatta), Brain Res., 110 (1976) 21--38. 14 Tobias, T.J., Afferents to prefrontal cortex from the thalamic mediodorsal nucleus in the rhesus monkey, Brain Res., 83 (1975) 191--212. 15 Walker, A.E., The medial dorsal thalamic nucleus. A comparative anatomical, physiological and clinical study, J. comp. Neurol., 73 (1940) 87--115. 16 Woolsey, C.N., Settiage, P.H., Meyer, D.R., Sencer, W., Hamuy, T.P. and Travis, A.M., Patterns of localization in precentral and 'supplementary' motor areas and their relation to the concept of a premo~or area. In Patterns of Organization in the Central Nervous System, Ees. Publ. Ass. nerv. ment. Disc., 30 (1952) 238--264.
103
PROJECTION OF PRECENTRAL MOTOR CORTEX UPON NUCLEUS MEDIALIS DORSALIS THALAMI IN THE MONKEY
K O N R A D AKERT, K U R T H A R T M A N N - V O N M O N A K O W
and HEINZ K U N Z L E
Brain Research Institute o f the University of Zi~'rich, August Fore!s~asse 1, CH-8029 Zh'rich (Switzerland)
(Received October 26th, 1978) . (Accepted November 2rid, 1978)
SUMMARY
The efferent connections of the lateral aspects of the precentral, premotor and granular frontal cortex were reexamined in 12 monkeys (Macaca fascicular/s) by means of anterograde labelling techniques using radioactive proline and leucine. A distinct projection of the precentral gyrus upon the psxalamellar portion of the nucleus medialis dorsalis (MD) was observed. The somatotopic arrangement within this projection is less well defined than within the ventrolateral thalamic complex. The facial division of area 4 has not only a marked ipsilateral but in contrast to the body representation also a distinct if much weaker contrala~ral projection. No label was found in MD after injections in the postcentral gyrus. Thus, MD represents a thalamic link between agranular (motor) and granular (association) cortex of the frontal lobe.
The relationships between medial thalamus and frontal cortex have been explored experimentally since the pioneering studies of Monakow [9] and Rutishauser [12], and with the advent of more powerful methods these relationships have been gradually refined by numerous subsequent investigators [2,11,13--15]. Akert [1] emphasized the 10xninar organization of thalamic afferents to agranular and granular frontal Brodmann fields with respect to their origin in ventrolateral and mediodorsal nuclear masses respectively. The latter findings have been recently confirmed and extended by Kievit and Kuypers [3] who applied the retrograde axonal flow technique for the demonstration of the remarkable laminar organisation of the thalamo-frontal connections particularly if examined in the horizontal plane. It is generally assumed that cortico-thalamic connections are organized in a reciprocal manner. An important exception to this rule was found recently in the course of systematic investigations of the afferent connections of area 4. In concerns the projections to the mediodorsal nucleus (MD) which heretofore has been
104
regm:ded as the domain of prefrontal connections. These findings will be briefly reported here. The present study was carried out in 12 monkeys (Macaca fascicularis) in which small, circumscribed injections into frontal cortical areas have been made
I
I
i I
f
f
i
I
I I .
~ /cL b~~-
•
.... %
f:
Ii
~,.
['
"" ARM
........
.**,I
CM \
i~
/" /
~
~', .,,,.
"-.... "
LEG
I
"~ ".,X,.,
,Pf -
Fig. 1. Projection of precentral motor cortex (precentral gyrus) upon the medial thalamic nuclei in the monkey. Note that face, arm and leg areas of the primary motor cortex project not only to centrum medianum (CM) and central lateralis (CL), but also to the adjacent portion of medialis dorsalis (MD). There is a shifting overlap with the face representation (above) extending more ventrally than the leg and arm areas (below). Mag. x15.
105
with radioactive leucine and proline. The procedures have been described in detail elsewhere [4 ] ..and the reconstructions of the injection and uptake sites are also displayed in detail in the same paper. Suffice it here to say that the injections specifically covered the lateral aspects of the precentral gyrus and the typical locations which, according to the electrophysiological maps of Woolsey et al. [16] represent the face, arm and leg areas of the primary motor cortex. Silver grains were traced to various thalamic nuclei, particulaHy to the ventrolateral group and centrum rnedianum [5]. This communication places its main emphasis on terminal and preterminal fields within the medial dorsal nucleus. The projection of area 4 to M D in the monkey 4s surprisingly dense. Its terminal and preterminal field occupies the lateral moiety of M D corresponding approximately to p. multiformis of Olszewski [10] (Fig. 1). The facial projection is particularly heavy and a faint contralateral mirror focus can also be seen (not illustrated). Face, arm and leg representations are characterized by a shifting overlap within a narrow sheath of cells with the face extending rr.ore ventrally than the leg and arm areas (Fig. 1). When compared with the rather distinct projections within the ventrolateral nuclei [5], it seems inevitable to conclude that the somatotopic arrangement in M D is not as clearly defined. Furthermore, an overlap with area 8 and area 6 projections [6,7] is also noted. All these precentral and prernotor areas seem to project within a relatively limited field of M D situated rather closely to the intralarninarnuclei which are additional recipients of frontal lobe connections [6]. This finding is all the more remarkable because reciprocal thalamocortical connections (i.e.from M D to area 4) have thus far not been observed [3 ]. The main and perhaps exclusive cortical target of M D seems to be the so
The skillful assistance of A. F~ih, E. Schneider, D. Savini and H. Hauser is gratefully acknowledged. This work was supported by the Swiss National Science Foundation, grant 3.636.75 and the Stiftung ffir wissenschaftliche Forschung an der Universit~it Zfirich. REFERENCES 1 Akert, K., Comparative anatomy of frontal cortex and thalamo-frontal In J.M. Warren and K. Akert (Eds.), The Frontal Granular Cortex and McGraw-Hill, New York, 1964, pp. 372--396. 2 Clark, W.E., Le Gros and Boggon, R.H., The thalamic connexions of the frontal lobes of the brain in the monkey. Philos. Trans. B., London, 224 359.
connections. Behavior, parietal and (1935) 3 1 3 -
i06 3 Kievit, J. and Kt~ypers, H.G.J.M., Organization of the thalamocortical connexions to the frontal l o r e in the Rhesus monkey. Exp. Brain Res. , 29 (1977) 299-322. 4 K/inzle, H., Bilateral projections from precentral motor cortex to the putamen and •other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis, Brain Res., 88(1975) 195--209. 5 Kiinzle, H., Thalamic projections from the precentral motor cortex in Macaca fascicularis, Brain Res., 105 (1976)253--267. 6 K~nzle, H., An autoradiographie analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 • and 9) in Macaca faseicularis, Brain Behav. Evol., 15 (1978) 185--234. 7 K/Inzle, H. and Akert, K., Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique, J. eomp. NeUrol., 173.(.1977) 147--164.. 8 Minkowski, M., Etude sur les connexions anatomiques des circonvolutions rolandiques, pa¢i~tales et frontales, Schweiz. Arch. Neurol. Neurochir. Psychiat., 12 (1923) 71--104. 9 Monakow, v., C., Ueher einige durch Exstirpation circumscripte:- Hirnrindenregionen bedingte Entwicklungshemmungen des Kaninchengehirns, Arch. f. Psychiat., 12 (1881) 141--156, 10 Olszewski, J., The thalamus of the macaca mulatta. An atlas for ~se with the stereotaxic instrument. Karger, Basel, 1952. 11 Pribram, K.H., Chow, K.L. and Semmes, J., Limit and organization of the cortical projection from the medial thalamic nucleus in the monkey. J. comp. Neurol., 98 (1953) 433--448. 12 Rutishauser, F., Experimenteller Beitrag zur Stabkranzfaserung im Frontalhirn des Affen. Monatschr. f. Psychiat. u. Neut., Bd. 5 (1899) 161--179. 13 Tanaka, D., Thalamic projections of the dorsomediai prefrontal cortex in the Rhesus monkey (Macaca mulatta), Brain Res., 110 (1976) 21--38. 14 Tobias, T.J., Afferents to prefrontal cortex from the thalamic mediodorsal nucleus in the rhesus monkey, Brain Res., 83 (1975) 191--212. 15 Walker, A.E., The medial dorsal thalamic nucleus. A comparative anatomical, physiological and clinical study, J. comp. Neurol., 73 (1940) 87--115. 16 Woolsey, C.N., Settiage, P.H., Meyer, D.R., Sencer, W., Hamuy, T.P. and Travis, A.M., Patterns of localization in precentral and 'supplementary' motor areas and their relation to the concept of a premo~or area. In Patterns of Organization in the Central Nervous System, Ees. Publ. Ass. nerv. ment. Disc., 30 (1952) 238--264.