ArticleConvergence of Limbic Input to the Cingulate Motor Cortex in the Rhesus Monkey
Introduction
The limbic lobe forms a continuous ring of cortex around the medial edge of the cerebral hemisphere that is uninterrupted by major sulci 30, 45, 82, 124. It is characterized by marked structural and functional heterogeneity that in many ways mirrors features of the isocortex that it borders. For example, the anterior part of the cingulate gyrus is bounded dorsally by the supplementary motor (M2) and primary motor cortices (M1) and has structural and functional commonalities with these isocortical motor fields. Sanides [140]and Braak [29]emphasized the cytoarchitectural continuity between the dorsal part of the anterior cingulate gyrus and the frontal motor cortices, and recent neuroanatomical studies in nonhuman primates have revealed that corticospinal, corticofacial, corticopontine, corticorubral, and corticostriate axons arise from this region of the cingulate gyrus 27, 44, 48, 54, 55, 61, 62, 79, 102, 103, 104, 105, 106, 111, 139, 165. More specifically, the cortex in the lower bank and fundus of the cingulate sulcus has been termed area 24c or M3 [99]and area 23c or M4 [105], and is the only part of the limbic lobe known to contribute to the corticorubral, corticofacial, and corticospinal pathways and be interconnected in an organized fashion with M1 and M2 76, 78, 80, 99, 105, 106, 117, 157. Functional studies in humans and nonhuman primates have long implicated the anterior cingulate region in motor control 19, 68, 77, 95, 103, 127, 148, 149, 150, 151, 152, 155, 159, 171, 175and a recent neuroimaging study has shown that the human anterior cingulate cortex may be organized somatotopically and is involved with the execution and suppression of complex forms of voluntary motor activity [125]. It is of interest that pathology in the anterior cingulate region in both humans and monkey alters not only emotion, affect, and attention, but leads as well to striking changes in motor behavior 3, 18, 33, 50, 74, 81, 116. In many circumstances a salient feature includes the poverty of movement or akinesia.
There is substantial evidence to support the notion that alterations in emotion and affect can have profound influences on motor behavior 75, 134, 135, 182. For example, many types of psychiatric illness are characterized by stereotyped rhythmic movements, the assumption of abnormal postures, awkwardness, and stiffness [118]. Manic–depressive illness also leads to profound alterations in motor behavior, ranging, as the name implies, from greatly exaggerated motility during the manic phase to hypomotility during the depressive phase. Hysterical reactions further underscore the association between altered affect and motor abnormalities. In this example, immobility and a perceived paralysis occur without accompanying organic motor system alterations. Less well documented, but commonly encountered phenomena such as catalepsy, paralysis as a consequence of fear, emotional tremor, and hyperreflexia in periods of emotional stress further remind one that emotional and motivational mechanisms of the central nervous system, thought to be mediated by the limbic system, can indeed, profoundly alter complex motor behaviors.
This occurrence of abnormal motor behavior during altered affective states implies to us that a rather strong structural linkage must occur between telencephalic limbic system structures and structures that govern the expression of voluntary motor behavior. In this study, we address this hypothesis by examining in the monkey, the ipsilateral projections of mesocortical areas that constitute the limbic lobe to the cortex lining the lower bank, and fundus of the cingulate sulcus, which gives rise to a component of the descending motor pathways. We describe a number of intrinsic limbic inputs to the cingulate motor cortex (M3 and M4) that provide a cortical entry point for limbic–motor interactions.
Section snippets
Abbreviations
ac, anterior commissure; amy, amyg, amygdala; as, spur of the arcuate sulcus; ca, caudate nucleus; cc, corpus callosum; cf, calcarine fissure; cgs, cingulate sulcus; cs, central sulcus; FB, fast blue; DY, diamidino yellow; gp, globus pallidus; hy, hypothalamus; HRP, horseradish peroxidase; Iap, insula, agranular-periallocortical; ic, internal capsule; Idg, insula, dysgranular; Ig, insula, granular; ins, insula; ios, inferior occipital sulcus; ipcd, inferior precentral dimple; ips, intraparietal
Materials and Methods
Twenty-nine rhesus monkey brains were investigated to determine limbic lobe inputs to the cingulate motor cortex. Four had injections of fluorescent dyes in different parts of the cingulate motor cortex (area 24c or M3 and area 23 or M4) for retrograde analysis. Twenty-three monkeys had injections of tritiated amino acids (TAA) into different parts of the limbic lobe for anterograde analysis. Two monkeys had injections of horseradish peroxidase (HRP) into the entorhinal cortex and gyrus rectus,
Area 24c (M3) cases.
Three cases were studied that had a single injection of FB into area 24c (cases 1, 2, 3A) (Fig. 1 , Fig. 2A , Fig. 3 , Fig. 4 ). The criteria of Condé [37]was used to assess the effectiveness of the fluorescent injection sites where zones 0–II correspond to the effective uptake site 37, 60, 73. In case 1, the solid deposit (zone 0) and zones I and II involved area 24c and encroached on the dorsal part of area 24b. Examination of the contralateral hemisphere demonstrated the highest
Discussion
Recently, attention has focused on the cortex of the lower bank and fundus of the cingulate sulcus for several reasons. It is the only part of the limbic lobe known to elicit movement following stimulation 77, 79, 95and neuronal activity patterns indicate it may contribute to mediating novel and practiced motor acts 125, 148. Furthermore, the cingulate motor cortex is connected with diverse parts of the granular prefrontal cortex 20, 76, 101and projects topographically to the primary and
Conclusions
Cortex lining the lower bank and fundus of the cingulate sulcus is a unique region of the limbic lobe, in that more than any other part of the limbic lobe, its structural features and functional capabilities suggest a strong and direct role in shaping the outcome of voluntary motor activity. Our observations indicate that the anterior part of the dorsal edge of the limbic lobe, area 24c (M3), forms a critical entry point for widespread limbic lobe input. The more posteriorly located area 23c
Acknowledgements
Supported by NIH grants NS 14944 and NS 33003.
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