Structural Basis for Cortico-Basal Ganglia Loop That Is Involved in Organized Behavior

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Employing retrograde transsynaptic transport of rabies virus, we investigated the organization of basal ganglia inputs to hindlimb, proximal and distal forelimb, and orofacial representations of the macaque primary motor cortex (MI). Four days after rabies injections into these MI regions, neuronal labeling occurred in the striatum and the subthalamic nucleus (STN) through the cortico-basal ganglia loop circuits. In the striatum, two distinct sets of the labeling were observed: one in the dorsal putamen, and the other in the ventral striatum (ventromedial putamen and nucleus accumbens). The dorsal striatal labeling was somatotopically arranged and its distribution pattern was in good accordance with that of the corticostriatal inputs, such that the hindlimb, orofacial, or forelimb area was located in the dorsal, ventral, or intermediate zone of the putamen, respectively. The distribution pattern of the ventral striatal labeling was essentially the same in all cases. In the STN, the som … More atotopic arrangement of labeled neurons was in register with that of corticosubthalamic inputs. The present results suggest that the cortico-basal ganglia motor circuits involving the dorsal putamen and the STN may constitute separate closed loops based on the somatotopy, while the ventral striatum provides common multisynaptic projections to all body-part representations in the MI. To investigate the somatotopic organization of the cerebellum, we then analyzed multisynaptic inputs to the MI. Three days after rabies injections into proximal forelimb, distal forelimb, and hindlimb representations of the macaque MI, second-order neurons via the thalamus were labeled in the deep cerebellar nuclei, including the dentate (DN), anterior interpositus (AIN), and posterior interpositus (PIN) nuclei. In the DN, the labeling of both the forelimb and the hindlimb was seen mainly in the dorsal aspect. The labeling of the hindlimb was located rostral to that of the forelimb, and the labeling of the proximal forelimb was located slightly rostral to that of the distal forelimb. The same rostrocaudal arrangement was observed in the AIN. In the PIN, however, labeling from the MI hindlimb and forelimb representations largely overlapped. At the 4-day postinjection period, third-order labeling occurred in Purkinje cells of the cerebellar hemisphere. The Purkinje cell labeling from the forelimb representation, including the proximal and distal regions, was observed primarily in lobules IV-VI and crus I. The proximal forelimb labeling was both rostral and lateral to that of the distal forelimb within lobules IV-VI. Yet, the hindlimb labeling was seen both rostral and lateral to that of the proximal forelimb within lobules III-VI. These results indicate that the hindlimb, proximal forelimb, and distal forelimb are arranged rostrocaudally in the DN and AIN, while there is dual somatotopy along the rostrocaudal and lateromedial axes in the cerebellar cortex. Less