Somatotopically arranged inputs from putamen and subthalamic nucleus to primary motor cortex

Juntendo University, Edo, Tokyo, Japan
Neuroscience Research (Impact Factor: 1.94). 12/2006; 56(3):300-8. DOI: 10.1016/j.neures.2006.07.012
Source: PubMed


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 somatotopic 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.

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Available from: Shigehiro Miyachi
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    • "Interestingly, however, the lateral striatal regions showing increasing D 2 /D 3 availability with disease duration were non-overlapping with the medial distribution of reduced D 2 /D 3 availability found in writer's cramp compared with control subjects. Figure 5 Differences in Non-human primate neuroanatomical tracing studies (Takada et al., 1998; Nambu et al., 2002, Kelly and Strick, 2004; Miyachi et al., 2006; Haber and Calzavara, 2009; Nambu, 2011) and human imaging studies (Maillard et al., 2000; Gerardin et al., 2003; Bingel et al., 2004) have helped elucidate the organization of the striatum and other basal ganglia structures, which is thought to reflect somatotopically organized cortical inputs to the striatum and outputs back to the cortex. Disorganization of the striatal somatotopic organization has been reported both in mouse models of dystonia (Chiken et al., 2008) as well as in humans (Vitek et al., 1999; Delmaire et al., 2005). "
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    ABSTRACT: Writer's cramp is a task-specific focal hand dystonia characterized by involuntary excessive muscle contractions during writing. Although abnormal striatal dopamine receptor binding has been implicated in the pathophysiology of writer's cramp and other primary dystonias, endogenous dopamine release during task performance has not been previously investigated in writer's cramp. Using positron emission tomography imaging with the D2/D3 antagonist (11)C-raclopride, we analysed striatal D2/D3 availability at rest and endogenous dopamine release during sequential finger tapping and speech production tasks in 15 patients with writer's cramp and 15 matched healthy control subjects. Compared with control subjects, patients had reduced (11)C-raclopride binding to D2/D3 receptors at rest in the bilateral striatum, consistent with findings in previous studies. During the tapping task, patients had decreased dopamine release in the left striatum as assessed by reduced change in (11)C-raclopride binding compared with control subjects. One cluster of reduced dopamine release in the left putamen during tapping overlapped with a region of reduced (11)C-raclopride binding to D2/D3 receptors at rest. During the sentence production task, patients showed increased dopamine release in the left striatum. No overlap between altered dopamine release during speech production and reduced (11)C-raclopride binding to D2/D3 receptors at rest was seen. Striatal regions where D2/D3 availability at rest positively correlated with disease duration were lateral and non-overlapping with striatal regions showing reduced D2/D3 receptor availability, except for a cluster in the left nucleus accumbens, which showed a negative correlation with disease duration and overlapped with striatal regions showing reduced D2/D3 availability. Our findings suggest that patients with writer's cramp may have divergent responses in striatal dopamine release during an asymptomatic motor task involving the dystonic hand and an unrelated asymptomatic task, sentence production. Our voxel-based results also suggest that writer's cramp may be associated with reduced striatal dopamine release occuring in the setting of reduced D2/D3 receptor availability and raise the possibility that basal ganglia circuits associated with premotor cortices and those associated with primary motor cortex are differentially affected in primary focal dystonias.
    Full-text · Article · Oct 2013 · Brain
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    • "The third-order labeling was confirmed by examining neuronal labeling in the basal ganglia in all but one monkey. In monkey Ch, a small number of the fourth-order neurons (i.e., interneurons in the striatum) were rabies-labeled (Miyachi et al., 2006). In the other monkeys, rabies labeling was observed in striatal projection neurons, but not in interneurons innervating the projection neurons, which indicates that the transneuronal labeling reached third-order neurons, but not fourth-order neurons. "
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    ABSTRACT: Different sectors of the prefrontal cortex have distinct neuronal connections with higher-order sensory areas and/or limbic structures and are related to diverse aspects of cognitive functions, such as visual working memory and reward-based decision-making. Recent studies have revealed that the prefrontal cortex (PF), especially the lateral PF, is also involved in motor control. Hence, different sectors of the PF may contribute to motor behaviors with distinct body parts. To test this hypothesis anatomically, we examined the patterns of multisynaptic projections from the PF to regions of the primary motor cortex (MI) that represent the arm, hand, and mouth, using retrograde transsynaptic transport of rabies virus. Four days after rabies injections into the hand or mouth region, particularly dense neuron labeling was observed in the ventrolateral PF, including the convexity part of ventral area 46. After the rabies injections into the mouth region, another dense cluster of labeled neurons was seen in the orbitofrontal cortex (area 13). By contrast, rabies labeling of PF neurons was rather sparse in the arm-injection cases. The present results suggest that the PF-MI multisynaptic projections may be organized such that the MI hand and mouth regions preferentially receive cognitive information for execution of elaborate motor actions.
    Full-text · Article · May 2013 · Neuroscience Research
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    • "110) " ; as another example, Karachi et al. (2004) mention: " In summary, the pallidosubthalamic projection appears to be topographically arranged, with the sensorimotor part of the STN occupying its dorsolateral half, and the limbic part being restricted to its most anterior and medioventral portion (p. 178) " ; finally, Miyachi et al. (2006) provide a figure (i.e., their Figure 6B) that presents the layout of subdivisions (see Table 2 for all the statements used to visualize all the included studies). One might argue that a temporal bias may be present, i.e., a lower number of subdivisions could have been found due to older methods and that more recent studies using advanced methodologies converge to a specific number of subdivisions. "
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