Spatial distribution of thalamic projections to the supplementary motor area and the primary motor cortex: A retrograde multiple labeling study in the macaque monkey

Shindo, Katsuhiro; Shima, Keisetsu; Tanji, Jun

doi:10.1002/cne.903570110

Cited by 58 publications

(46 citation statements)

References 69 publications

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“…In general, the patterns of thalamocortical motor connections reported for macaques (e.g., Jones et al, 1979;Schell and Strick, 1984;Darian-Smith et al, 1990;Nakano et al, 1993;Shindo et al, 1995;Matelli and Luppino, 1996;Rouiller et al, 1999;Morel et al, 2005) are similar to those reported here for galagos. In both macaques and galagos, M1 receives dense inputs from VLp, less dense inputs from VLa, and only a few inputs from VM and VA. PMV receives dense inputs from medial VLp (area X), and less dense inputs from VLa, VM and MDmf.…”

Section: Thalamic Connections Of Motor Areas and Prefrontal Cortexsupporting

confidence: 87%

The thalamic connections of motor, premotor, and prefrontal areas of cortex in a prosimian primate (Otolemur garnetti)

2006

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Connections of motor areas in the frontal cortex of prosimian galagos (Otolemur garnetti) were determined by injecting tracers into sites identified by microstimulation in the primary motor area (M1), dorsal premotor area (PMD), ventral premotor area (PMV), supplementary motor area (SMA), frontal eye field (FEF), and granular frontal cortex. Retrogradely labeled neurons for each injection were related to architectonically defined thalamic nuclei. Nissl, acetylcholinesterase, cytochrome oxidase, myelin, parvalbumin, calbindin, and Cat 301 preparations allowed the ventral anterior and ventral lateral thalamic regions, parvocellular and magnocellular subdivisions of ventral anterior nucleus, and anterior and posterior subdivisions of ventral lateral nucleus of monkeys to be identified. The results indicate that each cortical area receives inputs from several thalamic nuclei, but the proportions differ. M1 receives major inputs from the posterior subdivision of ventral lateral nucleus while premotor areas receive major inputs from anterior parts of ventral lateral nucleus (the anterior subdivision of ventral lateral nucleus and the anterior portion of posterior subdivision of ventral lateral nucleus). PMD and SMA have connections with more dorsal parts of the ventral lateral nucleus than PMV. The results suggest that galagos share many subdivisions of the motor thalamus and thalamocortical connection patterns with simian primates, while having less clearly differentiated subdivisions of the motor thalamus.

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Section: Thalamic Connections Of Motor Areas and Prefrontal Cortexsupporting

confidence: 87%

The thalamic connections of motor, premotor, and prefrontal areas of cortex in a prosimian primate (Otolemur garnetti)

2006

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“…The origin of this variability is unclear, but it does not appear to be correlated with experimental factors such as survival time, total volume of virus injected, or number of sites injected. More importantly, similar variations have been observed in other studies that used conventional tracers to define origin of thalamic projections to the SMA (Schell and Strick, 1984;Wiesendanger and Wiesendanger, 1985a;Darian-Smith et al, 1990;Rouiller et al, 1994Rouiller et al, , 1999Shindo et al, 1995;Matelli and Luppino, 1996;Sakai et al, 1999Sakai et al, , 2002. In particular, the ratio of neurons labeled in basal ganglia recipient nuclei of the thalamus (VLo, VApc, VLm, VLcr) to neurons labeled in cerebellar recipient nuclei (X, …”

Section: Discussionsupporting

confidence: 75%

“…VPLo, VLcc) ranged from 0.9:1 to 6.4:1 (n ϭ 8) (Shindo et al, 1995;Matelli and Luppino, 1996). This range is nearly identical to that of GPi/dentate neurons labeled in the present study after virus injections into the SMA (0.6:1-6.3:1) (Table 2).…”

Section: M1supporting

confidence: 82%

“…The SMA has been considered to be an important target of basal ganglia output (Schell and Strick, 1984;Wiesendanger and Wiesendanger, 1985a;Alexander et al, 1986;Darian-Smith et al, 1990;Rouiller et al, 1994Rouiller et al, , 1999Shindo et al, 1995;Matelli and Luppino, 1996;Sakai et al, 1999Sakai et al, , 2002. In addition, Wiesendanger and Wiesendanger (1985a,b) provided some evidence for cerebellar input to the SMA, especially to its rostral portion, which is now recognized as the pre-SMA.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output

Akkal¹,

Dum²,

Strick³

2007

J. Neurosci.

402

297

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We used retrograde transneuronal transport of neurotropic viruses in Cebus monkeys to examine the organization of basal ganglia and cerebellar projections to two cortical areas on the medial wall of the hemisphere, the supplementary motor area (SMA) and the pre-SMA. We found that both of these cortical areas are the targets of disynaptic projections from the dentate nucleus of the cerebellum and from the internal segment of the globus pallidus (GPi). On average, the number of pallidal neurons that project to the SMA and pre-SMA is approximately three to four times greater than the number of dentate neurons that project to these cortical areas. GPi neurons that project to the pre-SMA are located in a rostral, "associative" territory of the nucleus, whereas GPi neurons that project to the SMA are located in a more caudal and ventral "sensorimotor" territory. Similarly, dentate neurons that project to the pre-SMA are located in a ventral, "nonmotor" domain of the nucleus, whereas dentate neurons that project to the SMA are located in a more dorsal, "motor" domain. The differential origin of subcortical projections to the SMA and pre-SMA suggests that these cortical areas are nodes in distinct neural systems. Although both systems are the target of outputs from the basal ganglia and the cerebellum, these two cortical areas seem to be dominated by basal ganglia input.

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“…Two days after the injection, thalamic neurons were labeled mainly in the VLo and VPLo that project to the MI directly. Relatively sparse labeling of these thalamic neurons indicates that a little longer time than 2 d may be needed for sufficient labeling of first-order neurons (for comparison with conventional tracing, see Holsapple et al, 1991;Shindo et al, 1995). At a 3 d postinjection period, both the GPi and the cerebellar nuclei contained labeled neurons.…”

Section: Discussionmentioning

confidence: 99%

Organization of Multisynaptic Inputs from Prefrontal Cortex to Primary Motor Cortex as Revealed by Retrograde Transneuronal Transport of Rabies Virus

Miyachi¹,

Lu²,

Inoue³

et al. 2005

J. Neurosci.

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The organization of multisynaptic projections from the prefrontal cortex to the primary motor cortex (MI) was examined in macaque monkeys by retrograde transneuronal transport of rabies virus. In the first series of experiments, the virus was injected into the MI forelimb region, and the time-dependent distribution patterns of transsynaptic labeling were analyzed in the frontal lobe with various survivals (2-4 d). Two days after the viral injection, neuronal labeling emerged in the caudal aspects of the nonprimary motor-related areas that are known to project to the MI directly. At the same time, the motor thalamus contained labeled neurons. On the third day, cortical labeling extended into the rostral motor-related areas and, also, prearcuate area 8. Moreover, a number of labeled neurons were located in the internal pallidum and the cerebellar nuclei. At the 4 d postinjection period, neuronal labeling occurred widely in prefrontal areas as well as in the putamen and the cerebellar cortex. In the second series of experiments, the viral injection was made into the MI hindlimb region, and the distribution pattern of prefrontal labeling on the fourth day was compared with that in the forelimb-injection case. The labeled neurons in each prefrontal area were much fewer in the hindlimb-injection case than in the forelimb-injection case. Whereas ventral area 46 was most densely labeled from the forelimb region, only sparse labeling from the hindlimb region was observed in this prefrontal area. The present results suggest the importance of ventral area 46 in the cognitive control of forelimb movements.

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Spatial distribution of thalamic projections to the supplementary motor area and the primary motor cortex: A retrograde multiple labeling study in the macaque monkey

Cited by 58 publications

References 69 publications

The thalamic connections of motor, premotor, and prefrontal areas of cortex in a prosimian primate (Otolemur garnetti)

The thalamic connections of motor, premotor, and prefrontal areas of cortex in a prosimian primate (Otolemur garnetti)

Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output

Organization of Multisynaptic Inputs from Prefrontal Cortex to Primary Motor Cortex as Revealed by Retrograde Transneuronal Transport of Rabies Virus

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