Physiologic properties and somatotopic organization of the primate motor thalamus

J. L. Vitek, J. Ashe, M. R. DeLong, G. E. Alexander

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Abstract

1. To examine the functional organization of the primate 'motor' thalamus, neuronal activity was studied systematically in awake behaving monkeys throughout the nucleus ventralis lateralis, pars oralis (VLo), nucleus ventralis posterior lateralis, pars oralis (VPLo), ventralis lateralis, pars caudalis (VLc), and portions of ventralis anterior (VA) and Area X. In addition, portions of the sensory nucleus ventralis posterior lateralis, pars caudalis (VPLc) were explored. Isolated neurons were examined for their responses to somatosensory examination and active movement (n = 919) and for their response to torque-induced joint displacements (n = 375). A total of 684 neurons was determined histologically to lie within specific subnuclei of the motor (n = 574) or sensory (n = 110) thalamus. 2. The sensorimotor response properties of neurons in the thalamic subnuclei showed clear differences in their response to somatosensory examination. In order of decreasing frequency, the percent of neurons responding to passive somatosensory examination in each subnucleus were as follows: VPLc. 96% (106/110), VPLo. 93% (252/270), VLc, 77% (43/56), VLo, 37% (59/155), Area X, 22% (12/53), and VA, 12% (5/40). Conversely, neurons that responded only to active movement were most frequent in VLo, 44% (68/155), VA. 45% (18/40), and Area X, 40% (21/53) and relatively infrequent in VLc 11% (6/56) and VPLo, 3% (7/270). In VPLc, no neurons were found that responded only to active movement (0/110). 3. A well-defined somatotopic organization was found in VLo, VPLo, and VPLc and was suggested strongly for VLc. Individual body regions were represented in a series of lamellae, organized in a partial onion skin-like arrangement with the leg represented in the outermost lamella, and the trunk, arm, and orofacial regions represented in successively deeper lamellae. In general the body representations, although present for each subnucleus thoroughly examined, i.e., VLo, VPLo, and VPLc, also were contiguous across subnuclei. Based on the available data, a clear somatotopic picture could not be discerned for Area X or VA. 4. Responses to torque application were more common in neurons in VPLo (77%; 60/78) and VLc (73%; 16/22) than in VLo (44%; 12/27). Mean latencies were shortest for neurons in VPLo (25 ± 14 ms; mean ± SD) and the bordering (shell) region of VPLc (22 ± 15 ms) and were approximately twice as long in VLc (51 ± 23 ms) and VLo (47 ± 21 ms). 5. Short-latency (<20 ms) responses to torque application were found for a large proportion of cells in VPLo (45%; 27/60). These neurons were located largely in the lateral portions of ventro-caudal VPLo. The presence of short-latency torque responses in this portion of VPLo suggests that this region may act as a direct relay for proprioceptive information from the periphery to the motor cortex because this area of VPLo has been demonstrated to project directly to the motor cortex. 6. Although mean firing frequencies for VPLo (22 ± 11 Hz) were different from other subnuclei within the motor thalamus (12 ± 8, 13 ± 8, 15 ± 8, and 12 ± 8 Hz for VLc, VLo, VA, and Area X, respectively), there was a wide distribution of average rates with significant overlap between subnuclei. Mean firing frequencies in VPLc (26 ± 8 Hz) were similar to those in VPLo. 7. This study is the first physiological study to demonstrate a detailed somatotopy in both basal ganglia (VLo) and cerebellar (VPLo and VLc) receiving areas of the thalamus and to identify and localize neurons with short-latency responses to kinesthetic stimuli in the posterolateral portions of VPLo.

Original languageEnglish (US)
Pages (from-to)1498-1513
Number of pages16
JournalJournal of neurophysiology
Volume71
Issue number4
DOIs
StatePublished - 1994
Externally publishedYes

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