Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus

Jin Chung, K. H. Lee, D. J. Surmeier, L. S. Sorkin, J. Kim, W. D. Willis

Research output: Contribution to journalArticle

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Abstract

1. The activity of 132 neurons in the caudal part of the ventral posterior lateral nucleus (VPL(c)) of the thalamus was recorded from 23 anesthetized monkeys. All single thalamic units that could be excited by electrical search stimuli applied to the contralateral sciatic nerve were investigated. Responses of these cells to mechanical, thermal, and electrical stimuli applied in the periphery indicated that at least half of the sampled cells were nociceptive. 2. Based on responses to graded mechanical stimuli applied to the periphery, 110 of the sampled cells that received a predominant input from cutaneous receptive fields were classified. There were 56 low-threshold, 39 wide dynamic range, and 15 high-threshold cells. The same neurons were also classified into five mechanical types based on a cluster analysis: types 1-5 contained 25, 34, 17, 10, and 24 cells, respectively. The fact that about half the population of cells belonged to either the wide dynamic or the high threshold group (or mechanical types 3-5) suggested that a large population of VPL(c) neurons respond to mechanical nociceptive stimuli either exclusively or preferentially. 3. Responses of 63 thalamic neurons were tested to noxious heat pulses applied to their cutaneous receptive fields with a contact thermostimulator. Of these, 47 cells were excited, whereas only 16 cells did not respond. 4. The peripheral nerve that innervated the receptive field of each of 82 thalamic neurons was stimulated with graded strengths to activate A fibers only or both A and C fibers. All tested cells responded to peripheral A fiber volleys. In addition, 42 of these cells responded to peripheral C fiber volleys. The C fiber responses could be either short lasting (a few hundreds of milliseconds) or long lasting (up to several seconds). 5. The recording sites of 80 cells were reconstructed. Of these, 78 were in the VPL(c) nucleus and the remaining two were in the reticular nucleus of the thalamus. No obvious relationship between the response characteristics and the locations of the cells within the VPL(c) nucleus was found. 6. Sampled thalamic units had a variety of sources of input from the periphery, including both cutaneous and/or deep tissue receptive fields. The majority of the cells, however, had exclusively cutaneous receptive fields. The sizes of the cutaneous receptive fields were often very small, so that nearly half (41%) of the receptive fields of cells sampled occupied an area of skin smaller than half the foot. However, 6 of 46 cells tested could be excited by noxious mechanical stimuli applied to a variety of sites on the body and face. Inhibitory receptive fields were demonstrated for 10 cells using comparable stimuli. 7. Responses of thalamic neurons to stimulation of the various parts of the spinal cord white matter were tested: contralateral dorsal column; contralateral dorsolateral funiculus, and ipsilateral ventrolateral funiculus. Thalamic neurons showed complex response patterns of excitation and inhibition following stimulation of tracts in different parts of the spinal cord white matter. Some neurons were selectively excited by stimulation of one of these three spinal cord sites. Other cells could be excited by stimulation of more than one part of the spinal cord. The most consistent activation of thalamic neurons of every category was produced by stimulation of the dorsal column. These complex patterns of spinal cord input were confirmed by comparing responses before and after selective lesions of the spinal cord. The results suggest that there are populations of thalamic neurons responding exclusively to dorsal or ventral spinal pathways, whereas other cells receive parallel inputs from multiple spinal pathways.

Original languageEnglish (US)
Pages (from-to)370-390
Number of pages21
JournalJournal of Neurophysiology
Volume56
Issue number2
StatePublished - 1986

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Ventral Thalamic Nuclei
Lateral Thalamic Nuclei
Haplorhini
Neurons
Spinal Cord
Myelinated Nerve Fibers
Unmyelinated Nerve Fibers
Skin
Hot Temperature
Posterior Thalamic Nuclei
Population

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Chung, J., Lee, K. H., Surmeier, D. J., Sorkin, L. S., Kim, J., & Willis, W. D. (1986). Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. Journal of Neurophysiology, 56(2), 370-390.

Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. / Chung, Jin; Lee, K. H.; Surmeier, D. J.; Sorkin, L. S.; Kim, J.; Willis, W. D.

In: Journal of Neurophysiology, Vol. 56, No. 2, 1986, p. 370-390.

Research output: Contribution to journalArticle

Chung, J, Lee, KH, Surmeier, DJ, Sorkin, LS, Kim, J & Willis, WD 1986, 'Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus', Journal of Neurophysiology, vol. 56, no. 2, pp. 370-390.
Chung, Jin ; Lee, K. H. ; Surmeier, D. J. ; Sorkin, L. S. ; Kim, J. ; Willis, W. D. / Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus. In: Journal of Neurophysiology. 1986 ; Vol. 56, No. 2. pp. 370-390.
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T1 - Response characteristics of neurons in the ventral posterior lateral nucleus of the monkey thalamus

AU - Chung, Jin

AU - Lee, K. H.

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AU - Willis, W. D.

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N2 - 1. The activity of 132 neurons in the caudal part of the ventral posterior lateral nucleus (VPL(c)) of the thalamus was recorded from 23 anesthetized monkeys. All single thalamic units that could be excited by electrical search stimuli applied to the contralateral sciatic nerve were investigated. Responses of these cells to mechanical, thermal, and electrical stimuli applied in the periphery indicated that at least half of the sampled cells were nociceptive. 2. Based on responses to graded mechanical stimuli applied to the periphery, 110 of the sampled cells that received a predominant input from cutaneous receptive fields were classified. There were 56 low-threshold, 39 wide dynamic range, and 15 high-threshold cells. The same neurons were also classified into five mechanical types based on a cluster analysis: types 1-5 contained 25, 34, 17, 10, and 24 cells, respectively. The fact that about half the population of cells belonged to either the wide dynamic or the high threshold group (or mechanical types 3-5) suggested that a large population of VPL(c) neurons respond to mechanical nociceptive stimuli either exclusively or preferentially. 3. Responses of 63 thalamic neurons were tested to noxious heat pulses applied to their cutaneous receptive fields with a contact thermostimulator. Of these, 47 cells were excited, whereas only 16 cells did not respond. 4. The peripheral nerve that innervated the receptive field of each of 82 thalamic neurons was stimulated with graded strengths to activate A fibers only or both A and C fibers. All tested cells responded to peripheral A fiber volleys. In addition, 42 of these cells responded to peripheral C fiber volleys. The C fiber responses could be either short lasting (a few hundreds of milliseconds) or long lasting (up to several seconds). 5. The recording sites of 80 cells were reconstructed. Of these, 78 were in the VPL(c) nucleus and the remaining two were in the reticular nucleus of the thalamus. No obvious relationship between the response characteristics and the locations of the cells within the VPL(c) nucleus was found. 6. Sampled thalamic units had a variety of sources of input from the periphery, including both cutaneous and/or deep tissue receptive fields. The majority of the cells, however, had exclusively cutaneous receptive fields. The sizes of the cutaneous receptive fields were often very small, so that nearly half (41%) of the receptive fields of cells sampled occupied an area of skin smaller than half the foot. However, 6 of 46 cells tested could be excited by noxious mechanical stimuli applied to a variety of sites on the body and face. Inhibitory receptive fields were demonstrated for 10 cells using comparable stimuli. 7. Responses of thalamic neurons to stimulation of the various parts of the spinal cord white matter were tested: contralateral dorsal column; contralateral dorsolateral funiculus, and ipsilateral ventrolateral funiculus. Thalamic neurons showed complex response patterns of excitation and inhibition following stimulation of tracts in different parts of the spinal cord white matter. Some neurons were selectively excited by stimulation of one of these three spinal cord sites. Other cells could be excited by stimulation of more than one part of the spinal cord. The most consistent activation of thalamic neurons of every category was produced by stimulation of the dorsal column. These complex patterns of spinal cord input were confirmed by comparing responses before and after selective lesions of the spinal cord. The results suggest that there are populations of thalamic neurons responding exclusively to dorsal or ventral spinal pathways, whereas other cells receive parallel inputs from multiple spinal pathways.

AB - 1. The activity of 132 neurons in the caudal part of the ventral posterior lateral nucleus (VPL(c)) of the thalamus was recorded from 23 anesthetized monkeys. All single thalamic units that could be excited by electrical search stimuli applied to the contralateral sciatic nerve were investigated. Responses of these cells to mechanical, thermal, and electrical stimuli applied in the periphery indicated that at least half of the sampled cells were nociceptive. 2. Based on responses to graded mechanical stimuli applied to the periphery, 110 of the sampled cells that received a predominant input from cutaneous receptive fields were classified. There were 56 low-threshold, 39 wide dynamic range, and 15 high-threshold cells. The same neurons were also classified into five mechanical types based on a cluster analysis: types 1-5 contained 25, 34, 17, 10, and 24 cells, respectively. The fact that about half the population of cells belonged to either the wide dynamic or the high threshold group (or mechanical types 3-5) suggested that a large population of VPL(c) neurons respond to mechanical nociceptive stimuli either exclusively or preferentially. 3. Responses of 63 thalamic neurons were tested to noxious heat pulses applied to their cutaneous receptive fields with a contact thermostimulator. Of these, 47 cells were excited, whereas only 16 cells did not respond. 4. The peripheral nerve that innervated the receptive field of each of 82 thalamic neurons was stimulated with graded strengths to activate A fibers only or both A and C fibers. All tested cells responded to peripheral A fiber volleys. In addition, 42 of these cells responded to peripheral C fiber volleys. The C fiber responses could be either short lasting (a few hundreds of milliseconds) or long lasting (up to several seconds). 5. The recording sites of 80 cells were reconstructed. Of these, 78 were in the VPL(c) nucleus and the remaining two were in the reticular nucleus of the thalamus. No obvious relationship between the response characteristics and the locations of the cells within the VPL(c) nucleus was found. 6. Sampled thalamic units had a variety of sources of input from the periphery, including both cutaneous and/or deep tissue receptive fields. The majority of the cells, however, had exclusively cutaneous receptive fields. The sizes of the cutaneous receptive fields were often very small, so that nearly half (41%) of the receptive fields of cells sampled occupied an area of skin smaller than half the foot. However, 6 of 46 cells tested could be excited by noxious mechanical stimuli applied to a variety of sites on the body and face. Inhibitory receptive fields were demonstrated for 10 cells using comparable stimuli. 7. Responses of thalamic neurons to stimulation of the various parts of the spinal cord white matter were tested: contralateral dorsal column; contralateral dorsolateral funiculus, and ipsilateral ventrolateral funiculus. Thalamic neurons showed complex response patterns of excitation and inhibition following stimulation of tracts in different parts of the spinal cord white matter. Some neurons were selectively excited by stimulation of one of these three spinal cord sites. Other cells could be excited by stimulation of more than one part of the spinal cord. The most consistent activation of thalamic neurons of every category was produced by stimulation of the dorsal column. These complex patterns of spinal cord input were confirmed by comparing responses before and after selective lesions of the spinal cord. The results suggest that there are populations of thalamic neurons responding exclusively to dorsal or ventral spinal pathways, whereas other cells receive parallel inputs from multiple spinal pathways.

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