Neural coding of gustatory information in the thalamus of Macaca mulatta

T. C. Pritchard, R. B. Hamilton, R. Norgren

Research output: Contribution to journalArticle

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Abstract

Extracellular action potential were recorded from single neurons in the parvicellular division of the ventroposteromedial (VPMpc) nucleus of the thalamus of restrained, but alert, Old World monkeys during gustatory, tactile, and thermal stimulation of the oral cavity. In contrast to previous report in anesthetized or paralyzed rats, the spontaneous activity of these neurons was brisk and their evoked responses robust. Each of 50 taste-responsive neurons was tested with 1.0 M sucrose, 0.1 M NaCl, 0.003 M HCl, and 0.001 M QHCl before other concentrations of the same stimuli were used. Sucrose, which was effective in 80% of the neurons tested, evoked the largest responses of the 4 standard gustatory stimuli (16.1 spikes/s). The average response to NaCl, an effective stimulus for 44% of the neurons in the sample, was 7.5 spiks/s. HCl and QHCl, which few neurons responded to, typically evoked smaller respones. Most of the neurons tested showed monotonic intensity-response (I-R) functions. The power functions showed about the same degree of compression (range = 0.39-0.53), which has been described previously for brain stem neurons in anesthetized rodents. Only 9.1% of the responses were inhibitory, and there was no tendency for these responses to be associated with either specific neurons or stimuli. These data suggest that quality coding of gustatory information in the thalamus is not radically different from that seen among lower-order neurons in other species. Through the use of hierarchical cluster analysis, it was possible to divide the neuron sample into 2 groups, one of which consisted of sucrose-best neurons that had an average entropy value of 0.56. The neurons in the other group, though more heterogeneous, showed either primary or side-band sensitivity to NaCl. The average breadth of responsiveness of the 50 thalamic neurons as described by the entropy coefficient was 0.73. In addition to gustatory neurons, tactile (n = 15), thermal (n = 1), and nonresponsive (n = 25) neurons also were located within VPMpc. An additional 48 neurons that could not be classified as either sensory or motor in nature, inhibited their bursting spontaneous discharge just prior to the onset of fluid stimulation. Only 2 of these neurons demonstrated differential chemical sensitivity. The presence of these nongustatory neurons within the thalamic taste area suggests that the traditional characterization of VPMpc as a gustatory relay may understate its role in ingestive behavior and ignore other noningestive functions of the area.

Original languageEnglish (US)
Pages (from-to)1-14
Number of pages14
JournalJournal of neurophysiology
Volume61
Issue number1
DOIs
StatePublished - Jan 1 1989

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Macaca mulatta
Thalamus
Neurons
Sucrose
Touch
Entropy
Hot Temperature
Cercopithecidae

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

Cite this

Pritchard, T. C. ; Hamilton, R. B. ; Norgren, R. / Neural coding of gustatory information in the thalamus of Macaca mulatta. In: Journal of neurophysiology. 1989 ; Vol. 61, No. 1. pp. 1-14.
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Neural coding of gustatory information in the thalamus of Macaca mulatta. / Pritchard, T. C.; Hamilton, R. B.; Norgren, R.

In: Journal of neurophysiology, Vol. 61, No. 1, 01.01.1989, p. 1-14.

Research output: Contribution to journalArticle

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N2 - Extracellular action potential were recorded from single neurons in the parvicellular division of the ventroposteromedial (VPMpc) nucleus of the thalamus of restrained, but alert, Old World monkeys during gustatory, tactile, and thermal stimulation of the oral cavity. In contrast to previous report in anesthetized or paralyzed rats, the spontaneous activity of these neurons was brisk and their evoked responses robust. Each of 50 taste-responsive neurons was tested with 1.0 M sucrose, 0.1 M NaCl, 0.003 M HCl, and 0.001 M QHCl before other concentrations of the same stimuli were used. Sucrose, which was effective in 80% of the neurons tested, evoked the largest responses of the 4 standard gustatory stimuli (16.1 spikes/s). The average response to NaCl, an effective stimulus for 44% of the neurons in the sample, was 7.5 spiks/s. HCl and QHCl, which few neurons responded to, typically evoked smaller respones. Most of the neurons tested showed monotonic intensity-response (I-R) functions. The power functions showed about the same degree of compression (range = 0.39-0.53), which has been described previously for brain stem neurons in anesthetized rodents. Only 9.1% of the responses were inhibitory, and there was no tendency for these responses to be associated with either specific neurons or stimuli. These data suggest that quality coding of gustatory information in the thalamus is not radically different from that seen among lower-order neurons in other species. Through the use of hierarchical cluster analysis, it was possible to divide the neuron sample into 2 groups, one of which consisted of sucrose-best neurons that had an average entropy value of 0.56. The neurons in the other group, though more heterogeneous, showed either primary or side-band sensitivity to NaCl. The average breadth of responsiveness of the 50 thalamic neurons as described by the entropy coefficient was 0.73. In addition to gustatory neurons, tactile (n = 15), thermal (n = 1), and nonresponsive (n = 25) neurons also were located within VPMpc. An additional 48 neurons that could not be classified as either sensory or motor in nature, inhibited their bursting spontaneous discharge just prior to the onset of fluid stimulation. Only 2 of these neurons demonstrated differential chemical sensitivity. The presence of these nongustatory neurons within the thalamic taste area suggests that the traditional characterization of VPMpc as a gustatory relay may understate its role in ingestive behavior and ignore other noningestive functions of the area.

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