Gustatory neural coding in the amygdala of the alert macaque monkey

T. R. Scott, Z. Karadi, Y. Oomura, H. Nishino, C. R. Plata-Salaman, L. Lénárd, B. K. Giza, S. Aou

Research output: Contribution to journalArticle

68 Citations (Scopus)

Abstract

1. Neurons in the amygdala are implicated in mediating hedonic appreciation, emotional expression, and conditioning, particularly as these relate to feeding. The amygdala receives projections from the primary taste cortex in monkeys, offering a route by which it could gain access to the gustatory information required to guide feeding behavior. We recorded the activity of 35 neurons in the amygdala of alert rhesus macaques in response to a range of gustatory intensities and qualities to characterize taste- evoked activity in this area. 2. The stimulus array comprised 26 chemicals, including four concentrations of each of the four basic taste stimuli, a series of other sugars, salts, and acids, monosodium glutamate, and orange juice. 3. Neurons responsive to taste stimulation could be found in a 76- mm3 region of the amygdala, centered 9.1 mm lateral to the midline, 14.9 mm anterior to the interaural line, and 25.7 mm below the surface of the dura. They composed 7.2% (35/484) of the cells tested for gustatory sensitivity in the amygdala. 4. The mean spontaneous activity of taste cells was 8.2 ± 2.3 (SE) spikes per second. This rather high level provided an opportunity for reductions from spontaneous rate that was used regularly in the amygdala. When these negative response rates were included, the mean breadth-of-tuning coefficient of this sample of taste cells was 0.82. There was no strong evidence for gustatory neuron types, nor were functionally similar cells located together in a chemotopic arrangement. 5. Responses across 1.5 log units of stimulus concentration were nearly flat, with increasing excitation in some neurons largely offset by increasing inhibition in others. Taking the absolute value of the evoked activity, concentration-response functions rose monotonically to all basic stimuli except HCl, but were not sufficiently steep to account for human psychophysical data. The neural response to HCl did not rise with stimulus concentration within the range used. 6. Neural patterns representing the taste qualities of the basic stimuli were less sharply separated in the amygdala than at lower-order gustatory relays. Glucose elicited activity patterns that were most distinct from those of the nonsweet chemicals; those associated with NaCl were next most distinct. There was no clear separation between the patterns generated by chemicals that humans describe as sour and bitter. Monosodium glutamate evoked responses that did not correlate well with those of any basic stimulus, implying that its quality cannot be subsumed under the four basic tastes. 7. Taste-related activity in the amygdala did not provide an adequate neural basis for the discriminative capacity of humans or monkeys with regard to either stimulus quality or concentration. It is proposed that the amygdala contributes to gustatory processes not by providing precise distinctions among chemicals, but by imparting hedonic appreciation and emotional significance to the taste experience.

Original languageEnglish
Pages (from-to)1810-1820
Number of pages11
JournalJournal of Neurophysiology
Volume69
Issue number6
Publication statusPublished - 1993

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Macaca
Amygdala
Haplorhini
Neurons
Sodium Glutamate
Pleasure
Sugar Acids
Access to Information
Feeding Behavior
Macaca mulatta

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Scott, T. R., Karadi, Z., Oomura, Y., Nishino, H., Plata-Salaman, C. R., Lénárd, L., ... Aou, S. (1993). Gustatory neural coding in the amygdala of the alert macaque monkey. Journal of Neurophysiology, 69(6), 1810-1820.

Gustatory neural coding in the amygdala of the alert macaque monkey. / Scott, T. R.; Karadi, Z.; Oomura, Y.; Nishino, H.; Plata-Salaman, C. R.; Lénárd, L.; Giza, B. K.; Aou, S.

In: Journal of Neurophysiology, Vol. 69, No. 6, 1993, p. 1810-1820.

Research output: Contribution to journalArticle

Scott, TR, Karadi, Z, Oomura, Y, Nishino, H, Plata-Salaman, CR, Lénárd, L, Giza, BK & Aou, S 1993, 'Gustatory neural coding in the amygdala of the alert macaque monkey', Journal of Neurophysiology, vol. 69, no. 6, pp. 1810-1820.
Scott TR, Karadi Z, Oomura Y, Nishino H, Plata-Salaman CR, Lénárd L et al. Gustatory neural coding in the amygdala of the alert macaque monkey. Journal of Neurophysiology. 1993;69(6):1810-1820.
Scott, T. R. ; Karadi, Z. ; Oomura, Y. ; Nishino, H. ; Plata-Salaman, C. R. ; Lénárd, L. ; Giza, B. K. ; Aou, S. / Gustatory neural coding in the amygdala of the alert macaque monkey. In: Journal of Neurophysiology. 1993 ; Vol. 69, No. 6. pp. 1810-1820.
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