Gustatory neural coding in the cortex of the alert cynomolgus macaque: the quality of bitterness.

Abstract

We sought to define the gustatory neural representation in primates for stimuli that humans describe as predominantly bitter. Thus we analyzed the responses of single neurons from the insular cortex of two alert, male cynomolgus macaques in response to the oral application of four basic taste stimuli (glucose, NaCl, HCl, and quinine HCl) and fruit juice, and to a series of 15 other chemicals to which humans ascribe a bitter component. Gustatory neurons occupied a volume of 109 mm3 across an area of 4.0 mm in the anterposterior plane, 4.4 mm in the mediolateral, and 6.2 mm in the dorsoventral. Taste cells represented 161 (8.6%) of the 1881 neurons tested for chemical sensitivity. Fifty of these could be monitored throughout the delivery of the entire stimulus series, and their responses constitute the data of this study. The mean spontaneous discharge rate of the cortical gustatory cells was 3.2 +/- 3.3 spikes/s (range = 0.2-17.7 spikes/s). The mean breadth-of-tuning coefficient was a moderate 0.77 +/- 0.15 (range = 0.25-0.99). Forty-eight neurons responded to taste stimuli with excitation, and two responded with inhibition. Forty-one of the 50 neurons were able to be classified into one of four functional types based on their responses to the four basic stimuli used here. These were sugar (n = 22), salt (n = 7), acid (n = 7), and quinine (n = 5). A two-dimensional space was generated from correlations among the response profiles elicited by the stimuli array. The 16 bitter chemicals formed a coherent group that was most closely related to HCl, moderately to NaCl, and bore no relationship with glucose. Within the bitter stimuli, six formed a subgroup that was most separated from all nonbitter chemicals: quinine HCl, phenlythiocarbamide, propylthiouracil, caffeine, theophylline, and phenylalanine. Humans describe these stimuli as rather purely bitter. Of the remaining 10 bitter compounds, 4 were on the fringe of the bitter group leading to NaCl: MgCl2, CaCl2, NH4Cl, and arginine. Humans characterize these as bitter-salty. Three were on the fringe leading to HCl: urea, cysteine and vitamin B1. Humans call these bitter-sour. The remaining three (nicotine, histidine, and vitamin B2) occupied the center of the bitter group. Taste quality, inferred from the position of each stimulus in the space, correlated well with human descriptions of the same stimuli, reinforcing the value of the macaque as a neural model for human gustation.