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

We sought to define the gustatory neural representation in primates for sti muli that humans describe as predominantly bitter. Thus we analyzed the res ponses of single neurons from the insular cortex of two alert, male cynomol gus macaques in response to the oral application of four basic taste stimul i (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 n eurons occupied a volume of 109 mm(3) across an area of 4.0 mm in the anter posterior 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 chemica l sensitivity. Fifty of these could be monitored throughout the delivery of the entire stimulus series, and their responses constitute the data of thi s study. The mean spontaneous discharge rate of the cortical gustatory cell s 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 responde d with inhibition. Forty-one of the 50 neurons were able to be classified i nto 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 correlation s among the response profiles elicited by the stimuli array. The 16 bitter chemicals formed a coherent group that was most closely related to HCl, mod erately to NaCl, and bore no relationship with. glucose. Within the bitter stimuli, six formed a subgroup that was most separated from all nonbitter c hemicals: quinine HCl, phenlythiocarbamide, propylthiouracil, caffeine, the ophylline, and phenylalanine. Humans describe these stimuli as rather purel y 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 ch aracterize these as bitter-salty. Three were on the fringe leading to HCl: urea, cysteine and vitamin BI. Humans call these bitter-sour. The remaining three (nicotine, histidine, and vitamin B-2) occupied the center of the bi tter group. Taste quality, inferred from the position of each stimulus in t he space, correlated well with human descriptions of the same stimuli, rein forcing the value of the macaque as a neural model for human gustation.