Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey

Abstract

The responses of 165 single taste neurons in the anterior operculum of the alert cynomolgus monkey were analyzed. Chemicals were deionized water, blackcurrant juice, and the four basic taste stimuli: glucose, NaCl, HCl, and quinine HCl. Taste-evoked responses could be recorded from an opercular region that measured approximately 4.0 mm in its anteroposterior extent, 2.0 mm mediolaterally, and 3.0 mm dorsoventrally. Within this area, taste-responsive neurons were sparsely distributed such that multiunit activity was rarely encountered and neuronal isolation was readily achieved. Intensity-response functions were determined for nine cells.In each case, the lowest concentration of the dynamic response range conformed well to human electrophysiological and psychophysical thresholds for the basic taste stimuli. There was some evidence of chemotopic organization. Cells that responded best to glucose tended to be distributed toward the anterior operculum, whereas most acid-sensitive neurons were located more posteriorly. The proportion of cells responding best to NaCl peaked in the middle of the area, whereas quinine sensitivity was rather evenly distributed throughout. Opercular neurons in the monkey showed moderate breadth of sensitivity compared with taste cells of other species and at other synaptic levels. A breadth-of-tuning coefficient was calculated for each neuron. This is a metric that can range from 0.0 for a cell that responds specifically to only one of the four basic stimuli to 1.0 for one that responds equally to all four stimuli. The mean coefficient for 165 cells in the operculum was 0.67 (range = 0.12-0.99). Efforts were made to determine whether neurons could be divided into a discrete number of types, as defined by their responsiveness to the stimulus array used here. It was concluded that most taste cells may be assigned to a small number of groups, each of which is statistically independent of the others, but within which the constituent neurons are not identical. An analysis of taste quality indicated that the sweet and salty stimuli evoked patterns of activity that were significantly intercorrelated. Similarly, patterns representing HCl, quinine HCl, and water were related.