Gustatory neural coding in the monkey cortex: stimulus intensity

Abstract

1. We analyzed the activity of single neurons in gustatory cortex of alert cynomolgus monkeys in response to a range of stimulus intensities. Chemicals were deionized water, fruit juice, and several concentrations of the four prototypical taste stimuli: 10(-3)-1.0 M glucose, 10(-3)-1.0 M NaCl, 10(-4)-3 x 10(-2) M HCl, and 10(-5)-3 x 10(-3) M quinine HCl. 2. Taste-evoked responses could be recorded from a cortical gustatory area that measured 2.5 mm in its anteroposterior extent, 6.0 mm dorsoventrally, and 3.0 mm mediolaterally. Taste-responsive cells constituted 62 (3.7%) of the 1,661 neurons tested. Nongustatory cells gave responses associated with mouth movement (10.1%), somatosensory stimulation (2.2%), and approach or anticipation (0.9%). 3. Intensity-response functions were determined across 62 gustatory neurons. Neural thresholds for each stimulus quality conformed well to human psychophysical thresholds. Mean discharge rate was a direct function of stimulus concentration for glucose, NaCl, and quinine HCl. The most effective of the basic stimuli was glucose. 4. Power function exponents were calculated from the responses of neural subgroups most responsive to each basic stimulus. Those for glucose, NaCl, and quinine were within the range of psychophysically derived values. Thus the perceived intensity of each basic quality is presumably based on the activity of the appropriate neural subgroup rather than on the mean activity of all taste cells. 5. The mean breadth-of-tuning (entropy) coefficient for 62 gustatory neurons was 0.65 (range, 0.00-0.98). 6. There was no clear evidence of chemotopic organization in the gustatory cortex. 7. An analysis of taste quality indicated that sweet stimuli evoked patterns of activity that were clearly distinct from those of the nonsweet chemicals. Among the latter group, NaCl was differentiable from HCl and quinine HCl, whose patterns were closely related. 8. The response characteristics of cortical taste cells imply gustatory thresholds and intensity-response functions for the nonhuman primate that conform well to those reported in psychophysical studies of humans, reinforcing the value of this neural model for human taste intensity perception.

Differential Spatial Representation of Taste Modalities in the Rat Gustatory Cortex

“…Electrophysiological studies with rodents or nonhuman primates have shown that increasing the stimulus concentration would usually produce an increase in the firing rate. At the GC level, our results are consistent with the majority of both behavior and electrophysiological experiments (Yaxley et al, 1990;Scott et al, 1991) (but see Stapleton et al, 2006). In fact, we measured the responses to three increasing NaCl concentrations, and we found a monotonic increase in the maximum amplitude and in the size of the response (Fig.…”

Rapid Taste Responses in the Gustatory Cortex during Licking

“…These neurons were very broadly tuned, possessing an average entropy of H ϭ 0.971 Ϯ 0.007 (n ϭ 61). Previous single unit recordings from GC in awake or anesthetized rats have found average entropy values of 0.54 (Yamamoto et al, 1984(Yamamoto et al, , 1989, which approximately matches the 0.56 -0.75 found in awake, nonhuman primates (Yaxley et al, 1990;Scott et al, 1991;Smith-Swintosky et al, 1991). That our entropies were higher than those previously reported can be rationalized, in part, by noting that the gustatory responses often differ significantly from baseline for only a few milliseconds (Figs.…”

“…From the three examples given in Figures 7, 9, and 11, it is seen that the GC responses to increases in concentration were not simply a corresponding monotonic increase in firing rate as was found in some (Yaxley et al, 1990;Scott et al, 1991) but not all (Yamamoto et al, 1984) studies. Rather, neurons often exhibited complex responses to changes in concentration.…”

Representation of Salty Taste Stimulus Concentrations in the Primary Gustatory Area in Humans

“…Ito et al (2001) also noted that reaction time decreased with increases in tastant concentration in subhuman primates; however, the onset latencies of neuronal responses in the PGA (area 3, area G and other cortical areas) were not affected by changes in NaCl concentrations. Scott et al (1991) also noted that, in the macaque, the activity of single cortical neurons increased response magnitudes with increasing tastant concentration, whereas the onset latency for these neurons did not change significantly. The present findings detailing the relationship between NaCl concentrations and the response magnitudes and latencies of the neuronal activity in human area G are consistent with the results obtained from the PGA in monkeys.…”