Gustatory responses of neurons in the nucleus of the solitary tract of behaving rats

K. Nakamura, R. Norgren

Research output: Contribution to journalArticle

48 Scopus citations

Abstract

1. The activity of 117 single neurons was recorded in the rostral nucleus of the solitary tract (NST) and tested with each of four standard chemical stimuli [sucrose, NaCl, citric acid, and quinine HCl (QHCl)] and distilled water in awake, behaving rats. In 101 of these neurons, at least one sapid stimulus elicited a significant taste response. The mean spontaneous rate of the taste neurons was 4.1 ± 5.8 (SD) spikes/s. The mean response magnitudes were as follows: sucrose, 10.6 ± 11.7; NaCl, 8.6 ± 14.6; citric acid, 6.2 ± 7.8; and QHCl, 2.4 ± 6.6 spikes/s. 2. On the basis of their largest response, 42 taste neurons were classified as sucrose-best, 25 as NaCl-best, 30 as citric acid-best, and 4 as QHCl-best. The mean spontaneous rates for these categories were 4.9 ± 6.2 for sucrose-best cells, 5.8 ± 7.4 for NaCl-best, 1.6 ± 2.0 for citric acid-best, and 5.8 ± 6.0 spikes/s for QHCl-best. The spontaneous rate of the citric acid-best neurons was significantly lower than that of the other categories. 3. At the standard concentrations, 45 taste cells (44.6%) responded significantly to only one of the gustatory stimuli. Of the 30 acid-best neurons, 23 (76.7%) responded only to citric acid. For sucrose-best cells, specific sensitivity was less common (18/42, 42.9%), and for NaCl-best neurons, it was relatively uncommon (3/25, 12%). One of the 4 QHCl-best neurons was specific. In a concentration series, more than one-half of the 19 specific neurons tested responded to only one chemical at any strength. 4. The mean entropy for the excitatory responses of all gustatory neurons was 0.60. Citric acid-best cells showed the least breadth of responsiveness (0.49), sucrose-best cells were somewhat broader (0.56), but NaCl-best and QHCl-best cells were considerably less selective (0.77 and 0.79, respectively). Inhibition was observed infrequently and never reached the criterion for significance. 5. In the hierarchical cluster analysis, the four largest clusters segregated neurons primarily by best-stimulus category. The major exception to this was a group of sucrose-best neurons that also responded to NaCl and were grouped with the NaCl-best neurons. In a two-dimensional space, the specific taste neurons, those that responded to only one of the four standard sapid stimuli, remained in well-separated groups. These specific groups, however, were joined in a ring-like formation by other neurons that responded to more than one of the sapid stimuli. 6. The present sample of NST taste neurons recorded from awake, behaving rats exhibited several similarities to, and only one striking difference from, samples taken from anesthetized preparations. The mean spontaneous firing in awake rats was higher (4.1 vs. 2.34 spike/s), but the variance in both samples was high. The distribution of best-stimulus categories was quite similar in the two samples. Except for acid-best cells, the mean breadth of responsiveness also was similar. The acid-best neurons from awake rats were more narrowly tuned (0.49 vs. 0.80), but these data derive from different concentrations of different acids. The only striking difference between the two samples was in the percentage of neurons that responded to only one stimulus, the so-called specific neurons-34% in the chronic sample, 5.5% of the acute cells (on the basis of a common statistical criterion of ±2.0 SD). 7. The same sample of NST taste neurons differed from those observed in the parabrachial nuclei (PBN) of similar awake, behaving preparations. The spontaneous firing rate in the NST was low compared with that of PBN neurons (4.1 vs. 13.4 spikes/s). Responsiveness to NaCl is reduced in the NST relative to the PBN, whereas responsiveness to citric acid is increased. In PBN gustatory neurons, 71% were NaCl-best, 24% sucrose-best, 3% citric acid-best, and 2% QHCl-best. In the NST, the comparable figures were 25% NaCl-best, 41% sucrose-best, 30% acid-best, and 4% QHCl-best. The breadth of NaCl-best neurons becomes narrower from NST to PBN (0.57). Acid-best neurons are not only more common in the NST, they also are more narrowly tuned (NST = 0.49; PBN = 0.89). Sodium-best neurons are less common in the NST, but more broadly tuned (NST = 0.77; PBN = 0.57). Sucrose-best neurons do not differ (0.56 vs. 0.55).

Original languageEnglish (US)
Pages (from-to)1232-1248
Number of pages17
JournalJournal of neurophysiology
Volume66
Issue number4
DOIs
StatePublished - 1991

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)
  • Physiology

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