Taste responses of cortical neurons in freely ingesting rats

T. Yamamoto, R. Matsuo, Y. Kiyomitsu, R. Kitamura

Research output: Contribution to journalArticle

125 Citations (Scopus)

Abstract

1. Activities of 35 taste-responsive neurons in the cortical gustatory area were recorded with chronically implanted fine wires in freely ingesting Wistar rats. Quantitative analyses were performed on responses to distilled water, food solution, and four taste stimuli, sucrose, NaCl, HCl, and quinine hydrochloride. 2. Taste-responsive neurons were classified into type-1 and type-2 groups according to the response patterns to licking of the six taste stimuli. Type-1 neurons (n = 29) responded in excitatory or inhibitory directions to one or more of the taste stimuli. Type-2 neurons (n = 6) showed responses in different directions depending upon palatability of the liquids to rats: neurons showing excitatory (or inhibitory) responses to palatable stimuli exhibited inhibitory (or excitatory) responses to unpalatable stimuli. 3. Correlation coefficients of responses to pairs of stimuli across neurons suggested that palatable stimuli( water, food solution, sucrose, and NaCl) and unpalatable stimuli (HCl and quinine) elicited reciprocal (excitatory vs. inhibitory) responses in type-2 neurons, whereas type-1 neurons showed positively correlated responses to specific combinations of stimuli such as food solution and NaCl, sucrose and HCl, and NaCl and quinine, and HCl and quinine. 4. A tendency toward equalization of effectiveness in eliciting responses among the four basic taste stimuli was detected on the cortex. The ratios of mean evoked responses in 29 type-1 neurons in comparison with spontaneous rate (4.4 spikes/s) were 1.7, 1.9, 1.8, and 1.9 for sucrose, NaCl, HCl, and quinine, respectively. 5. The breadth of responsiveness to the four basic taste stimuli was quantified by means of the entropy measure introduced by Smith and Travers (33). The mean entropy value was 0.540 for 29 type-1 neurons, which was similar to 0.588 previously reported for rat chorda tympani fibers, suggesting that breadth of tuning is not more narrowly tuned in a higher level of the gustatory system in the rat. 6. Convergent inputs of other sensory modalities were detected exclusively in type-1 neurons. Thirteen (45%) of 29 type-1 neurons also responded to cold and/or warm water, but none of 6 type-2 neurons responded to thermal stimuli. Two (7%) of 29 type-1 neurons responded to almond and acetic acid odors, but the 6 type-2 neurons did not. Two (13%) of 16 type-1 neurons responded to interperitoneal injection of LiCl, which is known to induce gastrointestinal disorders, with a latency of ~5 min, but 5 type-2 neurons tested were not responsive to this stimulation. 7. Effects of conditioned taste aversion learning on neural responses were examined in 16 type-1 and 4 type-2 neurons. Three of the 16 type-1 neurons showed enhanced responses to a conditioned taste after acquisition of aversion, and all the 4 type-2 neurons exhibited alteration of the response direction (from excitatory to inhibitory or from inhibitory to excitatory) equivalent to that shown by aversive stimuli. 8. A regional difference in sensitivity in the cortex among the four basic taste qualities (chemotopic organization) was detected. When type-1 neurons were classified into best-stimulus categories, sucrose-best, NaCl-best, HCl-best, and quinine-best neurons tended to be located in this order from anterior to posterior direction within the taste area. Type-2 neurons were located in the periphery of the taste area. 9 These results suggest that taste quality is coded by type-1 neurons and the hedonic tone of taste stimuli is differentiated by type-2 neurons. The present study confirmed some of the findings previously obtained from cortical taste-responsive neurons in acutely anesthetized rats, but also revealed new response characteristics which were closely related to taste-mediated behaviors. The present results were also compared with the data obtained by other investigators from cortical taste-responsive neurons in alert monkeys.

Original languageEnglish
Pages (from-to)1244-1258
Number of pages15
JournalJournal of Neurophysiology
Volume61
Issue number6
Publication statusPublished - 1989
Externally publishedYes

Fingerprint

Neurons
Quinine
Sucrose
Entropy
Food
Water
Pleasure
Acetic Acid
Haplorhini

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Yamamoto, T., Matsuo, R., Kiyomitsu, Y., & Kitamura, R. (1989). Taste responses of cortical neurons in freely ingesting rats. Journal of Neurophysiology, 61(6), 1244-1258.

Taste responses of cortical neurons in freely ingesting rats. / Yamamoto, T.; Matsuo, R.; Kiyomitsu, Y.; Kitamura, R.

In: Journal of Neurophysiology, Vol. 61, No. 6, 1989, p. 1244-1258.

Research output: Contribution to journalArticle

Yamamoto, T, Matsuo, R, Kiyomitsu, Y & Kitamura, R 1989, 'Taste responses of cortical neurons in freely ingesting rats', Journal of Neurophysiology, vol. 61, no. 6, pp. 1244-1258.
Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R. Taste responses of cortical neurons in freely ingesting rats. Journal of Neurophysiology. 1989;61(6):1244-1258.
Yamamoto, T. ; Matsuo, R. ; Kiyomitsu, Y. ; Kitamura, R. / Taste responses of cortical neurons in freely ingesting rats. In: Journal of Neurophysiology. 1989 ; Vol. 61, No. 6. pp. 1244-1258.
@article{7428f1e26f564feab8fd75a33186adf3,
title = "Taste responses of cortical neurons in freely ingesting rats",
abstract = "1. Activities of 35 taste-responsive neurons in the cortical gustatory area were recorded with chronically implanted fine wires in freely ingesting Wistar rats. Quantitative analyses were performed on responses to distilled water, food solution, and four taste stimuli, sucrose, NaCl, HCl, and quinine hydrochloride. 2. Taste-responsive neurons were classified into type-1 and type-2 groups according to the response patterns to licking of the six taste stimuli. Type-1 neurons (n = 29) responded in excitatory or inhibitory directions to one or more of the taste stimuli. Type-2 neurons (n = 6) showed responses in different directions depending upon palatability of the liquids to rats: neurons showing excitatory (or inhibitory) responses to palatable stimuli exhibited inhibitory (or excitatory) responses to unpalatable stimuli. 3. Correlation coefficients of responses to pairs of stimuli across neurons suggested that palatable stimuli( water, food solution, sucrose, and NaCl) and unpalatable stimuli (HCl and quinine) elicited reciprocal (excitatory vs. inhibitory) responses in type-2 neurons, whereas type-1 neurons showed positively correlated responses to specific combinations of stimuli such as food solution and NaCl, sucrose and HCl, and NaCl and quinine, and HCl and quinine. 4. A tendency toward equalization of effectiveness in eliciting responses among the four basic taste stimuli was detected on the cortex. The ratios of mean evoked responses in 29 type-1 neurons in comparison with spontaneous rate (4.4 spikes/s) were 1.7, 1.9, 1.8, and 1.9 for sucrose, NaCl, HCl, and quinine, respectively. 5. The breadth of responsiveness to the four basic taste stimuli was quantified by means of the entropy measure introduced by Smith and Travers (33). The mean entropy value was 0.540 for 29 type-1 neurons, which was similar to 0.588 previously reported for rat chorda tympani fibers, suggesting that breadth of tuning is not more narrowly tuned in a higher level of the gustatory system in the rat. 6. Convergent inputs of other sensory modalities were detected exclusively in type-1 neurons. Thirteen (45{\%}) of 29 type-1 neurons also responded to cold and/or warm water, but none of 6 type-2 neurons responded to thermal stimuli. Two (7{\%}) of 29 type-1 neurons responded to almond and acetic acid odors, but the 6 type-2 neurons did not. Two (13{\%}) of 16 type-1 neurons responded to interperitoneal injection of LiCl, which is known to induce gastrointestinal disorders, with a latency of ~5 min, but 5 type-2 neurons tested were not responsive to this stimulation. 7. Effects of conditioned taste aversion learning on neural responses were examined in 16 type-1 and 4 type-2 neurons. Three of the 16 type-1 neurons showed enhanced responses to a conditioned taste after acquisition of aversion, and all the 4 type-2 neurons exhibited alteration of the response direction (from excitatory to inhibitory or from inhibitory to excitatory) equivalent to that shown by aversive stimuli. 8. A regional difference in sensitivity in the cortex among the four basic taste qualities (chemotopic organization) was detected. When type-1 neurons were classified into best-stimulus categories, sucrose-best, NaCl-best, HCl-best, and quinine-best neurons tended to be located in this order from anterior to posterior direction within the taste area. Type-2 neurons were located in the periphery of the taste area. 9 These results suggest that taste quality is coded by type-1 neurons and the hedonic tone of taste stimuli is differentiated by type-2 neurons. The present study confirmed some of the findings previously obtained from cortical taste-responsive neurons in acutely anesthetized rats, but also revealed new response characteristics which were closely related to taste-mediated behaviors. The present results were also compared with the data obtained by other investigators from cortical taste-responsive neurons in alert monkeys.",
author = "T. Yamamoto and R. Matsuo and Y. Kiyomitsu and R. Kitamura",
year = "1989",
language = "English",
volume = "61",
pages = "1244--1258",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "6",

}

TY - JOUR

T1 - Taste responses of cortical neurons in freely ingesting rats

AU - Yamamoto, T.

AU - Matsuo, R.

AU - Kiyomitsu, Y.

AU - Kitamura, R.

PY - 1989

Y1 - 1989

N2 - 1. Activities of 35 taste-responsive neurons in the cortical gustatory area were recorded with chronically implanted fine wires in freely ingesting Wistar rats. Quantitative analyses were performed on responses to distilled water, food solution, and four taste stimuli, sucrose, NaCl, HCl, and quinine hydrochloride. 2. Taste-responsive neurons were classified into type-1 and type-2 groups according to the response patterns to licking of the six taste stimuli. Type-1 neurons (n = 29) responded in excitatory or inhibitory directions to one or more of the taste stimuli. Type-2 neurons (n = 6) showed responses in different directions depending upon palatability of the liquids to rats: neurons showing excitatory (or inhibitory) responses to palatable stimuli exhibited inhibitory (or excitatory) responses to unpalatable stimuli. 3. Correlation coefficients of responses to pairs of stimuli across neurons suggested that palatable stimuli( water, food solution, sucrose, and NaCl) and unpalatable stimuli (HCl and quinine) elicited reciprocal (excitatory vs. inhibitory) responses in type-2 neurons, whereas type-1 neurons showed positively correlated responses to specific combinations of stimuli such as food solution and NaCl, sucrose and HCl, and NaCl and quinine, and HCl and quinine. 4. A tendency toward equalization of effectiveness in eliciting responses among the four basic taste stimuli was detected on the cortex. The ratios of mean evoked responses in 29 type-1 neurons in comparison with spontaneous rate (4.4 spikes/s) were 1.7, 1.9, 1.8, and 1.9 for sucrose, NaCl, HCl, and quinine, respectively. 5. The breadth of responsiveness to the four basic taste stimuli was quantified by means of the entropy measure introduced by Smith and Travers (33). The mean entropy value was 0.540 for 29 type-1 neurons, which was similar to 0.588 previously reported for rat chorda tympani fibers, suggesting that breadth of tuning is not more narrowly tuned in a higher level of the gustatory system in the rat. 6. Convergent inputs of other sensory modalities were detected exclusively in type-1 neurons. Thirteen (45%) of 29 type-1 neurons also responded to cold and/or warm water, but none of 6 type-2 neurons responded to thermal stimuli. Two (7%) of 29 type-1 neurons responded to almond and acetic acid odors, but the 6 type-2 neurons did not. Two (13%) of 16 type-1 neurons responded to interperitoneal injection of LiCl, which is known to induce gastrointestinal disorders, with a latency of ~5 min, but 5 type-2 neurons tested were not responsive to this stimulation. 7. Effects of conditioned taste aversion learning on neural responses were examined in 16 type-1 and 4 type-2 neurons. Three of the 16 type-1 neurons showed enhanced responses to a conditioned taste after acquisition of aversion, and all the 4 type-2 neurons exhibited alteration of the response direction (from excitatory to inhibitory or from inhibitory to excitatory) equivalent to that shown by aversive stimuli. 8. A regional difference in sensitivity in the cortex among the four basic taste qualities (chemotopic organization) was detected. When type-1 neurons were classified into best-stimulus categories, sucrose-best, NaCl-best, HCl-best, and quinine-best neurons tended to be located in this order from anterior to posterior direction within the taste area. Type-2 neurons were located in the periphery of the taste area. 9 These results suggest that taste quality is coded by type-1 neurons and the hedonic tone of taste stimuli is differentiated by type-2 neurons. The present study confirmed some of the findings previously obtained from cortical taste-responsive neurons in acutely anesthetized rats, but also revealed new response characteristics which were closely related to taste-mediated behaviors. The present results were also compared with the data obtained by other investigators from cortical taste-responsive neurons in alert monkeys.

AB - 1. Activities of 35 taste-responsive neurons in the cortical gustatory area were recorded with chronically implanted fine wires in freely ingesting Wistar rats. Quantitative analyses were performed on responses to distilled water, food solution, and four taste stimuli, sucrose, NaCl, HCl, and quinine hydrochloride. 2. Taste-responsive neurons were classified into type-1 and type-2 groups according to the response patterns to licking of the six taste stimuli. Type-1 neurons (n = 29) responded in excitatory or inhibitory directions to one or more of the taste stimuli. Type-2 neurons (n = 6) showed responses in different directions depending upon palatability of the liquids to rats: neurons showing excitatory (or inhibitory) responses to palatable stimuli exhibited inhibitory (or excitatory) responses to unpalatable stimuli. 3. Correlation coefficients of responses to pairs of stimuli across neurons suggested that palatable stimuli( water, food solution, sucrose, and NaCl) and unpalatable stimuli (HCl and quinine) elicited reciprocal (excitatory vs. inhibitory) responses in type-2 neurons, whereas type-1 neurons showed positively correlated responses to specific combinations of stimuli such as food solution and NaCl, sucrose and HCl, and NaCl and quinine, and HCl and quinine. 4. A tendency toward equalization of effectiveness in eliciting responses among the four basic taste stimuli was detected on the cortex. The ratios of mean evoked responses in 29 type-1 neurons in comparison with spontaneous rate (4.4 spikes/s) were 1.7, 1.9, 1.8, and 1.9 for sucrose, NaCl, HCl, and quinine, respectively. 5. The breadth of responsiveness to the four basic taste stimuli was quantified by means of the entropy measure introduced by Smith and Travers (33). The mean entropy value was 0.540 for 29 type-1 neurons, which was similar to 0.588 previously reported for rat chorda tympani fibers, suggesting that breadth of tuning is not more narrowly tuned in a higher level of the gustatory system in the rat. 6. Convergent inputs of other sensory modalities were detected exclusively in type-1 neurons. Thirteen (45%) of 29 type-1 neurons also responded to cold and/or warm water, but none of 6 type-2 neurons responded to thermal stimuli. Two (7%) of 29 type-1 neurons responded to almond and acetic acid odors, but the 6 type-2 neurons did not. Two (13%) of 16 type-1 neurons responded to interperitoneal injection of LiCl, which is known to induce gastrointestinal disorders, with a latency of ~5 min, but 5 type-2 neurons tested were not responsive to this stimulation. 7. Effects of conditioned taste aversion learning on neural responses were examined in 16 type-1 and 4 type-2 neurons. Three of the 16 type-1 neurons showed enhanced responses to a conditioned taste after acquisition of aversion, and all the 4 type-2 neurons exhibited alteration of the response direction (from excitatory to inhibitory or from inhibitory to excitatory) equivalent to that shown by aversive stimuli. 8. A regional difference in sensitivity in the cortex among the four basic taste qualities (chemotopic organization) was detected. When type-1 neurons were classified into best-stimulus categories, sucrose-best, NaCl-best, HCl-best, and quinine-best neurons tended to be located in this order from anterior to posterior direction within the taste area. Type-2 neurons were located in the periphery of the taste area. 9 These results suggest that taste quality is coded by type-1 neurons and the hedonic tone of taste stimuli is differentiated by type-2 neurons. The present study confirmed some of the findings previously obtained from cortical taste-responsive neurons in acutely anesthetized rats, but also revealed new response characteristics which were closely related to taste-mediated behaviors. The present results were also compared with the data obtained by other investigators from cortical taste-responsive neurons in alert monkeys.

UR - http://www.scopus.com/inward/record.url?scp=0024315752&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0024315752&partnerID=8YFLogxK

M3 - Article

VL - 61

SP - 1244

EP - 1258

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 6

ER -