Hunger Modulates the Responses to Gustatory Stimuli of Single Neurons in the Caudolateral Orbitofrontal Cortex of the Macaque Monkey
Abstract
In order to determine whether the responsiveness of neurons in the caudolateral orbitofrontal cortex (a secondary cortical gustatory area) is influenced by hunger, the activity evoked by prototypical taste stimuli (glucose, NaCl, HCl, and quinine hydrochloride) and fruit juice was recorded in single neurons in this cortical area before, while, and after cynomolgous macaque monkeys were fed to satiety with glucose or fruit juice. It was found that the responses of the neurons to the taste of the glucose decreased to zero while the monkey ate it to satiety during the course of which his behaviour turned from avid acceptance to active rejection. This modulation of responsiveness of the gustatory responses of the neurons to satiety was not due to peripheral adaptation in the gustatory system or to altered efficacy of gustatory stimulation after satiety was reached, because modulation of neuronal responsiveness by satiety was not seen at earlier stages of the gustatory system, including the nucleus of the solitary tract, the frontal opercular taste cortex, and the insular taste cortex. The decreases in the responsiveness of the neurons were relatively specific to the food with which the monkey had been fed to satiety. For example, in seven experiments in which the monkey was fed glucose solution, neuronal responsiveness decreased to the taste of the glucose but not to the taste of blackcurrant juice. Conversely, in two experiments in which the monkey was fed to satiety with fruit juice, the responses of the neurons decreased to fruit juice but not to glucose. These and earlier findings lead to a proposed neurophysiological mechanism for sensory‐specific satiety in which the information coded by single neurons in the gustatory system becomes more specific through the processing stages consisting of the nucleus of the solitary tract, the taste thalamus, and the frontal opercular and insular taste primary taste cortices, until neuronal responses become relatively specific for the food tasted in the caudolateral orbitofrontal cortex (secondary) taste area. Then sensory‐specific satiety occurs because in this caudolateral orbitofrontal cortex taste area (but not earlier in the taste system) it is a property of the synapses that repeated stimulation results in a decreased neuronal response. Evidence was obtained that gustatory processing involved in thirst also becomes interfaced to motivation in the caudolateral orbitofrontal cortex taste projection area, in that neuronal responses here to water were decreased to zero while water was drunk until satiety was produced.
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In the orbitofrontal cortex and amygdala of monkeys, individual neurons responsive to the taste of specific nutrients such as glucose, amino acids, and fat were modulated by hunger in a sensory-specific manner.
“In the orbitofrontal cortex and amygdala of monkeys, individual neurons responsive to the taste of specific nutrients such as glucose, amino acids, and fat were modulated by hunger in a sensory-specific manner”
From Food reward, hyperphagia, and obesity (2011) · cites this paper as [140]
In devaluation experiments, taste, olfactory, visual and oral texture neurons in the macaque orbitofrontal cortex respond to food when hunger is present, and not after feeding to satiety when the food is no longer rewarding.
“in devaluation experiments, taste, olfactory, visual and oral texture neurons in the macaque orbitofrontal respond to food when hunger is present, and not after feeding to satiety when the food is no longer rewarding (Rolls et al., 1989; Critchley and Rolls, 1996).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Rolls et al., 1989
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- Authors
- Rolls, E. T., Sienkiewicz, Z. J., & Yaxley, S.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Rolls, Edmund T.
- ORCID
- Rolls, Edmund T.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 1989-01
- Volume
- 1
- Issue
- 1
- Pages
- 53-60
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W1973024069
- Cited by
- 466
- References
- 45
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 5 · 2023: 4 · 2022: 10 · 2021: 13 · 2020: 11 · 2019: 14 · 2018: 11 · 2017: 10 · 2016: 14 · 2015: 14 · 2014: 13 · 2013: 20 · 2012: 21
- FWCI
- 3.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Health Sciences › Nursing › Nutrition and Dietetics › Biochemical Analysis and Sensing Techniques
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- gustatory neurons, sensory-specific satiety, satiety, glucose, fruit juice, taste cortex, nucleus tractus solitarius, thirst, water intake, motivation, macaque, single-unit recording, synaptic depression, taste adaptation
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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