The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger
Abstract
(1) In order to determine whether the responsiveness of neurons in the insular gustatory cortex is influenced by hunger, neuronal activity was analysed in it while macaque monkeys (Macaca fascicularis) were fed to satiety. The responses of single neurons in the insular gustatory cortex to the protypical taste stimuli glucose, NaCl, HCl and quinine HCl, and to fruit juice, were measured before, while, and after the monkey was fed to satiety with glucose or fruit juice. (2) While behavior turned from avid acceptance to active rejection upon repletion, the responsiveness of the neurons to the stimulus array, including the satiating solution, was unmodified. (3) It is concluded that in the insular gustatory cortex, neuronal responses to gustatory stimuli are not influenced by the normal transition from hunger to satiety. This is in contrast to the responses of a population of neurons recorded in the hypothalamus, which only respond to the taste of food when the monkey is hungry. Thus the neurons in the insular gustatory cortex are involved in a motivation-independent analysis of gustatory stimuli, whereas the hypothalamic neurons may be more closely related to the influence of motivational state on behavioral responsiveness to gustatory stimuli.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The insular primary taste cortex represents what the taste is independently of its reward value.
“the insular primary taste cortex represents what the taste is independently of its reward value (Yaxley et al., 1988; Rolls, 2015, 2016c, 2019c).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Yaxley et al., 1988
Cites
Cabanac, M. (1971) · Science · doi:10.1126/science.173.4002.1103 · Cited by 1,521 · see citing works
Insula of the old world monkey. III: Efferent cortical output and comments on function
Mesulam, M. ‐., & Mufson, E. J. (1982) · Journal of Comparative Neurology · doi:10.1002/cne.902120104 · Cited by 1,013 · see citing works
Silver Staining of Myelin by Means of Physical Development
Gallyas, F. (1979) · Neurological Research · doi:10.1080/01616412.1979.11739553 · Cited by 936 · see citing works
Sensory specific satiety in man☆
Rolls, B. J., Rolls, E. T., Rowe, E. A., & Sweeney, K. F. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90310-3 · Cited by 884 · see citing works
Self-citationThe frontal granular cortex and behavior
Pribram, K. H. (1965) · Neuropsychologia · doi:10.1016/0028-3932(65)90022-9 · Cited by 705 · see citing works
Mesulam, M. M., & Mufson, E. J. (1982) · The Journal of Comparative Neurology · doi:10.1002/cne.902120102 · Cited by 654 · see citing works
Variety in a meal enhances food intake in man.
Rolls, B., Rowe, E. A., Rolls, E., Kingston, B., Megson, A., & Gunary, R. (1981) · Physiology and Behavior · doi:10.1016/0031-9384(81)90014-7 · Cited by 621 · see citing works
Self-citationCortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta)
Aggleton, J. P., Burton, M. J., & Passingham, R. E. (1980) · Brain Research · doi:10.1016/0006-8993(80)90279-6 · Cited by 610 · see citing works
Glass-coated platinum-plated tungsten microelectrodes
Merrill, E. G., & Ainsworth, A. (1972) · Medical & Biological Engineering & Computing · doi:10.1007/bf02476084 · Cited by 597 · see citing works
Insula of the old world monkey. II: Afferent cortical input and comments on the claustrum
Mufson, E. J., & Mesulam, M. ‐. (1982) · Journal of Comparative Neurology · doi:10.1002/cne.902120103 · Cited by 559 · see citing works
The nucleus of the solitary tract in the monkey: Projections to the thalamus and brain stem nuclei
Beckstead, R. M., Morse, J. R., & Norgren, R. (1980) · The Journal of Comparative Neurology · doi:10.1002/cne.901900205 · Cited by 445 · see citing works
Food intake and chemical senses
勝木, 保. (1977) · University of Tokyo Press eBooks · Cited by 431 · see citing works
How sensory properties of foods affect human feeding behavior
Rolls, B. J., Rowe, E. A., & Rolls, E. T. (1982) · Physiology & Behavior · doi:10.1016/0031-9384(82)90259-1 · Cited by 419 · see citing works
Self-citationBeckstead, R. M., & Norgren, R. (1979) · The Journal of Comparative Neurology · doi:10.1002/cne.901840303 · Cited by 400 · see citing works
The Psychobiology of Human Food Selection
Barker, L. M. (1982) · Medical Entomology and Zoology · Cited by 315 · see citing works
Rolls, E. T., Sanghera, M. K., & Roper-Hall, A. (1979) · Brain Research · doi:10.1016/0006-8993(79)90010-6 · Cited by 312 · see citing works
Self-citationInsular interconnections with the amygdala in the rhesus monkey
Mufson, E. J., Mesulam, M. ‐., & Pandya, D. Ν. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90184-6 · Cited by 292 · see citing works
Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis
Pritchard, T. C., Hamilton, R. B., Morse, J. R., & Norgren, R. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902440208 · Cited by 292 · see citing works
Hypothalamic neuronal responses associated with the sight of food
Rolls, E. T., Burton, M. J., & Mora, F. (1976) · Brain Research · doi:10.1016/0006-8993(76)91048-9 · Cited by 290 · see citing works
Self-citationVisual responses of neurons in the dorsolateral amygdala of the alert monkey.
Sanghera, M., Rolls, E., & Roper-Hall, A. (1979) · Experimental Neurology · doi:10.1016/0014-4886(79)90175-4 · Cited by 287 · see citing works
Self-citationThe Neural and Molecular Bases of Learning
Frégnac, Y. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90158-0 · Cited by 277 · see citing works
The afferent connections of the substantia innominata in the monkey,Macaca fascicularis
Russchen, F. T., Amaral, D., & Price, J. L. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902420102 · Cited by 270 · see citing works
Gustatory responses of single neurons in the insula of the macaque monkey
Yaxley, S., Rolls, E. T., & Sienkiewicz, Z. J. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.4.689 · Cited by 262 · see citing works
Self-citationBurton, M. J., Rolls, E. T., & Mora, F. (1976) · Experimental Neurology · doi:10.1016/0014-4886(76)90189-8 · Cited by 252 · see citing works
Self-citationSensory-specific and motivation-specific satiety for the sight and taste of food and water in man
Rolls, E. T., Rolls, B. J., & Rowe, E. A. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90003-3 · Cited by 249 · see citing works
Self-citationGustatory responses in the frontal opercular cortex of the alert cynomolgus monkey
Scott, T. R., Yaxley, S., Sienkiewicz, Z. J., & Rolls, E. T. (1986) · Journal of Neurophysiology · doi:10.1152/jn.1986.56.3.876 · Cited by 228 · see citing works
Self-citationKatsuki, Y., Satō, M., Norgren, R., et al. (1981) · Medical Entomology and Zoology · Cited by 210 · see citing works
Activity of neurones in the inferotemporal cortex of the alert monkey
Rolls, E. T., Judge, S. J., & Sanghera, M. K. (1977) · Brain Research · doi:10.1016/0006-8993(77)90272-4 · Cited by 198 · see citing works
Self-citationNeurophysiological analysis of brain-stimulation reward in the monkey
Rolls, E. T., Burton, M. J., & Mora, F. (1980) · Brain Research · doi:10.1016/0006-8993(80)91216-0 · Cited by 193 · see citing works
Self-citationSanides, F. (1968) · Brain Research · doi:10.1016/0006-8993(68)90174-1 · Cited by 180 · see citing works
Rolls, E. T., Murzi, E., Yaxley, S., Thorpe, S. J., & Simpson, S. J. (1986) · Brain Research · doi:10.1016/0006-8993(86)91044-9 · Cited by 180 · see citing works
Self-citationRolls, E. T., Scott, T. R., Sienkiewicz, Z. J., & Yaxley, S. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp016984 · Cited by 165 · see citing works
Self-citationProjections of thalamic gustatory and lingual areas in the rat
Norgren, R., & Wolf, G. (1975) · Brain Research · doi:10.1016/0006-8993(75)90531-4 · Cited by 151 · see citing works
Rolls, E. T. (1975) · Medical Entomology and Zoology · Cited by 148 · see citing works
Self-citationBenjamin, R. M., & Burton, H. (1968) · Brain Research · doi:10.1016/0006-8993(68)90100-5 · Cited by 148 · see citing works
Gastric modulation of gustatory afferent activity
Glenn, J. F., & Erickson, R. P. (1976) · Physiology & Behavior · doi:10.1016/0031-9384(76)90216-x · Cited by 126 · see citing works
Unit study of exteroceptive inputs to claustrocortex in awake, sitting, squirrel monkey
Судаков, К. В., MacLean, P. D., Reeves, A. G., & Marino, R. (1971) · Brain Research · doi:10.1016/0006-8993(71)90521-x · Cited by 125 · see citing works
Blood Glucose Selectively Affects Taste-Evoked Activity in Rat Nucleus Tractus Solitarius
Giza, B. K., & Scott, T. R. (1983) · Physiology & Behavior · doi:10.1016/s0031-9384(24)00191-4 · Cited by 125 · see citing works
Gustatory responses in the nucleus tractus solitarius of the alert cynomolgus monkey
Scott, T. R., Yaxley, S., Sienkiewicz, Z. J., & Rolls, E. T. (1986) · Journal of Neurophysiology · doi:10.1152/jn.1986.55.1.182 · Cited by 112 · see citing works
Self-citationCENTRAL NERVOUS MECHANISMS RELATED TO FEEDING AND APPETITE
Rolls, E. T. (1981) · British Medical Bulletin · doi:10.1093/oxfordjournals.bmb.a071689 · Cited by 106 · see citing works
Self-citationSatiety does not affect gustatory activity in the nucleus of the solitary tract of the alert monkey
Yaxley, S., Rolls, E. T., Sienkiewicz, Z. J., & Scott, T. R. (1985) · Brain Research · doi:10.1016/0006-8993(85)90891-1 · Cited by 101 · see citing works
Self-citationCORTICAL ORGANIZATION IN GUSTATION (MACACA MULATTA)
Bagshaw, M. H., & Pribram, K. H. (1953) · Journal of Neurophysiology · doi:10.1152/jn.1953.16.5.499 · Cited by 91 · see citing works
Feeding Behavior Neural and Humoral Controls
(1986) · Elsevier eBooks · doi:10.1016/b978-0-12-589060-1.x5001-9 · Cited by 82 · see citing works
The neurophysiology of feeding.
Rolls, E. T. (1984) · PubMed · Cited by 56 · see citing works
Self-citationNEURONAL ACTIVITY RELATED TO THE CONTROL OF FEEDING
Rolls, E. T. (1986) · Elsevier eBooks · doi:10.1016/b978-0-12-589060-1.50011-0 · Cited by 51 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
A specific neural substrate for perceiving facial expressions of disgust
Phillips, M. L., Young, A. W., Senior, C., Brammer, M., Andrew, C., Calder, A. J., Bullmore, E. T., Perrett, D. I., Rowland, D., Williams, S. C. R., et al. (1997) · Nature · doi:10.1038/39051 · Cited by 1,609 · see citing works
The Orbitofrontal Cortex and Reward
Rolls, E. T. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.284 · Cited by 1,595 · see citing works
Self-citationThe functions of the orbitofrontal cortex
Rolls, E. T. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00277-x · Cited by 1,327 · see citing works
Self-citationDissociable neural responses to facial expressions of sadness and anger
Blair, R. J. R., Morris, J. S., Frith, C. D., Perrett, D. I., & Dolan, R. J. (1999) · Brain · doi:10.1093/brain/122.5.883 · Cited by 1,212 · see citing works
Reward, Motivation, and Reinforcement Learning
Dayan, P., & Balleine, B. W. (2002) · Neuron · doi:10.1016/s0896-6273(02)00963-7 · Cited by 855 · see citing works
Kringelbach, M. L. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.10.1064 · Cited by 824 · see citing works
Odor/taste integration and the perception of flavor
Small, D. M., & Prescott, J. (2005) · Experimental Brain Research · doi:10.1007/s00221-005-2376-9 · Cited by 712 · see citing works
The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making
Naqvi, N. H., & Bechara, A. (2010) · Brain Structure and Function · doi:10.1007/s00429-010-0268-7 · Cited by 598 · see citing works
The orbitofrontal cortex: reward, emotion and depression
Rolls, E. T., Cheng, W., & Feng, J. (2020) · Brain Communications · doi:10.1093/braincomms/fcaa196 · Cited by 474 · see citing works
Self-citationRolls, E. T., Sienkiewicz, Z. J., & Yaxley, S. (1989) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1989.tb00774.x · Cited by 466 · see citing works
Self-citationMeasuring facial expressions by computer image analysis
Bartlett, M. S., Hager, J. C., Ekman, P., & Sejnowski, T. J. (1999) · Psychophysiology · doi:10.1017/s0048577299971664 · Cited by 424 · see citing works
Orbitofrontal cortex neurons: role in olfactory and visual association learning
Rolls, E. T., Critchley, H. D., Mason, R., & Wakeman, E. A. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.75.5.1970 · Cited by 398 · see citing works
Self-citationGrabenhorst, F., Rolls, E. T., & Bilderbeck, A. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm185 · Cited by 337 · see citing works
Self-citationCerebral processing of food-related stimuli: effects of fasting and gender
Uher, R., Treasure, J., Heining, M., Brammer, M. J., & Campbell, I. C. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.12.008 · Cited by 258 · see citing works
Processing Faces and Facial Expressions
Posamentier, M. T., & Abdi, H. (2003) · Neuropsychology Review · doi:10.1023/a:1025519712569 · Cited by 257 · see citing works
Food for thought: hedonic experience beyond homeostasis in the human brain
Kringelbach, M. L. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2004.04.035 · Cited by 236 · see citing works
Rolls, E. (2008) · Acta Physiologica Hungarica · doi:10.1556/aphysiol.95.2008.2.1 · Cited by 214 · see citing works
Self-citationAltering expectancy dampens neural response to aversive taste in primary taste cortex
Nitschke, J. B., Dixon, G. E., Sarinopoulos, I., Short, S. J., Cohen, J. D., Smith, E. E., Kosslyn, S. M., Rose, R. M., & Davidson, R. J. (2006) · Nature Neuroscience · doi:10.1038/nn1645 · Cited by 199 · see citing works
Enhanced affective brain representations of chocolate in cravers vs. non‐cravers
Rolls, E. T., & McCabe, C. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05724.x · Cited by 188 · see citing works
Self-citationThe physiological control of eating: signals, neurons, and networks
Watts, A. G., Kanoski, S. E., Sanchez-Watts, G., & Langhans, W. (2022) · Physiological Reviews · doi:10.1152/physrev.00028.2020 · Cited by 168 · see citing works
Malhi, G. S., Lagopoulos, J., Sachdev, P. S., Ivanovski, B., Shnier, R., & Ketter, T. (2007) · Bipolar Disorders · doi:10.1111/j.1399-5618.2007.00485.x · Cited by 155 · see citing works
Human cortical representation of oral temperature
Guest, S., Grabenhorst, F., Essick, G., Chen, Y., Young, M., McGlone, F., de Araujo, I., & Rolls, E. T. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.07.004 · Cited by 129 · see citing works
Neural circuits and motivational processes for hunger
Sternson, S. M., Nicholas Betley, J., & Cao, Z. F. H. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.04.006 · Cited by 108 · see citing works
The Neurophysiology of Taste and Olfaction in Primates, and Umami Flavor<sup>a</sup>
ROLLS, E. T., CRITCHLEY, H. D., BROWNING, A., & HERNADI, I. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb10602.x · Cited by 80 · see citing works
Self-citationFood-related Neural Circuitry in Prader-Willi Syndrome: Response to High- Versus Low-calorie Foods
Dimitropoulos, A., & Schultz, R. T. (2008) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-008-0546-x · Cited by 73 · see citing works
Satiety-responsive neurons in the medial orbitofrontal cortex of the macaque.
Pritchard, T. C., Nedderman, E. N., Edwards, E. M., Petticoffer, A. C., Schwartz, G. J., & Scott, T. R. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.1.174 · Cited by 40 · see citing works
- Authors
- Yaxley, S., Rolls, E. T., & Sienkiewicz, Z. J.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Rolls, Edmund T.
- ORCID
- Rolls, Edmund T.
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1988-01
- Volume
- 42
- Issue
- 3
- Pages
- 223-229
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2007316161
- Cited by
- 206
- References
- 45
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 3 · 2023: 3 · 2022: 2 · 2021: 7 · 2020: 5 · 2019: 4 · 2018: 5 · 2017: 5 · 2016: 10 · 2015: 10 · 2014: 6 · 2013: 3 · 2012: 9
- FWCI
- 3.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Biochemical Analysis and Sensing Techniques
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- hunger, satiety, taste neurons, single-unit activity, macaque, food motivation, hypothalamic neurons, taste stimuli, glucose, fruit juice
- MeSH terms
- Amygdala, Animals, Brain Mapping, Frontal Lobe, Hunger, Hypothalamus, Macaca fascicularis, Male, Neural Pathways, Neurons, Satiation, Taste, Thalamic Nuclei
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.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
