Orbitofrontal cortex neurons: role in olfactory and visual association learning
Abstract
1. The orbitofrontal cortex is implicated in the rapid learning of new associations between visual stimuli and primary reinforcers such as taste. It is also the site of convergence of information from olfactory, gustatory, and visual modalities. To investigate the neuronal mechanisms underlying the formation of odor-taste associations, we made recordings from olfactory neurons in the orbitofrontal cortex during the performance of an olfactory discrimination task and its reversal in macaques. 2. It was found that 68% of odor-responsive neurons modified their responses after the changes in the taste reward associations of the odorants. Full reversal of the neuronal responses was seen in 25% of these neurons. Extinction of the differential neuronal responses after task reversal was seen in 43% of these neurons. 3. For comparison, visually responsive orbitofrontal neurons were tested during reversal of a visual discrimination task. Seventy-one percent of these visual cells showed rapid full reversal of the visual stimulus to which they responded, when the association of the visual with taste was reversed in the reversal task. 4. These demonstrate that of many orbitofrontal cortex olfactory neurons on the taste with which the odor is associated. 5. This modification is likely to be important for setting the motivational value of olfactory for feeding and other rewarded behavior. However, it is less complete, and much slower, than the modifications found or orbit frontal visual during visual-taste reversal. This relative inflexibility of olfactory responses is consistent with the need for some stability is odor-taste associations to facilitate the formation and perception of flavors.
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In visual discrimination reversal experiments, neurons in the macaque OFC reverse the visual stimulus in as little as one trial when the reward versus punishment taste received as an outcome for the choice reverses.
“In visual discrimination reversal experiments, neurons in the macaque OFC reverse the visual stimulus in as little as one trial when the reward versus punishment taste received as an outcome for the choice reverses (Thorpe et al., 1983; Rolls et al., 1996).”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Rolls et al., 1996
Non-reward and punishment are represented by different neurons in the OFC.
“These neurons do not respond to expected punishers [e.g. the discriminative stimulus for saline in Fig. 4C; (Thorpe et al., 1983)], but other neurons do respond to expected punishers (Rolls et al., 1996), showing that non-reward and punishment are represented by different neurons in the OFC.”
From The orbitofrontal cortex: reward, emotion and depression (2020) · cites this paper as Rolls et al., 1996
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Rolls, E. T. (2006) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2006.1852 · Cited by 248 · see citing works
Self-citationKondo, H., Saleem, K. S., & Price, J. L. (2005) · Journal of Comparative Neurology · doi:10.1002/cne.20796 · Cited by 236 · see citing works
Rolls, E. T., McCabe, C., & Redouté, J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm097 · Cited by 234 · see citing works
Self-citationFood 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
Does the orbitofrontal cortex signal value?
Schoenbaum, G., Takahashi, Y., Liu, T., & McDannald, M. A. (2011) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2011.06210.x · Cited by 232 · see citing works
Amygdaloid projections to ventromedial striatal subterritories in the primate
Fudge, J. L., Kunishio, K., Walsh, P., Richard, C., & Haber, S. N. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00546-2 · Cited by 226 · see citing works
Changes in behavior-related neuronal activity in the striatum during learning
Schultz, W. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00122-x · Cited by 225 · see citing works
Schoenbaum, G., Chiba, A., & Gallagher, M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-13-05179.2000 · Cited by 234 · see citing works
Behavioral planning in the prefrontal cortex
Tanji, J., & Hoshi, E. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00192-6 · Cited by 224 · see citing works
Umami: a delicious flavor formed by convergence of taste and olfactory pathways in the human brain
McCabe, C., & Rolls, E. T. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05445.x · Cited by 221 · see citing works
Self-citationRolls, E. (2008) · Acta Physiologica Hungarica · doi:10.1556/aphysiol.95.2008.2.1 · Cited by 214 · see citing works
Self-citationSensory processing in the brain related to the control of food intake
Rolls, E. T. (2007) · Proceedings of The Nutrition Society · doi:10.1017/s0029665107005332 · Cited by 210 · see citing works
Self-citationShanmugan, S., & Epperson, C. N. (2012) · Human Brain Mapping · doi:10.1002/hbm.22218 · Cited by 210 · see citing works
Selective attention to affective value alters how the brain processes taste stimuli
Fabian Grabenhorst, B., & Rolls, E. T. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06033.x · Cited by 206 · see citing works
Self-citationHoshi, E., Shima, K., & Tanji, J. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.2355 · Cited by 204 · see citing works
Brain activity during biofeedback relaxation: A functional neuroimaging investigation
Critchley, H. (2001) · Brain · doi:10.1093/brain/124.5.1003 · Cited by 196 · see citing works
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The Place of the Thalamus in Frontal Cortical-Basal Ganglia Circuits
Haber, S. N., & McFarland, N. R. (2001) · The Neuroscientist · doi:10.1177/107385840100700408 · Cited by 187 · see citing works
Decision Making: The Neuroethological Turn
Pearson, J. M., Watson, K. K., & Platt, M. L. (2014) · Neuron · doi:10.1016/j.neuron.2014.04.037 · Cited by 184 · see citing works
Neural activity in the human brain relating to uncertainty and arousal during anticipation
Critchley, H., Mathiast, C. J., & Dolan, R. J. (2001) · NeuroImage · doi:10.1016/s1053-8119(01)91735-5 · Cited by 191 · see citing works
Self-citationVerhagen, J. V., Kadohisa, M., & Rolls, E. T. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00321.2004 · Cited by 189 · see citing works
Self-citationEnhanced 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-citationHayes, J. E., & Duffy, V. B. (2007) · Chemical Senses · doi:10.1093/chemse/bjl050 · Cited by 181 · see citing works
Visuomotor Areas of the Frontal Lobe
Schall, J. D. (1997) · Cerebral cortex · doi:10.1007/978-1-4757-9625-4_13 · Cited by 177 · see citing works
Basolateral Amygdala Lesions Abolish Orbitofrontal-Dependent Reversal Impairments
Stalnaker, T. A., Franz, T. M., Singh, T., & Schoenbaum, G. M. (2007) · Neuron · doi:10.1016/j.neuron.2007.02.014 · Cited by 178 · see citing works
Re-evaluating the role of the orbitofrontal cortex in reward and reinforcement
Noonan, M. P., Kolling, N., Walton, M. E., & Rushworth, M. F. S. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08023.x · Cited by 169 · see citing works
Taste and Olfactory Processing in the Brain and Its Relation to the Control of Eating
Rolls, E. T. (1997) · Critical Reviews in Neurobiology · doi:10.1615/critrevneurobiol.v11.i4.20 · Cited by 173 · see citing works
Self-citationKadohisa, M., Rolls, E. T., & Verhagen, J. V. (2005) · Chemical Senses · doi:10.1093/chemse/bji036 · Cited by 173 · see citing works
Self-citationTremblay, L., & Schultz, W. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.4.1877 · Cited by 167 · see citing works
Behavioral flexibility in rats and mice: contributions of distinct frontocortical regions
Hamilton, D. A., & Brigman, J. L. (2015) · Genes, Brain and Behavior · doi:10.1111/gbb.12191 · Cited by 168 · see citing works
Neurons in the Primate Orbitofrontal Cortex Respond to Fat Texture Independently of Viscosity
Verhagen, J. V., Rolls, E. T., & Kadohisa, M. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00320.2003 · Cited by 163 · see citing works
Self-citation
- Authors
- Rolls, E. T., Critchley, H. D., Mason, R., & Wakeman, E. A.
- Affiliations
- University of Oxford (GB)
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1996-05-01
- Volume
- 75
- Issue
- 5
- Pages
- 1970-1981
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W1959149129
- Cited by
- 398
- References
- 45
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 10 · 2023: 6 · 2022: 9 · 2021: 11 · 2020: 7 · 2019: 11 · 2018: 9 · 2017: 12 · 2016: 14 · 2015: 15 · 2014: 12 · 2013: 7 · 2012: 14
- FWCI
- 5.69
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- orbitofrontal cortex, odor discrimination, visual discrimination, reversal learning, extinction, olfactory sensory neurons, visual neurons, flavor perception, macaque, single-unit recording
- MeSH terms
- Acoustic Stimulation, Animals, Association Learning, Behavior, Animal, Cerebral Cortex, Discrimination, Psychological, Macaca fascicularis, Microelectrodes, Neural Pathways, Neurons, Odorants, Orbit, Photic Stimulation, Radiography, Reinforcement, Psychology, Smell, Vision, Ocular
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