Experience-dependent neural integration of taste and smell in the human brain

Small, Dana M.; Voss, Joel; Mak, Y. Erica; Simmons, Katharine B.; Parrish, Todd; Gitelman, Darren

doi:10.1152/jn.00050.2004

Cited by 398Olfactory and Sensory Function StudiesMultisensory perception and integrationTactile and Sensory Interactions

Experience-dependent neural integration of taste and smell in the human brain

Small, Dana M., Voss, Joel, Mak, Y. Erica, Simmons, Katharine B., Parrish, Todd, Gitelman, Darren·2004·Journal of Neurophysiology

DOI 10.1152/jn.00050.2004

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Abstract

Flavor perception arises from the central integration of peripherally distinct sensory inputs (taste, smell, texture, temperature, sight, and even sound of foods). The results from psychophysical and neuroimaging studies in humans are converging with electrophysiological findings in animals and a picture of the neural correlates of flavor processing is beginning to emerge. Here we used event-related fMRI to evaluate brain response during perception of flavors (i.e., taste/odor liquid mixtures not differing in temperature or texture) compared with the sum of the independent presentation of their constituents (taste and/or odor). All stimuli were presented in liquid form so that olfactory stimulation was by the retronasal route. Mode of olfactory delivery is important because neural suppression has been observed in chemosensory regions during congruent taste-odor pairs when the odors are delivered by the orthonasal route and require subjects to sniff. There were 2 flavors. One contained a familiar/congruent taste-odor pair (vanilla/sweet) and the other an unfamiliar/incongruent taste-odor pair (vanilla/salty). Three unimodal stimuli, including 2 tastes (sweet and salty) and one odor (vanilla), as well as a tasteless/odorless liquid (baseline) were presented. Superadditive responses during the perception of the congruent flavor compared with the sum of its constituents were observed in the anterior cingulate cortex (ACC), dorsal insula, anterior ventral insula extending into the caudal orbitofrontal cortex (OFC), frontal operculum, ventral lateral prefrontal cortex, and posterior parietal cortex. These regions were not present in a similar analysis of the incongruent flavor compared with the sum of its constituents. All of these regions except the ventrolateral prefrontal cortex were also isolated in a direct contrast of congruent - incongruent. Additionally, the anterior cingulate, posterior parietal cortex, frontal operculum, and ventral insula/caudal OFC were also more active in vanilla + salty minus incongruent, suggesting that delivery of an unfamiliar taste-odor combination may lead to suppressed neural responses. Taken together with previous findings in the literature, these results suggest that the insula, OFC, and ACC are key components of the network underlying flavor perception and that taste-smell integration within these and other regions is dependent on 1) mode of olfactory delivery and 2) previous experience with taste/smell combinations.

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Neuroimaging evidence demonstrates convergence for taste and odour in the orbitofrontal and anterior cingulate cortex.
“neuroimaging evidence has demonstrated that convergence for taste and odour occur in the orbitofrontal and anterior cingulate cortex [146-148].”
From The Role of Intrinsic and Extrinsic Sensory Factors in Sweetness Perception of Food and Beverages: A Review (2019) · cites this paper as [148]

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Authors: Small, D. M., Voss, J., Mak, Y. E., Simmons, K. B., Parrish, T., & Gitelman, D.
Affiliations: Northwestern University (US)
ORCID: Small, Dana M.
Voss, Joel
Parrish, Todd
Gitelman, Darren
Venue: Journal of Neurophysiology
Publisher: American Physiological Society
Published: 2004-09
Volume: 92
Issue: 3
Pages: 1892-1903
ISSN: 0022-3077 (ISSN-L)
1522-1598
DOI: 10.1152/jn.00050.2004
OpenAlex: W2152813995
Cited by: 398
References: 78
Citations by year: 2026: 23 · 2025: 14 · 2024: 17 · 2023: 11 · 2022: 12 · 2021: 15 · 2020: 17 · 2019: 20 · 2018: 26 · 2017: 17 · 2016: 17 · 2015: 15 · 2014: 12 · 2013: 23 · 2012: 19
FWCI: 9.55
Type: journal article
Language: en
Open access: closed
Locations: Journal of Neurophysiology (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5r03dc006169-03)
National Institute on Aging (AG0094)
National Institute on Deafness and Other Communication Disorders (R03 DC 006169-01)
Topics: Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
Keywords: flavor perception, retronasal olfaction, anterior cingulate cortex, frontal operculum, posterior parietal cortex, ventrolateral prefrontal cortex
MeSH terms: Adult, Analysis of Variance, Brain, Brain Mapping, Female, Humans, Life Change Events, Male, Smell, Taste

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Experience-dependent neural integration of taste and smell in the human brain

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