Experience-Dependent Neural Integration of Taste and Smell in the Human Brain

• Published in: Journal of neurophysiology Vol. 92; no. 3; pp. 1892 - 1903
• Main Authors: Small, Dana M, Voss, Joel, Mak, Y. Erica, Simmons, Katharine B, Parrish, Todd, Gitelman, Darren
• Format: Journal Article
• Language: English
• Published: United States Am Phys Soc 01.09.2004
• Subjects: Adult; Analysis of Variance; Brain - physiology; Brain Mapping - methods; Female; Humans; Life Change Events; Male; Smell - physiology; Taste - physiology; Vanilla
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00050.2004

1 Cognitive Neurology and Alzheimer's Disease Center and 2 Departments of Neurology and 3 Radiology, Northwestern University Feinberg School of Medicine, Chicago 60611-3008; 4 Northwestern University Institute for Neuroscience, Evanston, Illinois 60208-3520; 5 The John B. Pierce Laboratory, New Haven 06519; and 6 Yale University School of Medicine, New Haven, Connecticut 06510 Submitted 15 January 2004; accepted in final form 18 April 2004 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. Address for reprint requests and other correspondence: D. M. Small, The John B. Pierce Laboratory, 290 Congress Ave., New Haven, CT 06519 (E-mail: dsmall{at}jbpierce.org ).