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J Neurophysiol (April 21, 2004). doi:10.1152/jn.00050.2004
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Submitted on January 15, 2004
Accepted on April 18, 2004

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

Dana M. Small1*, Joel Voss2, Y E. Mak3, Katharine B. Simmons3, Todd R. Parrish4, and Darren R. Gitelman5

1 Cognitive Neurology and Alzheimer's Disease Center, Northwestern University Feinberg School of Medicine, Chicago, IL, USA; The John B Pierce Laboratory, New Haven, CT, USA; Surgery, Yale University School of Medicine, New Haven, CT, USA
2 Cognitive Neurology and Alzheimer's Disease Center, Northwestern University Feinberg School of Medicine, Chicago, IL, USA; Institute for Neuroscience, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
3 Cognitive Neurology and Alzheimer's Disease Center, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
4 Cognitive Neurology and Alzheimer's Disease Center, Northwestern University Feinberg School of Medicine, Chicago, IL, USA; Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA; Radiology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA
5 Cognitive Neurology and Alzheimer's Disease Center, Northwestern University Feinberg School of Medicine, Chicago, IL, USA; Institute for Neuroscience, Northwestern University Feinberg School of Medicine, Chicago, IL, USA; Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

* To whom correspondence should be addressed. E-mail: d-small{at}northwestern.edu.

1. 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. 2. 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 to 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 via 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 via the orthonasal and require subjects to sniff. There were two 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 two tastes (sweet and salty) and one odor (vanilla), as well as a tasteless/odorless liquid (baseline) were presented. 3. Super-additive responses during the perception of the congruent flavor compared to the sum of its constituents were observed in the anterior cingulate cortex, dorsal insula, anterior ventral insula extending into the caudal orbitofrontal cortex, frontal operculum, ventral lateral prefrontal cortex and posterior parietal cortex. These regions were not present in a similar analysis of the incongruent flavor compared to the sum of its constituents. All of these regions except the ventrolateral prefrontal cortex were also isolated in a direct contrast of congruent minus incongruent. Additionally, the anterior cingulate, posterior parietal cortex, frontal operculum and ventral insula/caudal OFC were also more active in vanilla plus salty minus incongruent, suggesting that delivery of an unfamiliar taste-odor combination may lead to suppressed neural responses. 4. 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 upon 1) mode of olfactory delivery and 2) previous experience with taste/smell combinations.




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