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Altering expectancy dampens neural response to aversive taste in primary taste cortex

Abstract

The primary taste cortex consists of the insula and operculum. Previous work has indicated that neurons in the primary taste cortex respond solely to sensory input from taste receptors and lingual somatosensory receptors. Using functional magnetic resonance imaging, we show here that expectancy modulates these neural responses in humans. When subjects were led to believe that a highly aversive bitter taste would be less distasteful than it actually was, they reported it to be less aversive than when they had accurate information about the taste and, moreover, the primary taste cortex was less strongly activated. In addition, the activation of the right insula and operculum tracked online ratings of the aversiveness for each taste. Such expectancy-driven modulation of primary sensory cortex may affect perceptions of external events.

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Figure 1: Experimental design.
Figure 2: Subjects' online ratings of the unpleasantness (with the sign reversed to make values positive) of the tastes for the aversive, misleading, mildly aversive and neutral conditions while in the scanner (n = 43).
Figure 3: Circled middle insula and frontal operculum clusters and posterior insula and parietal operculum clusters that were more strongly activated by the highly aversive taste than by the neutral taste.
Figure 4: Circled right insula and operculum cluster for which activation was correlated with taste ratings.
Figure 5: Insula responses to tastes in each of the four conditions.
Figure 6: Operculum responses to tastes in each of the four conditions.
Figure 7: Insula and operculum responses to highly aversive taste following aversive and misleading mildly aversive cues.

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Acknowledgements

We acknowledge A. Alexander, M. Anderle, M. Carew, R. Fisher, T. Johnstone, R. Koch, A. Lakshmanan, K. Mackiewicz, H. Schaefer and E. Steege for their contributions to this project. J.B.N. was supported by a US National Institute of Mental Health Career Development Award (K08-MH63984), a Training Program in Emotion Research National Institute of Mental Health grant (T32-MH18931) and a HealthEmotions Research Institute fellowship. G.E.D. was supported by a National Science Foundation Graduate Fellowship. R.J.D. was supported by National Institute of Mental Health grants (MH40747, P50-MH52354, MH43454) and a National Institute of Mental Health Research Scientist Award (K05-MH00875). The research reported in this publication was also supported by the Mind Brain Body and Health Initiative, funded by the John D. and Catherine T. MacArthur Foundation, the Rockefeller Family and Associates and the Kohlberg Foundation, and by a core grant to the Waisman Center from the National Institute of Child Health and Human Development (P30 HD03352). Parts of this work were presented at the 32nd annual meeting of the Society for Neuroscience in San Diego, California, October 2004.

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Correspondence to Jack B Nitschke or Richard J Davidson.

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Supplementary information

Supplementary Fig. 1

Dorsal and ventral insula responses to tastes in each of the four conditions. (PDF 25317 kb)

Supplementary Fig. 2

Subjects' on-line ratings of the pleasantness of the pleasant and neutral tastes while in the scanner (n = 43). (PDF 2367 kb)

Supplementary Fig. 3

Circled middle insula/frontal operculum and posterior insula/parietal operculum clusters which were more strongly activated by the highly aversive taste than the neutral taste Fig. 3). (PDF 21255 kb)

Supplementary Fig. 4

Habituation of insula/operculum activation to the highly aversive taste across the eight experimental runs. (PDF 844 kb)

Supplementary Note (PDF 26 kb)

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Nitschke, J., Dixon, G., Sarinopoulos, I. et al. Altering expectancy dampens neural response to aversive taste in primary taste cortex. Nat Neurosci 9, 435–442 (2006). https://doi.org/10.1038/nn1645

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