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

Nature Neuroscience volume 9, pages 435–442 (2006)Cite this article

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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References

  1. Ogawa, H. Gustatory cortex of primates: anatomy and physiology. Neurosci. Res. 20, 1–13 (1994).

    Article  CAS  Google Scholar 

  2. Rolls, E.T. The Brain and Emotion (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  3. Scott, T.R., Yaxley, S., Sienkiewicz, Z.J. & Rolls, E.T. Gustatory responses in the frontal opercular cortex of the alert cynomolgus monkey. J. Neurophysiol. 56, 876–890 (1986).

    Article  CAS  Google Scholar 

  4. Yaxley, S., Rolls, E.T. & Sienkiewicz, Z.J. Gustatory responses of single neurons in the insula of the macaque monkey. J. Neurophysiol. 63, 689–700 (1990).

    Article  CAS  Google Scholar 

  5. Sudakov, K., MacLean, P.D., Reeves, A. & Marino, R. Unit study of exteroceptive inputs to claustrocortex in awake, sitting, squirrel monkey. Brain Res. 28, 19–34 (1971).

    Article  CAS  Google Scholar 

  6. Scott, T.R., Giza, B.K. & Yan, J. Gustatory neural coding in the cortex of the alert cynomolgus macaque: the quality of bitterness. J. Neurophysiol. 81, 60–71 (1999).

    Article  CAS  Google Scholar 

  7. Cerf-Ducastel, B., Van de Moortele, P.F., MacLeod, P., Le Bihan, D. & Faurion, A. Interaction of gustatory and lingual somatosensory perceptions at the cortical level in the human: a functional magnetic resonance imaging study. Chem. Senses 26, 371–383 (2001).

    Article  CAS  Google Scholar 

  8. Kobayakawa, T. et al. Spatio-temporal analysis of cortical activity evoked by gustatory stimulation in humans. Chem. Senses 24, 201–209 (1999).

    Article  CAS  Google Scholar 

  9. Small, D.M. et al. Human cortical gustatory areas: a review of functional neuroimaging data. Neuroreport 10, 7–14 (1999).

    Article  CAS  Google Scholar 

  10. O'Doherty, J., Rolls, E.T., Francis, S., Bowtell, R. & McGlone, F. Representation of pleasant and aversive taste in the human brain. J. Neurophysiol. 85, 1315–1321 (2001).

    Article  CAS  Google Scholar 

  11. Zald, D.H., Lee, J.T., Fluegel, K.W. & Pardo, J.V. Aversive gustatory stimulation activates limbic circuits in humans. Brain 121, 1143–1154 (1998).

    Article  Google Scholar 

  12. Zald, D.H., Hagen, M.C. & Pardo, J.V. Neural correlates of tasting concentrated quinine and sugar solutions. J. Neurophysiol. 87, 1068–1075 (2002).

    Article  Google Scholar 

  13. O'Doherty, J.P., Deichmann, R., Critchley, H.D. & Dolan, R.J. Neural responses during anticipation of a primary taste reward. Neuron 33, 815–826 (2002).

    Article  CAS  Google Scholar 

  14. Small, D.M. et al. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39, 701–711 (2003).

    Article  CAS  Google Scholar 

  15. Penfield, W. & Jasper, H.H. Epilepsy and the Functional Anatomy of the Human Brain (Little, Boston, 1954).

    Book  Google Scholar 

  16. Börnstein, W.S. Cortical representation of taste in man and monkey: I. Functional and anatomical relations of taste, olfaction and somatic sensibility. Yale J. Biol. Med. 12, 719–736 (1940).

    PubMed  PubMed Central  Google Scholar 

  17. Motta, G. The cortical taste centers. Bull. Sci. Med. (Bologna) 131, 480–493 (1959).

    CAS  Google Scholar 

  18. Pritchard, T.C., Macaluso, D.A. & Eslinger, P.J. Taste perception in patients with insular cortex lesions. Behav. Neurosci. 113, 663–671 (1999).

    Article  CAS  Google Scholar 

  19. Penfield, W. & Faulk, M.E.,Jr. The insula: further observations on its function. Brain 78, 445–470 (1955).

    Article  CAS  Google Scholar 

  20. Ostrowsky, K. et al. Functional mapping of the insular cortex: clinical implication in temporal lobe epilepsy. Epilepsia 41, 681–686 (2000).

    Article  CAS  Google Scholar 

  21. Rolls, E.T., Scott, T.R., Sienkiewicz, Z.J. & Yaxley, S. The responsiveness of neurones in the frontal opercular gustatory cortex of the macaque monkey is independent of hunger. J. Physiol. (Lond.) 397, 1–12 (1988).

    Article  CAS  Google Scholar 

  22. Yaxley, S., Rolls, E.T. & Sienkiewicz, Z.J. The responsiveness of neurons in the insular gustatory cortex of the macaque monkey is independent of hunger. Physiol. Behav. 42, 223–229 (1988).

    Article  CAS  Google Scholar 

  23. Wager, T.D. et al. Placebo-induced changes in fMRI in the anticipation and experience of pain. Science 303, 1162–1167 (2004).

    Article  CAS  Google Scholar 

  24. Ploghaus, A., Becerra, L., Borras, C. & Borsook, D. Neural circuitry underlying pain modulation: expectation, hypnosis, placebo. Trends Cogn. Sci. 7, 197–200 (2003).

    Article  Google Scholar 

  25. Tanriover, N., Rhoton, A.L., Jr, Kawashima, M., Ulm, A.J. & Yasuda, A. Microsurgical anatomy of the insula and the sylvian fissure. J. Neurosurg. 100, 891–922 (2004).

    Article  Google Scholar 

  26. Mai, J.K., Assheuer, J. & Paxinos, G. Atlas of the Human Brain (Elsevier, Amsterdam, 2004).

    Google Scholar 

  27. Price, D.D. Psychological and neural mechanisms of the affective dimension of pain. Science 288, 1769–1772 (2000).

    Article  CAS  Google Scholar 

  28. Craig, A.D. How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3, 655–666 (2002).

    Article  CAS  Google Scholar 

  29. Phelps, E.A., O'Connor, K.J., Gatenby, J.C., Grillon, C. & Davis, M. Activation of the left amygdala to a cognitive representation of fear. Nat. Neurosci. 4, 437–441 (2001).

    Article  CAS  Google Scholar 

  30. Critchley, H.D., Mathias, C.J. & Dolan, R.J. Fear conditioning in humans: the influence of awareness and autonomic arousal on functional neuroanatomy. Neuron 33, 653–663 (2002).

    Article  CAS  Google Scholar 

  31. Phillips, M.L. et al. A specific neural substrate for perceiving facial expressions of disgust. Nature 389, 495–498 (1997).

    Article  CAS  Google Scholar 

  32. Wicker, B. et al. Both of us disgusted in My insula: the common neural basis of seeing and feeling disgust. Neuron 40, 655–664 (2003).

    Article  CAS  Google Scholar 

  33. Taylor, S.F., Liberzon, I. & Koeppe, R.A. The effect of graded aversive stimuli on limbic and visual activation. Neuropsychologia 38, 1415–1425 (2000).

    Article  CAS  Google Scholar 

  34. Nitschke, J.B., Sarinopoulos, I., Mackiewicz, K.L., Schaefer, H.S. & Davidson, R.J. Functional neuroanatomy of aversion and its anticipation. Neuroimage 29, 106–116 (2006).

    Article  Google Scholar 

  35. Augustine, J.R. Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res. Brain Res. Rev. 22, 229–244 (1996).

    Article  CAS  Google Scholar 

  36. Adolphs, R., Damasio, H., Tranel, D., Cooper, G. & Damasio, A.R. A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J. Neurosci. 20, 2683–2690 (2000).

    Article  CAS  Google Scholar 

  37. Craig, A.D., Chen, K., Bandy, D. & Reiman, E.M. Thermosensory activation of insular cortex. Nat. Neurosci. 3, 184–190 (2000).

    Article  CAS  Google Scholar 

  38. Critchley, H.D., Wiens, S., Rotshtein, P., Ohman, A. & Dolan, R.J. Neural systems supporting interoceptive awareness. Nat. Neurosci. 7, 189–195 (2004).

    Article  CAS  Google Scholar 

  39. Damasio, A.R. Looking for Spinoza: Joy, Sorrow, and the Feeling Brain (Harcourt, Orlando, Florida, 2003).

    Google Scholar 

  40. Benedetti, F., Arduino, C. & Amanzio, M. Somatotopic activation of opioid systems by target-directed expectations of analgesia. J. Neurosci. 19, 3639–3648 (1999).

    Article  CAS  Google Scholar 

  41. Montgomery, G. & Kirsch, I. Mechanisms of placebo pain reduction: an empirical investigation. Psychol. Sci. 7, 174–176 (1996).

    Article  Google Scholar 

  42. Stewart-Williams, S. & Podd, J. The placebo effect: dissolving the expectancy versus conditioning debate. Psychol. Bull. 130, 324–340 (2004).

    Article  Google Scholar 

  43. Rainville, P., Duncan, G.H., Price, D.D., Carrier, B. & Bushnell, M.C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science 277, 968–971 (1997).

    Article  CAS  Google Scholar 

  44. Petrovic, P., Kalso, E., Petersson, K.M. & Ingvar, M. Placebo and opioid analgesia: imaging a shared neuronal network. Science 295, 1737–1740 (2002).

    Article  CAS  Google Scholar 

  45. Mayberg, H.S. et al. The functional neuroanatomy of the placebo effect. Am. J. Psychiatry 159, 728–737 (2002).

    Article  Google Scholar 

  46. Talairach, J. & Tournoux, P. Co-planar Stereotaxic Atlas of the Human Brain 3-dimensional Proportional System: An Approach to Cerebral Imaging (Thieme, Stuttgart, 1988).

    Google Scholar 

  47. Pfaffmann, C.P., Bartoshuck, L.M. & McBurney, D.H. Taste psychophysics. in Handbook of Sensory Physiology: Chemical Senses, Taste (eds. Autrum, H., Jang, R., Loewenstein, W.R., MacKay, D.M. & Teuber, H.L.) 75–101 (Springer-Verlag, Berlin, 1971).

    Google Scholar 

  48. Lancaster, J.L. et al. Automated tailarach atlas labels for functional brain mapping. Hum. Brain Mapp. 10, 120–131 (2000).

    Article  CAS  Google Scholar 

  49. Cumming, G. & Finch, S. Inference by eye: confidence intervals and how to read pictures of data. Am. Psychol. 60, 170–180 (2005).

    Article  Google Scholar 

  50. Loftus, G.R. & Masson, M.E. Using confidence intervals in within-subject designs. Psychon. Bull. Rev. 1, 476–490 (1994).

    Article  CAS  Google Scholar 

Download references

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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Authors and Affiliations

  1. Departments of Psychiatry and Psychology, Waisman Laboratory for Brain Imaging and Behavior, Waisman Center, University of Wisconsin, 1500 Highland Avenue, Madison, 53705-2274, Wisconsin, USA

    Jack B Nitschke, Gregory E Dixon, Issidoros Sarinopoulos, Sarah J Short & Richard J Davidson

  2. Department of Psychology, Center for the Study of Brain, Mind and Behavior, Princeton University, Princeton, 08544, New Jersey, USA

    Jonathan D Cohen

  3. Department of Psychology, Columbia University, 1190 Amsterdam Avenue, New York, 10027, New York, USA

    Edward E Smith

  4. Department of Psychology, Harvard University, Cambridge, 02138, Massachusetts, USA

    Stephen M Kosslyn

  5. Mind Brain Body and Health Initiative, University of Texas Medical Branch, Galveston, 77555, Texas, USA

    Robert M Rose

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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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