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Category-specific integration of homeostatic signals in caudal but not rostral human insula

Nature Neuroscience volume 16, pages 1551–1552 (2013)Cite this article

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Abstract

Prevailing theories hold that the insula is functionally organized along its caudal-to-rostral axis, with posterior regions coding lower-level sensory information and anterior regions coding higher-level stimulus significance relative to the body's homeostatic needs. Contrary to predictions of this model, the response of the taste-sensitive region of the caudal, but not rostral, insula to food images was directly related to the body's homeostatic state as indexed by levels of peripheral glucose.

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Figure 1: fMRI task descriptions.
Figure 2: Insula gustatory cortex responses to food and non-food pictures as a function of circulating glucose level.

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Acknowledgements

We would like to thank K. Burrows for help with data management and analysis of the high-sweetness and low-sweetness food pictures. This research supported by the Intramural Research Programs of the NIMH and the NIDDK, as well as by NIMH grant K01MH096175-01 to W.K.S., a grant from the Oklahoma Center for the Advancement of Science and Technology (OCAST HR10-141) to W.K.S., a NARSAD Young Investigator Award to W.K.S., a grant to W.K.S. from the Oklahoma Tobacco Research Center, and The William K. Warren Foundation. The study was conducted under NIH Clinical Study Protocol 09-DK-0081 (ClinicalTrials.gov ID NCT00846040).

Author information

Authors and Affiliations

  1. Laureate Institute for Brain Research, Tulsa, Oklahoma, USA

    W Kyle Simmons & Jason A Avery

  2. Faculty of Community Medicine, The University of Tulsa, Tulsa, Oklahoma, USA

    W Kyle Simmons

  3. Laboratory of Brain and Cognition, National Institute of Mental Health (NIHM), National Institutes of Health (NIH), Bethesda, Maryland, USA

    W Kyle Simmons, Kristina M Rapuano, Seth J Kallman, John E Ingeholm, Stephen J Gotts & Alex Martin

  4. Laboratory of Biological Modeling, National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK), NIH, Bethesda, Maryland, USA

    Bernard Miller & Kevin D Hall

  5. Department of Biological Science, The University of Tulsa, Tulsa, Oklahoma, USA

    Jason A Avery

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Contributions

W.K.S. designed and conducted the experiments, contributed to data analysis and wrote the manuscript. K.M.R. and S.J.K. conducted the experiments and contributed to data analysis, J.E.I. contributed to the construction of equipment for the study and conducted the experiment, B.M. conducted the experiment and contributed to interpreting metabolic data, S.J.G. contributed to data analysis and writing the manuscript, J.A.A. contributed to writing the manuscript, and K.D.H. and A.M. helped design the experiment and contributed to writing the manuscript.

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Correspondence to W Kyle Simmons.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Overall study design.

All participants ate a standard meal at noon, with blood draw at 13:45 and fMRI scanning at 14:00. In the scanner, subjects performed the food/non-food picture repetition detection task prior to performing the gustatory mapping task. In the scanner pictures were presented to subjects in full-color.

Supplementary Figure 2 Category-specific integration of circulating glucose and response to food vs nonfood pictures.

Although the anterior insula gustatory cortex exhibited virtually no relationship between glucose and responses to food images compared to non-food images, the more caudal dorsal mid-insula exhibited a strong food-specific sensitivity to circulating glucose.

Supplementary Figure 3 Category-specific integration of circulating glucose and response to high sweet and low sweet food pictures.

In the anterior insula there was little relationship between glucose and either the high sweet or the low sweet category responses, and the two classes of food did not differ in their association with glucose. In the dorsal mid-insula, both the high sweet and the low sweet category responses were related to circulating glucose levels. The two functions did not differ between each other in their association to circulating glucose, perhaps because the dorsal mid-insula taste cortex's responses to food pictures may be relatively more strongly related to inferences about the overall taste intensity of the pictured foods, rather than inferences about their sweetness.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–3 (PDF 806 kb)

Supplementary Table 1

Brain regions exhibiting greater activation to tastants than to tasteless control solution in the Gustatory Mapping Task (PDF 95 kb)

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Simmons, W., Rapuano, K., Kallman, S. et al. Category-specific integration of homeostatic signals in caudal but not rostral human insula. Nat Neurosci 16, 1551–1552 (2013). https://doi.org/10.1038/nn.3535

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