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Evidence for a large-scale brain system supporting allostasis and interoception in humans

Nature Human Behaviour volume 1, Article number: 0069 (2017) Cite this article

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Abstract

Large-scale intrinsic brain systems have been identified for exteroceptive senses (such as sight, hearing and touch). We introduce an analogous system for representing sensations from within the body, called interoception, and demonstrate its relation to regulating peripheral systems in the body, called allostasis. Employing the recently introduced Embodied Predictive Interoception Coding (EPIC) model, we used tract-tracing studies of macaque monkeys, followed by two intrinsic functional magnetic resonance imaging samples (N = 280 and N = 270) to evaluate the existence of an intrinsic allostatic–interoceptive system in the human brain. Another sample (N = 41) allowed us to evaluate the convergent validity of the hypothesized allostatic–interoceptive system by showing that individuals with stronger connectivity between system hubs performed better on an implicit index of interoceptive ability related to autonomic fluctuations. Implications include insights for the brain’s functional architecture, dissolving the artificial boundary between mind and body, and unifying mental and physical illness.

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Figure 1: We identified key visceromotor cortical regions (in red) that provide cortical control of the body’s internal milieu.
Figure 2: Eight regions (‘seeds’) used to estimate the unified allostasis/interoceptive system connecting the cortical and amygdalar visceromotor regions and primary interoceptive regions.
Figure 3: The unified allostatic–interoceptive system is composed of two large-scale intrinsic networks that share several hubs.
Figure 4: Subcortical connectivity of the two integrated intrinsic networks within the allostatic–interoceptive system (N = 280; P < 0.05 uncorrected).
Figure 5: The default mode and salience networks each support a wide array of psychological functions.

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Acknowledgements

We thank M. A. Garcia-Cabezas for comments and advice on neuroanatomy, and H. Evrard for discussions on anatomical connectivity. This research was supported by funds from the National Institutes on Aging (R01 AG030311) to L.F.B. and B.C.D., the US Army Research Institute for the Behavioral and Social Sciences Contracts (W5J9CQ-11-C-0046 and W5J9CQ-12-C-0049) to L.F.B., the National Cancer Institute (U01 CA193632) to L.F.B., the National Institute of Mental Health Ruth L. Kirschstein National Research Service Award (F32MH096533) to I.R.K., the National Cancer Institute (UG1 CA189961 and R25 CA102618) to support I.R.K., the National Institutes of Mental Health (K01MH096175-01) and Oklahoma Tobacco Research Center grants to W.K.S., a Fyssen Foundation postdoctoral fellowship and Alicia Koplowitz Foundation short-term fellowship to L.C. and the Fonds de recherche sante Quebec fellowship award to C.X. The views, opinions and findings contained in this paper are those of the authors and shall not be construed as an official Department of the Army position, policy or decision, unless so designated by other documents. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Author notes

  1. Bradford C. Dickerson and Lisa Feldman Barrett: These authors jointly supervised this work.

Authors and Affiliations

  1. Department of Psychology, Northeastern University, 105–107 Forsyth Street, Boston, 02115, Massachusetts, USA

    Ian R. Kleckner, Jiahe Zhang, Lorena Chanes, Karen S. Quigley & Lisa Feldman Barrett

  2. Department of Neurology, Massachusetts General Hospital and Harvard Medical School, 15 Parkman Street, Boston, 02114, Massachusetts, USA

    Alexandra Touroutoglou

  3. Athinoula A. Martinos Center for Biomedical Imaging, 149 13th Street, Charlestown, 02129, Massachusetts, USA

    Alexandra Touroutoglou, Lorena Chanes, Chenjie Xia, Bradford C. Dickerson & Lisa Feldman Barrett

  4. Psychiatric Neuroimaging Division, Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School, 55 Fruit Street Boston, Massachusetts 02114, USA

    Alexandra Touroutoglou, Lorena Chanes & Lisa Feldman Barrett

  5. Department of Neurology, Frontotemporal Disorders Unit, Massachusetts General Hospital and Harvard Medical School, 55 Fruit Street Boston, Massachusetts 02114, USA

    Chenjie Xia & Bradford C. Dickerson

  6. Laureate Institute for Brain Research, 6655 South Yale Avenue, Tulsa, 74136, Oklahoma, USA

    W. Kyle Simmons

  7. School of Community Medicine, The University of Tulsa, 4502 East 41st Street, Tulsa, Oklahoma 74135, USA

    W. Kyle Simmons

  8. Edith Nourse Rogers Memorial VA Hospital, 200 Springs Road, Bedford, 01730, Massachusetts, USA

    Karen S. Quigley

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Contributions

The study was designed and analysed by all the authors, and the manuscript was written by I.R.K. and L.F.B. with comments and edits from other authors.

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Kleckner, I., Zhang, J., Touroutoglou, A. et al. Evidence for a large-scale brain system supporting allostasis and interoception in humans. Nat Hum Behav 1, 0069 (2017). https://doi.org/10.1038/s41562-017-0069

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