Homeostatic circuits selectively gate food cue responses in insular cortex

Yoav Livneh; Rohan N Ramesh; Christian R Burgess; Kirsten M Levandowski; Joseph C Madara; Henning Fenselau; Glenn J Goldey; Veronica E Diaz; Nick Jikomes; Jon M Resch; Bradford B Lowell; Mark L Andermann

doi:10.1038/nature22375

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Homeostatic circuits selectively gate food cue responses in insular cortex

Journal article

Open access

Peer reviewed

Homeostatic circuits selectively gate food cue responses in insular cortex

Yoav Livneh, Rohan N Ramesh, Christian R Burgess, Kirsten M Levandowski, Joseph C Madara, Henning Fenselau, Glenn J Goldey, Veronica E Diaz, Nick Jikomes, Jon M Resch, …

Nature (London), Vol.546(7660), pp.611-616

06/29/2017

DOI: 10.1038/nature22375

PMCID: PMC5577930

PMID: 28614299

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Abstract

Physiological needs bias perception and attention to relevant sensory cues. This process is 'hijacked' by drug addiction, causing cue-induced cravings and relapse. Similarly, its dysregulation contributes to failed diets, obesity, and eating disorders. Neuroimaging studies in humans have implicated insular cortex in these phenomena. However, it remains unclear how 'cognitive' cortical representations of motivationally relevant cues are biased by subcortical circuits that drive specific motivational states. Here we develop a microprism-based cellular imaging approach to monitor visual cue responses in the insular cortex of behaving mice across hunger states. Insular cortex neurons demonstrate food-cue-biased responses that are abolished during satiety. Unexpectedly, while multiple satiety-related visceral signals converge in insular cortex, chemogenetic activation of hypothalamic 'hunger neurons' (expressing agouti-related peptide (AgRP)) bypasses these signals to restore hunger-like response patterns in insular cortex. Circuit mapping and pathway-specific manipulations uncover a pathway from AgRP neurons to insular cortex via the paraventricular thalamus and basolateral amygdala. These results reveal a neural basis for state-specific biased processing of motivationally relevant cues.

Cues

Peptide Fragments - metabolism

Hypothalamus - physiology

Mice, Inbred C57BL

Homeostasis

Male

Agouti-Related Protein - metabolism

Cerebral Cortex - cytology

Neural Pathways

Satiety Response - physiology

Animals

Hypothalamus - cytology

Cerebral Cortex - physiology

Mice

Neurons - metabolism

Photic Stimulation

Hunger - physiology

Food

Details

Title: Subtitle: Homeostatic circuits selectively gate food cue responses in insular cortex
Creators: Yoav Livneh - Division of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Rohan N Ramesh - Program in Neuroscience, Harvard Medical School, Boston, Massachusetts 02115, USA
Christian R Burgess - Division of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Kirsten M Levandowski - Division of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Joseph C Madara - Division of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Henning Fenselau - Division of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Glenn J Goldey - Division of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Veronica E Diaz - Division of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Nick Jikomes - Program in Neuroscience, Harvard Medical School, Boston, Massachusetts 02115, USA
Jon M Resch - Division of Endocrinology, Diabetes and Metabolism, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Massachusetts 02215, USA
Bradford B Lowell - Program in Neuroscience, Harvard Medical School, Boston, Massachusetts 02115, USA
Mark L Andermann - Program in Neuroscience, Harvard Medical School, Boston, Massachusetts 02115, USA
Resource Type: Journal article
Publication Details: Nature (London), Vol.546(7660), pp.611-616
DOI: 10.1038/nature22375
PMID: 28614299
PMCID: PMC5577930
NLM abbreviation: Nature
ISSN: 0028-0836
eISSN: 1476-4687
Publisher: England
Grant note: R01 DK096010 / NIDDK NIH HHS R01 DK111401 / NIDDK NIH HHS R01 DK089044 / NIDDK NIH HHS DP2 DK105570 / NIDDK NIH HHS Howard Hughes Medical Institute R01 DK075632 / NIDDK NIH HHS R01 DK109930 / NIDDK NIH HHS F32 DK103387 / NIDDK NIH HHS P30 DK046200 / NIDDK NIH HHS F31 DK105678 / NIDDK NIH HHS P30 DK057521 / NIDDK NIH HHS
Language: English
Date published: 06/29/2017
Academic Unit: Iowa Neuroscience Institute; Neuroscience and Pharmacology
Record Identifier: 9984065750602771

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