Editors' ChoiceNeuroscience

Hunger signals suppress risk perception

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Sci. Signal.  13 Dec 2016:
Vol. 9, Issue 458, pp. ec292
DOI: 10.1126/scisignal.aam5658

Animals respond to diverse cues in their environment through the integration of multiple sensory inputs, from which decisions can affect the animal’s survival. For example, a decision to venture out toward a food source exposes the animal to predators and other dangerous elements. Thus, threat versus reward is weighed during decision-making that modulates animal behavior. In the nematode worm Caenorhabditis elegans, attractive food odors and aversive hyperosmolarity (which can desiccate and kill the worm) are detected by chemosensory AWA and polymodal nociceptive ASH neurons, respectively, which propagate through a network of interneurons that are ultimately integrated onto RIM sensorimotor interneurons, which mediate a change in the worm’s direction of motion (turning toward or away from the stimulus). Using a food deprivation protocol in C. elegans, in which spots of diluted diacetyl food odor are applied to agar outside a barrier ring of hyperosmotic fructose, Ghosh et al. found that hunger signals effectively override this integrated network and suppress the perception of the threat of dessication and death (see also Li et al.). Calcium imaging and cell-specific manipulation of gene expression revealed that activation of the G protein–coupled receptor PDFR-1 by the neuropeptide PDF-2 in RIM sensorimotor interneurons stimulated secretion of tyramine from RIM neurons, which provided positive feedback to the polymodal (ASH) neurons through a tyramine receptor TYRA-2, thereby enhancing the perception of threat. Worms lacking pdf-2, tyra-2, or tdc-1 (encoding the enzyme that synthesizes tyramine) more readily moved across the hyperosmotic barrier than did wild-type worms. Computational modeling and in vivo experiments showed that one hour of food deprivation inhibited RIM neuron function, thereby increasing threat tolerance and the willingness to cross the hyperosmotic barrier. These findings reveal underlying molecular mechanisms and complex circuitry controlling multisensory threat-reward decision-making.

D. D. Ghosh, T. Sanders, S. Hong, L. Y. McCurdy, D. L. Chase, N. Cohen, M. R. Koelle, M. N. Nitabach, Neural architecture of hunger-dependent multisensory decision making in C. elegans. Neuron 92, 1049–1062 (2016). [PubMed]

Z. Li, A. J. Iliff, X. Z. S. Xu, An elegant circuit for balancing risk and reward. Neuron 92, 933–935 (2016). [PubMed]