The ability of the taste system to identify a tastant (what it tastes like) enables animals to recognize and discriminate between the different basic taste qualities1,2. The valence of a tastant (whether it is appetitive or aversive) specifies its hedonic value and elicits the execution of selective behaviours. Here we examine how sweet and bitter are afforded valence versus identity in mice. We show that neurons in the sweet-responsive and bitter-responsive cortex project to topographically distinct areas of the amygdala, with strong segregation of neural projections conveying appetitive versus aversive taste signals. By manipulating selective taste inputs to the amygdala, we show that it is possible to impose positive or negative valence on a neutral water stimulus, and even to reverse the hedonic value of a sweet or bitter tastant. Remarkably, mice with silenced neurons in the amygdala no longer exhibit behaviour that reflects the valence associated with direct stimulation of the taste cortex, or with delivery of sweet and bitter chemicals. Nonetheless, these mice can still identify and discriminate between tastants, just as wild-type controls do. These results help to explain how the taste system generates stereotypic and predetermined attractive and aversive taste behaviours, and support the existence of distinct neural substrates for the discrimination of taste identity and the assignment of valence.
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We thank M. Tessier-Lavigne, N. Renier and P. Ariel for help with CUBIC; members of the Zuker laboratory and R. Axel for helpful discussions. We also acknowledge the Bio-Imaging Resource Center at Rockefeller University. Research reported in this publication was supported by the National Institute on Drug Abuse of the National Institutes of Health under award number R01DA035025 (C.S.Z). N.J.P.R. is supported by the Intramural Research Program of the NIH, NIDCR; and C.D.S. was supported by R01 MH082017 from NIMH. C.S.Z. is an investigator of the Howard Hughes Medical Institute and a Senior Fellow at Janelia Farm Research Campus.
Nature thanks I. de Araujo and P. Kenny for their contribution to the peer review of this work.
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Nature Reviews Neuroscience (2018)