The coding of valence and identity in the mammalian taste system

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.The identity and hedonic value of tastes are encoded in distinct neural substrates; in mice, the amygdala is necessary and sufficient to drive valence-specific behaviours in response to bitter or sweet taste stimuli, and the cortex can independently represent taste identity.

[1]  Edmund C Schwartz,et al.  Neural Representations of Unconditioned Stimuli in Basolateral Amygdala Mediate Innate and Learned Responses , 2015, Cell.

[2]  K. Tye,et al.  From circuits to behaviour in the amygdala , 2015, Nature.

[3]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[4]  N. Onoda,et al.  Cortical spatial aspects of optical intrinsic signals in response to sucrose and NaCl stimuli , 2004, Neuroreport.

[5]  Kristin Scott Taste Recognition: Food for Thought , 2005, Neuron.

[6]  Karl Deisseroth,et al.  Molecular and Circuit-Dynamical Identification of Top-Down Neural Mechanisms for Restraint of Reward Seeking , 2017, Cell.

[7]  Alan Carleton,et al.  Differential Spatial Representation of Taste Modalities in the Rat Gustatory Cortex , 2007, The Journal of Neuroscience.

[8]  Stephen Maren Neurobiology of Pavlovian fear conditioning. , 2001, Annual review of neuroscience.

[9]  Brian Zingg,et al.  AAV-Mediated Anterograde Transsynaptic Tagging: Mapping Corticocollicular Input-Defined Neural Pathways for Defense Behaviors , 2017, Neuron.

[10]  K. Conzelmann,et al.  Central amygdala circuits modulate food consumption through a positive-valence mechanism , 2017, Nature Neuroscience.

[11]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

[12]  Anirvan Ghosh,et al.  Chemogenetic Synaptic Silencing of Neural Circuits Localizes a Hypothalamus→Midbrain Pathway for Feeding Behavior , 2014, Neuron.

[13]  J. Price,et al.  A description of the amygdaloid complex in the rat and cat with observations on intra‐amygdaloid axonal connections , 1978, The Journal of comparative neurology.

[14]  Michele Pignatelli,et al.  Antagonistic negative and positive neurons of the basolateral amygdala , 2016, Nature Neuroscience.

[15]  David J. Anderson,et al.  Central amygdala PKC-δ+ neurons mediate the influence of multiple anorexigenic signals , 2014, Nature Neuroscience.

[16]  Paul H. E. Tiesinga,et al.  The Scalable Brain Atlas: Instant Web-Based Access to Public Brain Atlases and Related Content , 2013, Neuroinformatics.

[17]  K. Tye,et al.  Organization of Valence-Encoding and Projection-Defined Neurons in the Basolateral Amygdala , 2018, Cell reports.

[18]  Xiaoke Chen,et al.  A Gustotopic Map of Taste Qualities in the Mammalian Brain , 2011, Science.

[19]  Allan R. Jones,et al.  A robust and high-throughput Cre reporting and characterization system for the whole mouse brain , 2009, Nature Neuroscience.

[20]  B. Roth,et al.  Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand , 2007, Proceedings of the National Academy of Sciences.

[21]  N. Canteras,et al.  Integrated Control of Predatory Hunting by the Central Nucleus of the Amygdala , 2017, Cell.

[22]  E. Susaki,et al.  Whole-Brain Imaging with Single-Cell Resolution Using Chemical Cocktails and Computational Analysis , 2014, Cell.

[23]  G. Schoenbaum,et al.  Neural Encoding in Orbitofrontal Cortex and Basolateral Amygdala during Olfactory Discrimination Learning , 1999, The Journal of Neuroscience.

[24]  Allan R. Jones,et al.  Genome-wide atlas of gene expression in the adult mouse brain , 2007, Nature.

[25]  Lief E. Fenno,et al.  Amygdala circuitry mediating reversible and bidirectional control of anxiety , 2011, Nature.

[26]  S. Ikemoto,et al.  Similar Roles of Substantia Nigra and Ventral Tegmental Dopamine Neurons in Reward and Aversion , 2014, The Journal of Neuroscience.

[27]  S. Tonegawa,et al.  Basolateral to Central Amygdala Neural Circuits for Appetitive Behaviors , 2017, Neuron.

[28]  Ian R. Wickersham,et al.  A Circuit Mechanism for Differentiating Positive and Negative Associations , 2015, Nature.

[29]  Alan C Spector,et al.  The representation of taste quality in the mammalian nervous system. , 2005, Behavioral and cognitive neuroscience reviews.

[30]  Arno Klein,et al.  A reproducible evaluation of ANTs similarity metric performance in brain image registration , 2011, NeuroImage.

[31]  N. Ryba,et al.  Common Sense about Taste: From Mammals to Insects , 2009, Cell.

[32]  N. Ryba,et al.  Coding of Sweet, Bitter, and Umami Tastes Different Receptor Cells Sharing Similar Signaling Pathways , 2003, Cell.

[33]  H. Grill,et al.  The taste reactivity test. II. Mimetic responses to gustatory stimuli in chronic thalamic and chronic decerebrate rats , 1978, Brain Research.

[34]  Yueqing Peng,et al.  Sweet and bitter taste in the brain of awake behaving animals , 2015, Nature.

[35]  Dimitri Perrin,et al.  Advanced CUBIC protocols for whole-brain and whole-body clearing and imaging , 2015, Nature Protocols.

[36]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.