Laminar differences in taste coding: a circuit perspective

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 DESCRIPTION (provided by applicant): How is gustatory information represented in the cortex? The answer to this question has been one of the mostly intensely debated topics in the field of gustatory neuroscience1-3. Two theories have been proposed and discussed over the past decades. According to the labeled-line theory the physiochemical identity of a gustatory stimulus is encoded by specific subsets of neurons, each of which is narrowly tuned to a single taste quality (i.e. salty, sweet, sour, bitter or umami)4-7. An alternative theory, the across-neuron pattern theory, postulates that taste coding relies on the combined activity of large ensembles of cortical neurons8. According to this theory, neurons do not need to be selective for specific taste qualities, instead each neuron can densely represent information by encoding multiple qualities3,9. Both theories are supported by experimental evidence. While a recent 2-photon calcium imaging study suggested the exclusive presence of narrowly tuned neurons in GC of anesthetized mice7; years of electrophysiological recordings in anesthetized and alert rodents demonstrate the presence of both narrowly tuned and densely coding neurons in GC10-13. Despite evidence that neurons using different coding strategies exist in GC, the debate is still polarized and no unifying view of taste coding in the cortex has emerged. The overarching goal of this proposal is to test the hypothesis that narrowly tuned and densely coding neurons reflect different stages of cortical processing. Specifically, we propose that the coding scheme varies depending on the cortical layers, with superficial layers (i.e., layers 2/3) featuring narroly tuned neurons and deep layers (i.e., layers 4 and 5) containing densely coding neurons. In addition, the experiments in this proposal aim at providing a mechanistic explanation for these differences, linking coding properties with laminar-dependent variations in inhibitory drive. The experiments will rely on a combination of sophisticated electrophysiological approaches to directly relate coding properties, balance between excitation and inhibition, and properties of local microcircuits. The framework of this grant is firmly grounded in the literature on cortical coding of sensory information14-17, and supported by our preliminary results, showing layer-specific differences in taste response properties and local connectivity. This research will help the field go beyond a dated debate and will move the discussion on taste coding toward a more circuit-oriented perspective. If successful this research will provide, for the first time, a unifid view of taste coding in cortical circuits of alert rodents.