Neurons in the gustatory cortex (GC) respond to sensory stimuli with time-varying modulations of their firing rates. Electrophysiological recordings from anesthetized and awake animals have shown that firing activity can change over few seconds following the onset of stimulus presentation (Grossman et al., 2008; Gutierrez et al., 2010; Jones et al., 2007; Stapleton et al., 2006; Yamamoto et al., 1984b; Yokota et al., 2011). These dynamics are a critical feature of gustatory responses and are believed to mediate the processing of different aspects of gustatory information (Fontanini and Katz, 2006, 2009; Gutierrez et al., 2010; Katz et al., 2002a). While a great deal of work has focused on understanding the functional significance of these patterns, little is known about their genesis. I is not known, for instance, why some neurons display rapid taste responses, some are activated at much longer latencies (i.e. hundreds of milliseconds) and some others do not respond at all. Pharmacological experiments relying on local infusions of the GABA blocker bicuculline point to inhibition as a key player in shaping responses (Ogawa et al., 1998). However, the lack of synaptic resolution of extracellular techniques has limited our understanding of how interactions between inhibition and excitation could influence the time course of responses in different neurons. The experiments in this proposal are designed to test the general hypothesis that time-varying spiking responses are determined by specific combinations of excitation and inhibition. The use of in vivo intracellular techniques will allow to resolve synaptic potentials ad dissect the balance between excitation and inhibition in anesthetized rats (Haider et al., 2006; Stone et al., 2011; Wilent and Contreras, 2005). Intracellular injection of biocytin, followed by histological reconstructions, will be used to identify the cell type and the location of the neuron recorded. The ability to identify the recorded neurons will be instrumental in understanding whether cells in the different layers and divisions (granular, dysgranular and agranular) of GC show specific patterns of synaptic interactions. The analysis of synaptic responses to thalamic, amygdalar and gustatory stimulation will allow us to determine how specific elements in the circuit integrate bottom-up sensory inputs with top-down modulations This framework represents an entirely novel approach to the study of GC in intact animals and promises to provide the first integrative view of the synaptic bases of gustatory cortical processing.

Public Health Relevance

This proposal aims at understanding the synaptic basis of taste processing in the gustatory cortex. The experiments are designed to unveil how the integration of excitatory and inhibitory potentials shapes neural responses to gustatory stimuli in different subpopulations of cortical neurons. The contribution of two pathways, the thalamic and the amygdalar pathway, will be investigated. The combination of in vivo intracellular techniques, electrical stimulation, optogenetic approaches and sensory stimulation will allow us unprecedented resolution in the study of this largely unexplored topic in taste research. The results of this effort will provide novel and important insights on the cortical mechanism underlying taste processing. Identifying the role of different neural subpopulation and the contribution of thalamic and amygdalar pathways will provide selective targets for manipulating the perception of taste quality and valence in normal and pathological conditions.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC012543-04
Application #
8850422
Study Section
Somatosensory and Chemosensory Systems Study Section (SCS)
Program Officer
Sullivan, Susan L
Project Start
2012-07-01
Project End
2016-06-30
Budget Start
2015-07-01
Budget End
2016-06-30
Support Year
4
Fiscal Year
2015
Total Cost
Indirect Cost
Name
State University New York Stony Brook
Department
Other Basic Sciences
Type
Schools of Arts and Sciences
DUNS #
804878247
City
Stony Brook
State
NY
Country
United States
Zip Code
11794
Vincis, Roberto; Fontanini, Alfredo (2016) A gustocentric perspective to understanding primary sensory cortices. Curr Opin Neurobiol 40:118-124
Haley, Melissa S; Fontanini, Alfredo; Maffei, Arianna (2016) Laminar- and Target-Specific Amygdalar Inputs in Rat Primary Gustatory Cortex. J Neurosci 36:2623-37
Kusumoto-Yoshida, Ikue; Liu, Haixin; Chen, Billy T et al. (2015) Central role for the insular cortex in mediating conditioned responses to anticipatory cues. Proc Natl Acad Sci U S A 112:1190-5
Linster, Christiane; Fontanini, Alfredo (2014) Functional neuromodulation of chemosensation in vertebrates. Curr Opin Neurobiol 29:82-7