The gustatory cortex (GC) receives modulatory inputs from multiple regions of the limbic system. Lateral hypothalamus, medial prefrontal cortex, mediodorsal thalamus and basolateral amygdala (BLA) are all known to send projections to GC (Saper 1982; Allen, Saper et al. 1991; Maffei, Haley et al. 2012). Among these inputs, those from the BLA are the ones whose functional significance has been studied the most. Pharmacological and electrophysiological experiments in alert animals have suggested that inputs from BLA are necessary for GC to process information pertaining to the hedonic value of gustatory stimuli (Piette, Baez- Santiago et al. 2012) and the anticipatory value of taste-predictive cues (Samuelsen, Gardner et al. 2012). In addition, plastic changes of the BLA-GC connection have been associated with taste aversion learning (Guzman-Ramos and Bermudez-Rattoni 2012). Despite the abundance of studies investigating the functional role of the BLA-GC connection (Jones, French et al. 1999; Grossman, Fontanini et al. 2008; Guzman-Ramos and Bermudez-Rattoni 2012; Piette, Baez- Santiago et al. 2012; Parkes and Balleine 2013), very little is known on the synaptic organization and plasticity of these inputs. Evidence from intracellular and extracellular recordings in vivo suggests that BLA-GC inputs might exert complex excitatory as well as inhibitory actions (Yamamoto, Azuma et al. 1984; Hanamori 2009; Stone, Maffei et al. 2011), yet no information is available on the synaptic mechanisms underlying these effects. Furthermore, while analysis of BLA evoked potentials in GC provides evidence for learning-related plasticity at this connection (Escobar, Chao et al. 1998; Jones, French et al. 1999; Escobar and Bermudez-Rattoni 2000; Rodriguez-Duran, Castillo et al. 2011), the mechanisms, rules and postsynaptic targets of this plasticity are unknown. Until recently it has been impossible to selectively activate BLA afferents in vitro to finely dissect th GC circuits recruited by amygdalar inputs. The availability of optogenetic tools has however changed the situation (Zhang, Gradinaru et al. 2010; Stuber, Sparta et al. 2011; Yizhar, Fenno et al. 2011; Britt and Bonci 2013; Wang, Kloc et al. 2013), finally allowing us the fundamental questions pertaining to the synaptic organization of amygdalar afferents to GC to be addressed. The experiments proposed here rely on these novel techniques, combined with in vitro whole cell patch clamp recordings, to directly measure the properties of amygdalar synapses onto pyramidal cells and inhibitory interneurons in GC. This methodological approach will be complemented with pharmacological and behavioral manipulations to test the following hypotheses: 1) BLA afferents make direct functional synapses onto different cell types within GC local circuits; 2) Synaptic inputs onto pyramidal neurons and inhibitory interneurons show activity-dependent plasticity; 3) The strength of BLA- GC synapses is affected by hedonic learning. Altogether these experiments will allow us to investigate the synaptic organization of BLA-GC inputs, their plasticity and the changes associated with aversion learning. This framework represents an entirely novel approach to the study of GC inputs in brain slices and promises to provide the first circuit-level description of amygdalar synapses in the gustatory cortex.

Public Health Relevance

The gustatory cortex (GC), i.e. the primary cortical area devoted to elaborate taste information, receives inputs from a series of brain regions. The basolateral nucleus of amygdala (BLA) is one of the areas whose role in influencing GC has been studied the most. Projections from the BLA are fundamental for shaping the way in which GC processes gustatory information and learns about taste valence. Yet, very little is known about the properties of the BLA inputs to GC. For instance it is not known whether and how BLA inputs excite different subpopulations of GC neurons; are BLA inputs distributed only on pyramidal neurons, as proposed in the past, or they also activate subpopulations of inhibitory interneurons, as newer evidence might suggest? In addition very little is known on whether BLA synapses onto GC neurons are plastic and how they change with learning. These are all fundamental questions that need to be addressed if we want to understand how BLA shapes activity in GC. The experiments in this grant will rely on a combination of in vitro patch clamp recordings, optogenetic tools, pharmacological manipulations and behavioral training to investigate the synaptic organization and plasticity of the BLA-GC connection. The results of this effort will provide novel and important insights on the cortical mechanism underlying taste processing. Understanding how neural circuits in GC are regulated by BLA will provide potential pharmacological targets for shaping the perception of taste quality and valence in normal and pathological conditions.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
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Somatosensory and Chemosensory Systems Study Section (SCS)
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Sullivan, Susan L
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State University New York Stony Brook
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Stony Brook
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Tatti, Roberta; Haley, Melissa S; Swanson, Olivia K et al. (2017) Neurophysiology and Regulation of the Balance Between Excitation and Inhibition in Neocortical Circuits. Biol Psychiatry 81:821-831
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Samuelsen, Chad L; Fontanini, Alfredo (2017) Processing of Intraoral Olfactory and Gustatory Signals in the Gustatory Cortex of Awake Rats. J Neurosci 37:244-257
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