Neural activity from receptors in the anterior tongue gives rise to a gustatory message that reflects the activation of both the taste and trigeminal somatosensory pathways. Currently not understood, and is the focus of this application, are the peripheral and central mechanisms regarding how the trigeminal (TG) system influences the taste system. The overall goals in this proposal are (1) to determine how compounds that activate TG neurons can modulate responses evoked from taste receptors cells (TRCs) and chorda tympani (CT) neurons, and (2) to quantify the contributions of the trigeminal somatosensory (mechanosenosry and nociceptive) pathways to the encoding of gustatory information in the insular cortex. It is proposed that, when activated, TG neurons will release neuropeptides, such as substance P and CCK, that will bind to receptors on TRCs and thereby modulate them. That in turn will modulate the activity of CT neurons to lingual applications of NaCl, acid, sucrose, and quinine. This hypothesis will be tested by activating the TG nerve electrically and chemically (e.g., with capsaicin, the pungent ingredient in hot pepper) and also by comparing CT responses before during and after the system injection of agonists and antagonists of substance P and CCK. A variety of methods (RT-PCR, immunocytochemistry, patch clamp, and measuring changes in intracellular calcium) will be used to determine whether CT modulation by TG activators such as capsaicin, is direct (on TRCs) and/or indirect via peptide release. Emphasis will be on identifying receptors for neuropeptides, capsaicin (VR1), and proton-gated channels in TRCs, lingual epithelium and geniculate ganglion neurons. To quantify the contribution of the TG somatosenory pathways to the cortical encoding of gustatory information, bundles of microelectrodes will be implanted in the primary gustatory (insular) cortex. Then, in lightly anesthetized rats, the simultaneous responses of populations of single insular neurons to a set of standard tastants will be measured before and after the selective inactivation of TG ganglion innervating the anterior tongue, a procedure that will simulate lingual nerve injuries. In addition, cortical-cortical influences on gustatory coding will be tested by reversibly inactivating the primary somatosensory cortex (SI). Information obtained from both the peripheral and cortical recordings will provide novel molecular, cellular and circuit mechanisms regarding the modulation of sensory information, and quantitative information regarding the contributions of the TG system to gustatory coding.

Agency
National Institute of Health (NIH)
Institute
National Institute on Deafness and Other Communication Disorders (NIDCD)
Type
Research Project (R01)
Project #
5R01DC001065-10
Application #
6350552
Study Section
Special Emphasis Panel (ZRG1-IFCN-4 (01))
Program Officer
Davis, Barry
Project Start
1991-04-01
Project End
2005-01-31
Budget Start
2001-02-01
Budget End
2002-01-31
Support Year
10
Fiscal Year
2001
Total Cost
$290,395
Indirect Cost
Name
Duke University
Department
Biology
Type
Schools of Medicine
DUNS #
071723621
City
Durham
State
NC
Country
United States
Zip Code
27705
Tellez, Luis A; Perez, Isaac O; Simon, Sidney A et al. (2012) Transitions between sleep and feeding states in rat ventral striatum neurons. J Neurophysiol 108:1739-51
MacDonald, Christopher J; Meck, Warren H; Simon, Sidney A (2012) Distinct neural ensembles in the rat gustatory cortex encode salt and water tastes. J Physiol 590:3169-84
Tandon, Shashank; Simon, Sidney A; Nicolelis, Miguel A L (2012) Appetitive changes during salt deprivation are paralleled by widespread neuronal adaptations in nucleus accumbens, lateral hypothalamus, and central amygdala. J Neurophysiol 108:1089-105
Picazo-Juárez, Giovanni; Romero-Suárez, Silvina; Nieto-Posadas, Andrés et al. (2011) Identification of a binding motif in the S5 helix that confers cholesterol sensitivity to the TRPV1 ion channel. J Biol Chem 286:24966-76
Oliveira-Maia, A J; Roberts, C D; Simon, S A et al. (2011) Gustatory and reward brain circuits in the control of food intake. Adv Tech Stand Neurosurg 36:31-59
Oliveira-Maia, Albino J; Roberts, Craig D; Walker, Q David et al. (2011) Intravascular food reward. PLoS One 6:e24992
Gutierrez, Ranier; Simon, Sidney A (2011) Chemosensory processing in the taste - reward pathway. Flavour Fragr J 26:231-238
Gutierrez, Ranier; Simon, Sidney A; Nicolelis, Miguel A L (2010) Licking-induced synchrony in the taste-reward circuit improves cue discrimination during learning. J Neurosci 30:287-303
Carleton, Alan; Accolla, Riccardo; Simon, Sidney A (2010) Coding in the mammalian gustatory system. Trends Neurosci 33:326-34
Rosenbaum, Tamara; Simon, Sidney A; Islas, Leon D (2010) Ion channels in analgesia research. Methods Mol Biol 617:223-36

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