title: Capsaicin induces theta-band synchronization between gustatory and autonomic insular cortices.
abstract: In the insular cortex, the primary gustatory area caudally adjoins the primary autonomic area that is involved in visceral sensory-motor integration. However, it has not been addressed whether neural activity in the gustatory insula (Gu-I) is coordinated with that in the autonomic insula (Au-I). We have demonstrated that TRPV1 activation in Gu-I induces theta-band synchronization between Gu-I and Au-I in rat slice preparations. Electron-microscopic immunohistochemistry revealed that TRPV1 immunoreactivity was much higher in Gu-I than in Au-I, and was mostly detected in dendritic spines receiving asymmetrical synapses. Whole-cell voltage-clamp recordings revealed that, in Gu-I, capsaicin-induced currents in layer 3 (L3) pyramidal cells (PCs) displayed no apparent desensitization, while those in layer 5 (L5) PCs displayed Ca(2+)-dependent desensitization, suggesting that L3 and L5 PCs respond differentially to TRPV1 activation. Voltage-sensitive dye imaging demonstrated that TRPV1 activation in Gu-I can alter an optical response with a monophasic and columnar temporospatial pattern evoked within Gu-I into an oscillatory one extending over Gu-I and Au-I. Power and cross-power spectral analyses of optical responses revealed theta-band synchronization between Gu-I and Au-I. Whole-cell current-clamp recordings demonstrated that such theta-band waves were mediated by sustained rhythmic firings at 4 and 8 Hz in L3 and L5 PCs, respectively. These results strongly suggested that theta-band oscillatory neural coordination between Gu-I and Au-I was induced by two distinct TRPV1-mediated theta-rhythm firings in L3 and L5 PCs in Gu-I. This network coordination induced by TRPV1 activation could be responsible for autonomic responses to tasting and ingesting spicy foods.
authors.affiliation: Department of Neuroscience and Oral Physiology, Osaka University Graduate School of Dentistry, Suita, Osaka 565-0871, Japan.
authors.forename: Mitsuru
authors.initials: M
authors.lastname: Saito
authors.forename: Hiroki
authors.initials: H
authors.lastname: Toyoda
authors.forename: Shinpei
authors.initials: S
authors.lastname: Kawakami
authors.forename: Hajime
authors.initials: H
authors.lastname: Sato
authors.forename: Yong Chul
authors.initials: YC
authors.lastname: Bae
authors.forename: Youngnam
authors.initials: Y
authors.lastname: Kang
mesh_terms: D000704:Analysis of Variance; D000818:Animals; D000831:Animals, Newborn; D000075368:Anoctamins; D001703:Biophysics; D002118:Calcium / Q000494:pharmacology; D002211:Capsaicin / Q000494:pharmacology*; D002540:Cerebral Cortex / Q000166:cytology* / Q000187:drug effects / Q000502:physiology; D018118:Chloride Channels; D004224:Diterpenes / Q000494:pharmacology; D004305:Dose-Response Relationship, Drug; D004558:Electric Stimulation; D004791:Enzyme Inhibitors / Q000494:pharmacology; D005260:Female; D066298:In Vitro Techniques; D008297:Male; D008564:Membrane Potentials / Q000187:drug effects / Q000502:physiology; D016253:Microscopy, Immunoelectron; D009474:Neurons / Q000187:drug effects / Q000502:physiology* / Q000648:ultrastructure; D018408:Patch-Clamp Techniques; D051381:Rats; D017207:Rats, Sprague-Dawley; D018689:Sensory System Agents / Q000494:pharmacology*; D013347:Subcellular Fractions / Q000378:metabolism / Q000648:ultrastructure; D050916:TRPV Cation Channels / Q000378:metabolism / Q000648:ultrastructure; D013755:Tetradecanoylphorbol Acetate / Q000031:analogs & derivatives / Q000494:pharmacology; D013826:Theta Rhythm / Q000187:drug effects*; D056969:Voltage-Sensitive Dye Imaging / Q000379:methods
chemical_list: C575623:Ano2 protein, rat; D000075368:Anoctamins; D018118:Chloride Channels; D004224:Diterpenes; D004791:Enzyme Inhibitors; D018689:Sensory System Agents; D050916:TRPV Cation Channels; C493922:Trpv1 protein, rat; C468130:iodoresiniferatoxin; C020922:4-O-methyl-12-O-tetradecanoylphorbol 13-acetate; D013755:Tetradecanoylphorbol Acetate; D002211:Capsaicin; D002118:Calcium