TY - JOUR
T1 - Capsaicin induces theta-band synchronization between gustatory and autonomic insular cortices
AU - Saito, Mitsuru
AU - Toyoda, Hiroki
AU - Kawakami, Shinpei
AU - Sato, Hajime
AU - Bae, Yong Chul
AU - Kang, Youngnam
PY - 2012/9/26
Y1 - 2012/9/26
N2 - 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 Ca2+-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.
AB - 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 Ca2+-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.
UR - http://www.scopus.com/inward/record.url?scp=84866640565&partnerID=8YFLogxK
U2 - 10.1523/JNEUROSCI.5906-11.2012
DO - 10.1523/JNEUROSCI.5906-11.2012
M3 - Article
C2 - 23015437
AN - SCOPUS:84866640565
SN - 0270-6474
VL - 32
SP - 13470
EP - 13487
JO - Journal of Neuroscience
JF - Journal of Neuroscience
IS - 39
ER -