Functional mapping of gustatory neurons in the insular cortex revealed by pERK-immunohistochemistry and in vivo optical imaging.

Neural plasticity in the gustatory area of the insular cortex (IC) plays a critical role in detecting novel taste and taste memory formation, which require extracellular signal-regulated kinase 1-2 (ERK1-2) phosphorylation. However, the distribution patterns of phosphorylated ERK1-2 (pERK) responses to gustatory stimulation remain unknown. This study examined distribution patterns of gustatory stimulation-driven pERK expression in the IC of anesthetized and alert rats. In both pentobarbital-anesthetized and alert rats, gustatory stimulation (10% sucrose) induced pERK-like immunoreactivity in pyramidal cells of all IC subdivisions: agranular (AI), dysgranular (DI), and granular IC (GI). Alert naïve rats exhibited approximately 10-fold larger number of pERK-like immunopositive (pERK-LI) cells than anesthetized naïve rats in response to sucrose application. Most pERK-LI cells were located in layers II/III but not deeper layers and almost no parvalbumin/somatostatin-immunopositive cells expressed pERK. In the AI, rostral regions exhibited more pERK-LI cells than caudal regions, whereas most pERK-LI cells existed in the DI/GI around the intersection of the rhinal fissure and middle cerebral artery (MCA), where in vivo optical imaging revealed activation during sucrose application in addition to the ventral primary and secondary somatosensory cortices. Gustatory experience affected the number of pERK-LI cells in the IC: sucrose stimulation induced more pERK-LI cells in the DI/GI of alert naïve rats than sucrose-exposed rats, which had received sucrose solution for 1 week. These results suggest that pyramidal cells in the upper layers of the gustatory region are highly susceptible to ERK1-2 phosphorylation by gustatory stimulation, which may induce neuroplastic changes in the IC.