Abstract
Postingestive signals are important for shaping appetitive and consummatory responses, but the brain mechanisms required to assimilate interoceptive events with those at the frontlines of ingestion (taste-guided) are poorly understood. Here, we investigated whether an insular cortex (IC) region, which receives viscerosensory input, including gustatory, is required to modify taste-elicited consummatory reactions in response to a real-time interoceptive change using a serial taste reactivity (TR) test where the rats’ oromotor and somatic reactions to intraoral infusions of sucrose were periodically assessed over 45 minutes following Lithium Chloride (LiCl) administration. Results showed that neurally-intact rats shifted from an ingestive repertoire to an aversive one as LiCl took effect. Overall, this hedonic shift was delayed in rats with bilateral neurotoxic IC lesions. Rats with greater neuronal loss in posterior gustatory IC displayed fewer aversive reactions to sucrose following this initial LiCl injection. We further assessed if the failure to integrate interoceptive feedback with ongoing taste-guided behavior impaired acquisition and/or expression of conditioned aversion and/or avoidance in these same rats. Although, as a group, LiCl-injected rats with IC lesions subsequently avoided the sugar in a 48-hour two-bottle test, their preference for sucrose was significantly greater than that of the LiCl-injected neurally-intact rats. Overall lesion size, as well as proportion of the posterior gustatory and/or anterior visceral IC were each associated with impaired avoidance. These findings reveal new roles for the posterior gustatory and anterior visceral IC cortices in multisensory integrative function.
Significance Statement
Adaptive eating and drinking behaviors require that the brain incorporates interoceptive state information into appropriate taste-guided appetitive and consummatory responses in real time and over the long term through learning. Here, we show for the first time that loss of function in a subregion of insular cortex that receives both general visceral and gustatory sensory inputs hinders rapid adjustments to consummatory behaviors in response to a negative interoceptive event. We further show that this primary integrative deficit precludes robust adaptive avoidance behavior that normally safeguards against enduring the same visceral consequences again. Collectively, the findings yield new insights into the neural organization of taste-interoceptive integration in insular cortex, which subserve key aspects of short- and long-term control of ingestive behavior.
Footnotes
The authors declare no conflicts of interest.
Funding was provided R01 DC009821 (awarded to ACS) from the National Institute of Deafness and Communications Disorders, Dornsife institutional start-up funds (to LAS), and a Dornsife Neuroscience program graduate research fellowship (to AJ).
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
