Interoceptive insular cortex participates in sensory processing of gastrointestinal malaise and associated behaviors

Abstract

The insular cortex plays a central role in the perception and regulation of bodily needs and emotions. Its modular arrangement, corresponding with different sensory modalities, denotes a complex organization, and reveals it to be a hub that is able to coordinate autonomic and behavioral responses to many types of stimuli. Yet, little is known about the dynamics of its electrical activity at the neuronal level. We recorded single neurons in behaving rats from the posterior insula cortex (pIC), a subdivision considered as a primary interoceptive cortex, during gastrointestinal (GI) malaise, a state akin to the emotion of disgust in humans. We found that a large proportion of pIC neurons were modulated during the rodent compensatory behaviors of lying on belly (LOB) and Pica. Furthermore, we demonstrated that LOB was correlated with low-frequency oscillations in the field potentials and spikes at the theta (8 Hz) band, and that low-frequency electrical microstimulation of pIC elicited LOB and Pica. These findings demonstrate that pIC neurons play a critical role in GI malaise perception, and that the pIC influences the expression of behaviors that alleviate GI malaise. Our model provides an accessible approach at the single cell level to study innate emotional behaviors, currently elusive in humans.

LiCl-induced sickness modulates spontaneous activity and response dynamics in rat gustatory cortex

“…The fact that neurons are embedded in networks, and that the states of such networks can be indexed in terms of EEG power (particularly in θ and µ frequency ranges [25,26,56], motivated our decision to characterize changes in LFP activity within GC as an animal shifts from a healthy state into one of emesis, and to then relate this shift to changes in the dynamics of taste coding. This analysis allows us to show that LiCl causes a modulation of µ power at approximately 15mins post-injection-a result consistent with human [69] and rat data [70]. In both the literature and our current data, the latency of these changes in µ are strongly correlated with the appearance of illness-related behaviors [70].…”

“…This analysis allows us to show that LiCl causes a modulation of µ power at approximately 15mins post-injection-a result consistent with human [69] and rat data [70]. In both the literature and our current data, the latency of these changes in µ are strongly correlated with the appearance of illness-related behaviors [70].…”

“…In both the literature and our current data, the latency of these changes in µ are strongly correlated with the appearance of illness-related behaviors [70]. We show that rearing durations, a measure of healthy exploratory behavior [2, 64, 65, 70-72], drop starting at approximately 12min post-LiCl injection. This finding is consistent with decades of work showing that poisoning-related behaviors, and specifically those brought on by systemic nausea, emerge (depending on dose) at roughly 10min post administration [2-4, 70].…”

“…We show that rearing durations, a measure of healthy exploratory behavior [2,64,65,[70][71][72], drop starting at approximately 12min post-LiCl injection. This finding is consistent with decades of work showing that poisoning-related behaviors, and specifically those brought on by systemic nausea, emerge (depending on dose) at roughly 10min post administration [2][3][4]70].…”

“…We show that rearing durations, a measure of healthy exploratory behavior [2,64,65,[70][71][72], drop starting at approximately 12min post-LiCl injection. This finding is consistent with decades of work showing that poisoning-related behaviors, and specifically those brought on by systemic nausea, emerge (depending on dose) at roughly 10min post administration [2][3][4]70]. In our hands, the emergence of this illness-induced behavioral change lags closely (~55sec) behind the change in GC µ power induced by the same LiCl dose, a fact that is all the more striking given that the neural and behavioral datasets were collected independently.…”