Bilateral lesions in a specific subregion of posterior insular cortex impair conditioned taste aversion expression in rats

Abstract

Gustatory cortex (GC) is widely regarded for its integral role in the acquisition and retention of conditioned taste aversions (CTAs) in rodents, but large lesions in this area do not always result in CTA impairment. Recently, using a new lesion mapping system, we found severe CTA expression deficits were associated with damage to a critical zone that included the posterior half of GC in addition to the insular cortex (IC) that is just dorsal and caudal to this region (visceral cortex). Importantly, lesions in anterior GC were without effect. Here, neurotoxic-induced bilateral lesions were placed in the anterior half of this critical damage zone, at the confluence of the posterior GC and the anterior visceral cortex (termed IC2), the posterior half of this critical damage zone that contains just VC (termed IC3), or both of these subregions (IC2+IC3). Then, pre- and post-surgically acquired CTAs (to 0.1M NaCl and 0.1M sucrose, respectively) were assessed postsurgically in 15-min single-bottle and 96-h two-bottle tests. Li-injected rats with histologically-confirmed bilateral lesions in IC2 exhibited the most severe CTA deficits, while those with bilateral lesions in IC3 were relatively normal, exhibiting transient disruptions in the single-bottle sessions. Group-wise lesion maps showed CTA-impaired rats had more extensive damage to IC2 than did unimpaired rats. Some individual differences in CTA expression among individual rats with similar lesion profiles were observed, suggesting idiosyncrasies in the topographical representation of information in IC. Nevertheless, this study implicates IC2 as the critical zone of IC for normal CTA expression.

Nicotine pre-treatment reduces sensitivity to the interoceptive stimulus effects of commonly abused drugs as assessed with taste conditioning paradigms

“…Lesioning of the anterior IC, a structure heavily implicated in integration of interoceptive cues of stimuli, particularly drugs of abuse (Naqvi and Bechara, 2010) results in interference with the acquisition of CTA induced by drugs of abuse, but not LiCl, remarkably similar to the results observed here (Geddes et al, 2008; Mackey et al, 1986; Zito et al, 1988). Acquisition of LiCl-induced CTA is dependent on relatively more caudal areas of the IC (Schier et al, 2016; Schier et al, 2014). Nicotine administered to the anterior IC increases GABAergic tone and ultimately results in a depression of synaptic potentiation (Sato et al, 2017), primarily at layer 5-pyramidal neurons, the primary excitatory output of the IC.…”

The role of the gustatory cortex in incidental experience-evoked enhancement of later taste learning

“…Our data reveal that innocuous taste experience specifically affects processing of the association between taste and malaise in gustatory cortex (GC on the processing of a new taste (sucrose, see below) or nausea alone. We also found no significant differences in the expression of c-Fos across the anterior to posterior axis of the structure, suggesting that, while distinct sub-divisions of GC may contribute differently to CTA memory itself (Schier et al 2016), TPE affects learning-related activity uniformly across the entirety of GC.…”

Experience-dependent c-Fos expression in the primary chemosensory cortices of the rat

“…However, gustatory cortex is multisensory, responding to tactile, temperature, auditory, and odor stimuli (Samuelsen et al, 2012, 2013; Samuelsen and Fontanini, 2017; Stapleton et al, 2006; Verhagen et al, 2004) suggesting it to be the first region capable of integrating taste and odor signals (Small, 2012). Research has shown that gustatory cortex mediates taste and odor experience-dependent behaviors, including conditioned taste aversion (Roman and Reilly, 2007; Schier et al, 2016), taste-potentiated odor aversion (Lin et al, 2009a), taste neophobia (Koh et al, 2003; Lin et al, 2012, 2009b) and odor-taste associations (Schul et al, 1996). Here, we add to these works showing experience-dependent differences in gustatory cortex to taste, odor and odor-taste stimuli.…”