Insular cortex and amygdala lesions differentially affect acquisition on inhibitory avoidance and conditioned taste aversion

doi:10.1016/0006-8993(91)90616-4

Brain Research

Volume 549, Issue 1, 17 May 1991, Pages 165-170

https://doi.org/10.1016/0006-8993(91)90616-4 Get rights and content

These experiments examined the effects of NMDA-induced lesions of the amygdala and insular (gustatory) cortex (IC) on inhibitory avoidance learning and conditioned taste aversion (CTA) in rats. IC lesions, but not amygdala lesions, disrupted CTA. In contrast, lesions of either brain region disrupted inhibitory avoidance learning. These findings support the view that the IC is strongly involved in the acquisition of external as well as visceral aversively motivated behavior. Despite extensive functional interconnections, these 2 brain regions appear to have different roles in mediating different forms of aversively based learning.

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The insular cortex (IC) has been linked to the processing of interoceptive and exteroceptive signals associated with addictive behavior. However, whether the IC modulates the acquisition of drug-related affective states by direct top-down connectivity with ventral tegmental area (VTA) dopamine neurons is unknown. We found that photostimulation of VTA terminals of the anterior insular cortex (aIC) induces rewarding contextual memory, modulates VTA activity, and triggers dopamine release within the VTA. Employing neuronal recordings and neurochemical and transsynaptic tagging techniques, we disclose the functional top-down organization tagging the aIC pre-synaptic neuronal bodies and identifying VTA recipient neurons. Furthermore, systemic administration of amphetamine altered the VTA excitability of neurons modulated by the aIC projection, where photoactivation enhances, whereas photoinhibition impairs, a contextual rewarding behavior. Our study reveals a key circuit involved in developing and retaining drug reward-related contextual memory, providing insight into the neurobiological basis of addictive behavior and helping develop therapeutic addiction strategies.
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Association between events in time and space is a major mechanism for all animals, including humans, which allows them to learn about the world and potentially change their behavior in the future to adapt to different environments. Conditioning taste aversion (CTA) is a single-trial learning paradigm where animals are trained to avoid a novel flavor which is associated with malaise. Many variables can be analyzed with this model and the circuits involved are well described. Thus, the amygdala and the gustatory cortex (GC) are some of the most relevant structures involved in CTA. In the present study we focused in plastic changes that occur during appetitive and/or aversive taste memory formation. Previous studies have demonstrated that memory consolidation, in hippocampal dependent paradigms, induces plastic changes like increase in the concentration of proteins considered as markers of neuronal plasticity, such as the growth associated protein 43 (GAP-43) and synaptophysin (SYN). In the present experiment in male rats we evaluated changes in GAP-43 and SYN expression, using immunofluorescence, induce by the formation of aversive and appetitive taste memory. We found that taste aversive memory formation can induce an increase in GAP-43 in the granular layer of the GC. Furthermore, we also found an increase in SYN expression in both layers of the GC, the basolateral amygdala (BLA) and the central amygdala (CeA). These results suggest that aversive memory representation induces a new circuitry (inferred from an increase in GAP 43). On the other hand, an appetitive taste learning increased SYN expression in the GC (both layers), the BLA and the CeA without any changes in GAP 43. Together these results indicate that aversive memory formation induces structural and synaptic changes, while appetitive memory formation induces synaptic changes; suggesting that aversive and appetitive memories require a different set of cortical and amygdala plastic changes.
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Citation Excerpt :
Therefore, we suggest that emulation of US amygdalar events is necessary to initiate the molecular pathways involved in modifications of the amygdala-insular network and the coactivation of NMDA and β-adrenergic receptors during the post-learning period facilitates the taste avoidance memory consolidation through protein synthesis-dependent mechanisms. Although unspecific modifications between the amygdala and different brain structures could be induced by our pharmacological manipulations, we focused on the response in the IC considering that taste aversion memory involves the functional integrity of this structure [42–46]; it is also possible that the communication of the amygdala-insular cortex had been modified affecting the trace of the taste in a way that an avoidance response is displayed in a second encounter. The amygdala has afferents to the IC [47,48] and receives feedback information from the insula [49].
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Insular cortex and amygdala lesions differentially affect acquisition on inhibitory avoidance and conditioned taste aversion

Physiol. Behav.

Brain Research

Brain Research

Physiol. Behav.

Pharm. Biochem. Behav.

Behav. Neur. Biol.

Brain Research

Brain Research

Behav. Biol.

Brain Research

Neuroscience

Behav. Brain Res.

Pharmacol. Biochem. Behav.

Brain Research

Brain Research

Exp. Neurol.

Differential effects of amygdaloid lesion on conditioned taste aversion learning by rats

Physiol. Behav.

The gustatory neocortex of the rat

Physiol. Psychol.

Involvement of the gustatory neocortex in the learning of taste aversion

Physiol. Behav.