Associative learning is indispensable to elaborate adaptive behaviour. Lateral thalamic nuclei connected to the amygdala are shown to be involved in fear learning. However, the neural mechanisms and elements that control the acquisition and recall of conditioned fear memory are remained unclear. Here we apply circuit-based optogenetic, in vivo electrophysiological and neuroanatomical tracing methods to dissect this network and investigate its contribution to associative fear behaviour. The majority of the thalamic cells retrogradely labelled from the lateral aymgdala and the neigbouring amygdalostriatal transition area (AStr) were located in the suprageniculate (SG) and the posterior intralaminar thalamic nuclei (PIL). Both thalamic cell groups co-express the calcium-binding protein calretinin (CR). Viral injection of SG/PIL in CR-Cre mice reveals strong axonal labelling in LA and AStr as well as in associative cortices, while the encompassed CR-negative auditory thalamic relay cells are strongly connected to the primary auditory cortex and only weakly to the amygdala. This pattern suggests that these two thalamic populations process distinct types of information regarding environmental (auditory/visual) cues. Applying bi-directional optogenetic control on axon terminals of CR thalamic cells in the amygdala, we find that the information carried by these cells mediates the formation, recall and extinction of fear memory. Furthermore, this route also encodes the contextual experience of the aversive situation. Finally, by performing in vivo extracellular recordings in freely behaving mice, we show that the activity of CR-positive thalamic cells correlates well with each stage of associative learning. Our findings demonstrate that the CR-expressing lateral thalamic cells connected to the amygdala are good candidates to mediate experience-dependent memory processes and thus, shape behavioural responses to the environment signals. FINANCIAL SUPPORT: KTIA_NAP_13-2-2015-0010.
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