Abstract

Changes in neuronal connectivity occurring upon the formation of aversive memory were examined in C57BL/6 (C57) mice 24 h after they were trained for tone fear conditioning (TFC) and contextual fear conditioning (CFC). Although TFC and CFC are amenable to distinct learning systems each involving a specific neural substrate, we found that mice trained in the two protocols showed the same increase in spine density and spine size in class I basolateral amygdala (BLA) and in dorsal hippocampus CA1 pyramidal neurons. Our findings suggest that, because of their remarkably functional hippocampus, C57 mice might engage this region in any fear situation they face. These observations raise a point relevant to aversive memory studies, i.e., how the peculiarity of memory in certain individuals impacts on the components of the fear circuitry. It is suggested that enhanced connectivity in brain regions dispensable for specific forms of learning could considerably increase the resistance of aversive memory traces to treatments aimed at disrupting them.

Highlights

  • Fear conditioning (FC), the most common model of aversive memory in rodents, is rapidly induced and persists over a considerable period of time

  • tone fear conditioning (TFC) and contextual fear conditioning (CFC) are amenable to distinct learning systems each involving a specific neural substrate, we found that mice trained in the two protocols showed the same increase in spine density and spine size in class I basolateral amygdala (BLA) and in dorsal hippocampus CA1 pyramidal neurons

  • Studies aimed at dissecting the neural basis of FC have identified a role for the basolateral amygdala (BLA) in the formation of tone and contextual fear conditioning (CFC; Phillips and LeDoux, 1994) or the latter, a role for the hippocampus, which is required for implementing the contextual representation acting as a conditioned stimulus (CS) (Maren et al, 1998; Anagnostaras et al, 1999)

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Summary

Introduction

Fear conditioning (FC), the most common model of aversive memory in rodents, is rapidly induced and persists over a considerable period of time. Studies aimed at dissecting the neural basis of FC have identified a role for the basolateral amygdala (BLA) in the formation of tone and contextual fear conditioning (CFC; Phillips and LeDoux, 1994) or the latter, a role for the hippocampus, which is required for implementing the contextual representation acting as a CS (Maren et al, 1998; Anagnostaras et al, 1999) This has led to consider the two paradigms as amenable to distinct learning systems: (i) an elemental associative learning system involving the BLA but independent from the hippocampus (Phillips and LeDoux, 1992; Paré et al, 2004) and (ii) a contextual associative learning system involving by both regions (Selden et al, 1991; Phillips and LeDoux, 1992). This dichotomy, is challenged by data showing that manipulation of hippocampal cholinergic activity modulates tone fear conditioning (TFC) and CFC performance in opposite ways, pointing to hippocampal control of amygdala function in both tasks (Desmedt et al, 1998; Calandreau et al, 2006)

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