Prior fear learning enables the rapid assimilation of new fear memories directly into cortical networks

Abstract

Long-term memory formation involves the reorganization of brain circuits, termed system consolidation. Whether and how a prior fear experience influences system consolidation of new memories is poorly understood. In rats, we found that prior auditory fear learning allows the secondary auditory cortex to immediately encode new auditory memories, with these new memories purely requiring the activation of cellular mechanisms of synaptic consolidation within secondary auditory cortex. Similar results were obtained in the anterior cingulate cortex for contextual fear memories. Moreover, prior learning enabled connections from these cortices to the basolateral amygdala (BLA) to support recent memory retention. We propose that the reorganization of circuits that characterizes system consolidation occurs only in the first instance that an event is learned, subsequently allowing the immediate assimilation of new analogous events in final storage sites.

Potentiated cholinergic and corticofugal inputs support reorganized sensory processing in the basolateral amygdala during auditory threat acquisition and retrieval

“…Despite the symmetry in the native functional connectivity between HO-AC and BLA, only the CAmy projection neurons and descending functional coupling assays exhibited discriminative plasticity. The asymmetric potentiation in CAmy influence on BLA ensembles reinforces inactivation studies showing the necessary involvement HO-AC CAmy projections in the recall of short-term threat memory with complex sounds (Dalmay et al, 2019), in the recall of remote auditory threat memories (Cambiaghi et al, 2016), and in the re-acquisition of additional auditory threat associations (Concina et al, 2022). Future work is needed to address whether the asymmetric CS+ response potentiation in the CAmy neurons is distinct from other projection neuron types across the cortical column.…”

“…These findings can be explained by a dual-stream model, which purports that the auditory thalamus and cortex feature intermingled functional populations of highly plastic neurons that reflect the learned significance of environmental sounds (e.g., CAmy projection neurons) alongside other populations that are optimized for stability to encode environmental stimuli based on their physical features and overall novelty independent of fear associations (Gründemann, 2021; Leppla et al, 2022). Alternatively, unidentified regular- and fast-spiking units that on average did not exhibit discriminative enhancement of the CS could nevertheless encode associative threat memory at more remote time point than the next-day Recall session used here (Cambiaghi et al, 2016; Concina et al, 2022; Yang et al, 2016). A third possibility is that most HO-AC neurons do encode the discriminative threat memory at the time scale studied here, but the representation of the memory is not based in overall changes in firing rate but instead in the stability of neurons that are functionally connected into CS+ and CS− ensembles (Dalmay et al, 2019; Grewe et al, 2017; Taylor et al, 2021; Wood et al, 2022).…”