Danger Changes the Way the Brain Consolidates Neutral Information; and Does So by Interacting with Processes Involved in the Encoding of That Information

Abstract

This study examined the effect of danger on consolidation of neutral information in two regions of the rat (male and female) medial temporal lobe: the perirhinal cortex (PRh) and basolateral amygdala complex (BLA). The neutral information was the association that forms between an auditory stimulus and a visual stimulus (labelled S2 and S1) across their pairings in sensory preconditioning. We show that, when the sensory preconditioning session is followed by a shocked context exposure, the danger shifts consolidation of the S2-S1 association from the PRh to the BLA; and does so by interacting with processes involved in encoding of the S2-S1 pairings. Specifically, we show that the initial S2-S1 pairing in sensory preconditioning is encoded in the BLA and not the PRh; whereas the later S2-S1 pairings are encoded in the PRh and not the BLA. When the sensory preconditioning session is followed by a context alone exposure, the BLA-dependent trace of the early S2-S1 pairings decays and the PRh-dependent trace of the later S2-S1 pairings is consolidated in memory. However, when the sensory preconditioning session is followed by a shocked context exposure, the PRh-dependent trace of the later S2-S1 pairings is suppressed and the BLA-dependent trace of the initial S2-S1 pairing is consolidated in memory. These findings are discussed with respect to mutually inhibitory interactions between the PRh and BLA, and the way that these regions support memory in other protocols, including recognition memory in people.Significance Statement:The perirhinal cortex (PRh) and basolateral amygdala complex (BLA) process the pairings of neutral auditory and visual stimuli in sensory preconditioning. The involvement of each region in this processing is determined by the novelty/familiarity of the stimuli as well as events that occur immediately after the preconditioning session. Novel stimuli are represented in the BLA; however, as these stimuli are repeatedly presented without consequence, they come to be represented in the PRh. Whether the BLA- or PRh-dependent representation is consolidated in memory depends on what happens next. When nothing of significance occurs, the PRh-dependent representation is consolidated and the BLA-dependent representation decays; but when danger is encountered, the PRh-dependent representation is inhibited and the BLA-dependent representation is selected for consolidation.

Integration of sensory and fear memories in the rat medial temporal lobe: advancing research by Wong et al. (2019)

“…Specifically, we will examine whether communication between the PRh and BLA is required for chaining of the sound-light and light-shock memories under circumstances where the sound-light memory was not encoded in the PRh: e.g., after just one sound-light pairing in stage 1 (Qureshi et al, 2023), or when the sound-light pairings are administered in a dangerous context (Holmes et al, 2013(Holmes et al, , 2018. We will also examine whether integration always occurs through chaining after many sound-light pairings, or whether there are manipulations that can restore the potential for mediated learning (e.g., manipulations that restore the relative novelty of the sound and light in stage 2, such as the lapse of time).…”

“…This conclusion was based on a series of experiments which examined the involvement of the perirhinal cortex (PRh) in stage 3 2 of the protocol described above. The PRh was selected as the region of interest as it encodes the sound-light memory that forms in stage 1 (Holmes et al, 2013(Holmes et al, , 2018Qureshi et al, 2023) but plays no role in formation of the directly conditioned light-shock memory in stage 2 (Bang & Brown, 2009;Campeau & Davis, 1995;Kholodar-Smith et al, 2008;Lindquist et al, 2004;Romanski & LeDoux, 1992;Wilensky et al, 2006). Indeed, Wong et al confirmed past findings that neuronal activity in the PRh is not needed for acquisition of directly conditioned fear to the light.…”