Fear memory in humans is consolidated over time independent of sleep

Abstract

Background: Many pathological fear memories rely on processes of fear conditioning upon an aversive event. These fear memories may continue to change after acquisition, but the factors contributing to these changes are not well understood. Sleep is known to consolidate, strengthen and change newly acquired declarative and procedural memories. However, evidence on the role of time and sleep in the consolidation of fear memories is inconclusive. Here, we used highly sensitive electrophysiological measures to examine the development of fear-conditioned responses over time and sleep in humans. Methods: We assessed event-related brain potentials (ERP) in 18 healthy young individuals during fear conditioning before and after a 2-hour afternoon nap or a corresponding wake interval in a counterbalanced within-subject design. The procedure involved pairing a neutral tone (CS+) with a highly unpleasant sound (US). As a control, another neutral tone (CS-) was paired with a neutral sound. Fear responses were examined before the interval during a habituation phase and an acquisition phase as well as after the interval during an extinction phase and a re-acquisition phase. Results: Differential fear conditioning during acquisition was evidenced by a more negative slow ERP component preceding the CS+ compared to the CS- (stimulus-preceding negativity). This differential fear response was even stronger after the interval during re-acquisition compared to initial acquisition, but this effect was similarly pronounced after sleep and wakefulness. Conclusions: These findings suggest that fear memories are consolidated over time, with this effect being independent of intervening sleep.

Negative attributes of mixed-valence memories strengthen over long retention intervals and the degree of enhancement is predicted by individual differences in state anxiety.

“…It has previously been reported that under certain conditions, aversive memories can strengthen over long retention intervals or during extinction (i.e., nonreinforced exposure to a CS) in both human and laboratory animals (Pavlov et al, 2023;Pickens et al, 2009;Poulos et al, 2016), and this learned fear "incubation" has been hypothesized to contribute to some posttraumatic stress responses (Careaga et al, 2016;Eysenck, 1968). Relatedly, "negativity bias" (in which an individual over-values negative outcomes relative to positive outcomes; Kahneman & Tversky, 1984) results from asymmetries in the activation in memory of positive and negative valence outcomes (Norris, 2021), and it has been observed that the representation of negative outcomes tend to be more stable and recede at a slower rate than positive outcomes (Norris et al, 2010).…”