Interactions of time of day and sleep with between-session habituation and extinction memory in young adult males

Abstract

Within-session habituation and extinction learning co-occur as do subsequent consolidation of habituation (i.e., between-session habituation) and extinction memory. We sought to determine if, as we predicted: (1) between-session habituation is greater across a night of sleep vs. a day awake; (2) time-of-day accounts for differences; (3) between-session habituation predicts consolidation of extinction memory; (4) sleep predicts between-session habituation and/or extinction memory. Participants (N=28) completed 4–5 sessions alternating between mornings and evenings over 3 successive days (2 nights) with session 1 in either the morning (N=13) or evening (N=15). Twelve participants underwent laboratory polysomnography. During 4 sessions, participants completed a loud-tone habituation protocol while skin-conductance response (SCR), blink-startle electromyography (EMG), heart-rate acceleration (HRA) and deceleration (HRD) were recorded. For sessions 1 and 2, between-session habituation of EMG, SCR and HRD was greater across sleep. SCR and HRD were generally lower in the morning. Between-session habituation of SCR for sessions 1 and 2 was positively related to intervening (first night) slow wave sleep. In the evening before night 2, participants also underwent fear conditioning and extinction learning phases of a second protocol. Extinction recall was tested the following morning. Extinction recall was predicted only by between-session habituation of SCR across the same night (second night) and by intervening REM. We conclude that: 1) sleep augments between-session habituation, as does morning testing; 2) extinction recall is predicted by concurrent between-session habituation; and 3) both phenomena may be influenced by sleep.

Effects of sleep on memory for conditioned fear and fear extinction.

“…And, because SCR at fear conditioning and extinction did not differ between groups (Figure 2A, B), a key role for intervening sleep in the observed generalization was suggested (Figure 2C, D). Subsequent studies replicated the finding of generalized extinction memory over a night of sleep (Pace-Schott et al, 2013; Pace-Schott et al, 2014). …”

“…In this regard, it is notable that sleep, following within-session habituation, appears to prevent between-session sensitization seen in the corresponding wake group in corrugator EMG (Pace-Schott et al, 2011; Pace-Schott, Verga, et al, 2012) or heart-rate decleration (Pace-Schott et al, 2014). …”

“…Notably, the design of this experiment controlled for time-of-day effects. In another experiment, between-session habituation to a loud-tone stimulus, as measured by orbicularis oculi EMG and SCR, was greater across a night of sleep than across a day of continual wakefulness (Pace-Schott et al, 2014). Notably, in this study, time-of-day alone could not account for these sleep effects and percent SWS in the intervening nocturnal sleep was again associated with the degree of between-session habituation.…”

“…Therefore it is not surprising that the complex neuroendocrine changes taking place across sleep, that include amygdala and vmPFC activation in REM as well as fluctuations in cortisol, norepinephrine and NMDA-receptor mediated LTP, should also promote consolidation of both fear and extinction memory. Similarly, sleep-dependent generalization of both fear conditioning (Kuriyama, Soshi, & Kim, 2010; Menz et al, 2013) and extinction learning (Pace-Schott et al, 2009; Pace-Schott et al, 2014; Pace-Schott, Verga, et al, 2012a) can also be explained by their shared substrates as emotional memory processes.…”

Emotional trait and memory associates of sleep timing and quality

“…Future analyses of larger samples using structural equation modeling and similar techniques may help disambiguate these factors. Ambulatory polysomnography on the night preceding Session 1 as well as between sessions would yield important additional predictors such as sleep stage percentages (Pace-Schott et al, 2014; Spoormaker et al, 2012) that are potentially more powerful than actigraphy measures.…”