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 whether, as we predicted: (1) between-session habituation is greater across a night of sleep versus 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 and heart-rate 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.

Figure 1

Experimental protocol. In both groups participants completed one-hour sessions, 12 hours apart, alternating between approximately 8–9 AM and 8–9 PM, over the course of 3 successive days and 2 nights. The APAPA group had the first of 5 sessions in the morning of the first day and the PAPA group had the first of 4 sessions in the evening of that day. Both groups had their last session on the morning of the third day. All participants completed the loud-tone protocol at their first 4 sessions and the fear conditioning and extinction protocol across the second night of the study.

Figure 2

Comparison of baseline values of EMG, SCL and HR between groups. A. First Session-Pair Analyses of baseline SCL showing a significantly greater SCL in the first (PM) vs. second (AM) session of the PAPA group (N=12 APAPA, 14 PAPA). B. First Session-Pair Analyses of baseline HR showing significantly greater HR in the second (PM) vs. first (AM) session of the APAPA group (N=12 APAPA, 14 PAPA). C. Analyses by Time-of-Day of HR showing significantly greater HR in the PM vs. AM collapsing across Group (N=19). SCL: skin conductance level, μS: microSiemens, BPM: beats per minute. * p < .05. Error bars depict standard error of the mean.

Figure 3

Comparisons of blink-startle response (orbicularis oculi EMG) to loud tones across sessions and between times-of-day. A. First Session-Pair Analyses of EMG Mean Response percentage change from session 1 to session 2 showing a significant difference between PAPA (PM to AM) and APAPA (AM to PM) groups (N=11 APAPA, 15 PAPA). B. First Session-Pair Analyses of EMG Relative Habituation showing significantly greater intra-session habituation (more negative correlation coefficient) in the second (AM) compared to first (PM) session of the APAPA group (N=11 APAPA, 15 PAPA). C. Analyses by Session-Order for Change Across Session Pairs across 2 PM to AM sessions in the PAPA group compared to 2 AM to PM changes in the APAPA group (p < .05 for Group x Session Pair interaction) (N=7 APAPA, 11 PAPA). D. Time-of-day analysis collapsing across groups showing lack of a Time-of-Day (AM vs. PM) main effect (N=18). EMG μV^1/2 (or EMG^1/2) square-root transformed electromyographic response in microVolts, * p < .05, ** p < .01, Error bars depict standard error of the mean.

Figure 4

Comparisons of SCR to loud tones across sessions and between times-of-day. A. First Session-Pair Analyses showing significantly lower SCR Mean Response in the second (AM) vs. first (PM) session of the PAPA group (N=13 APAPA, 15 PAPA). B. Analyses by Session-Order for Change Across Session Pairs across 2 PM to AM sessions in the PAPA group compared to 2 AM to PM changes in the APAPA group. There were significantly greater decreases across both PM to AM sessions combined in the PAPA group than across both AM to PM changes combined in the APAPA group (N=9 APAPA, 10 PAPA). C. Analyses by Time-of-Day collapsing across groups showing significantly greater SCR to the loud tones in the PM compared to AM (N=21). SCR μS^1/2: square-root transformed skin conductance response in microSiemens, * p < .05, Error bars depict standard error of the mean.

Figure 5

Comparisons of HRD to loud tones across sessions and between times-of-day. A. First Session-Pair Analyses showing significantly greater HRD Mean Response at the second (PM) compared to the first (AM) session in the APAPA group (N=13 APAPA, 15 PAPA). B. Analyses by Session-Order for Change Across Session Pairs across 2 PM to AM sessions in the PAPA group compared to 2 AM to PM changes in the APAPA group. There were significantly greater decreases across both PM to AM sessions combined in the PAPA group than across both AM to PM changes combined in the APAPA group (N=10 APAPA, 11 PAPA). C. Analyses by Time-of-Day collapsing across groups showing significantly greater HRD to the loud tones in the PM compared to AM (N=21). HRD BPM^1/2: square-root transformed heart rate deceleration in beats-per-minute, * p < .05, Error bars depict standard error of the mean.

Figure 6

Differential skin conductance response to the extinguished (CS+E) and unextinguished conditioned stimuli at the extinction recall phase occurring in the morning of Day 3 (N=12 APAPA, 13 PAPA). Neither a main effect of CS+ type nor a CS+ type x Trial interaction was noted indicating generalization of extinction memory from the CS+E to the CS+U. SCR^1/2, differential skin conductance response in microsiemens.