A new face of sleep: The impact of post-learning sleep on recognition memory for face-name associations
Introduction
Remembering the name of someone we have recently met is a task that is encountered regularly (Allison et al., 1994, Farah, 1996). However, remembering the correct name that is associated with a face is more difficult, especially when it has been learned recently. Findings from a functional magnetic resonance imaging (fMRI) study suggest that successful encoding of face-name pairs requires the coordination of neural activity in hippocampal, prefrontal, and parietal regions (Miller et al., 2008) and that a stronger connectivity between the hippocampal and posteromedial regions during rest predicts better performance on a face-name task (Wang et al., 2010).
While the benefit of sleep after learning is established (for review see Ackermann and Rasch, 2014, Diekelmann, 2014, Genzel et al., 2014, Inostroza and Born, 2013, Prince and Abel, 2013, Stickgold and Walker, 2007, Tononi and Cirelli, 2014) it has been suggested that sleep preferentially enhances the types of memory that rely on the hippocampus (Maquet, 2001, Marshall and Born, 2007), and that the positive effect of sleep on declarative memory stems from an active role of sleep in memory consolidation (Drosopoulos et al., 2007, Inostroza and Born, 2013, Schönauer et al., 2014, Tononi and Cirelli, 2014), rather than from reduced interference (Talamini, Nieuwenhuis, Takashima, & Jensen, 2008).
The strength of sleep dependent memory consolidation can be mediated by the “macrostructure”, the amount of time spent in a specific sleep stage (Aeschbach et al., 2008, Gais et al., 2000, Huber et al., 2004, Wagner et al., 2007), as well as by the “microstructure”, which refers to sleep related mechanisms like sleep spindles and synaptic plasticity (Gais et al., 2002, Inostroza and Born, 2013, Schönauer et al., 2014, Tononi and Cirelli, 2014). Recent studies using hippocampal-dependent episodic associative memory-encoding tasks such as the contextual learning paradigm (van der Helm, Gujar, Nishida, & Walker, 2011) and the face-name task (Mander, Santhanam, Saletin, & Walker, 2011) found that performance correlates positively with stage-2 NREM sleep from a nap. Those same studies have also found that fast spindles associate with successful encoding (Mander et al., 2011, Mander et al., 2014, van der Helm et al., 2011).
However, the effects of sleep macrostructure in associative recognition tasks are not consistent. Two studies using word-based recognition tasks found that sleep early in the night enhanced recognition memory (Drosopoulos, Wagner, & Born, 2005), especially if that interval was rich in SWS (Daurat, Terrier, Foret, & Tiberge, 2007). In contrast, a nap study by Schönauer et al. (2014) found that while subjects performed significantly better in the nap condition (two hours of sleep in the morning or afternoon) than in the wake condition in an associative recognition task for phone numbers and names, the time spent in specific sleep stages did not correlate with memory performance.
The duration of sleep required for memory enhancement has also been investigated. Enhancement of declarative memory has been observed after an 8-h overnight sleep opportunity (Benson and Feinberg, 1977, Drosopoulos et al., 2007, Gais et al., 2006, Gais et al., 2007), as well as after the first half of nocturnal sleep (Barrett and Ekstrand, 1972, Fowler et al., 1973, Plihal and Born, 1997, Yaroush et al., 1971) and after shorter 1–2 h naps in the afternoon (Gorfine et al., 2007, Tucker and Fishbein, 2008). However, the optimal amount of sleep needed to benefit memory is unclear, and comparing results from different studies is complicated by the fact that retention intervals (between presentation and recall) of equal length but containing different amounts of sleep will contain different amounts of wakefulness, which itself may influence memory. Two main ideas for how memory consolidation might be affected by the duration of sleep have been suggested: a minimum duration of sleep that improves memory in an “all-or-none” way, with longer sleep durations producing no additional enhancement; or a dose-dependent impact of sleep duration on memory consolidation, where more sleep produces a greater benefit (Diekelmann, Wilhelm, & Born, 2009). In the case of recognition memory, there is evidence to support both hypotheses (Daurat et al., 2007, Drosopoulos et al., 2005, Hu et al., 2006, Wagner et al., 2007). Furthermore, one experiment even found that recognition performance was not better for a sleep group than for a sleep deprivation group, suggesting that the effect of sleep on recognition memory may be partially due to interactions between sleep and circadian rhythmicity (Nesca & Koulack, 1994).
These studies have demonstrated that sleep can improve associative recognition memory but do not answer the question as to whether sleep dependent memory consolidation for face-name pairs is mediated by the duration of sleep or the amount of time spent in a specific sleep stage during typical sleep at night. We designed the present study to explore the role of a full night of sleep on recognition memory for face-name associations. We aimed to determine whether sleep improves memory consolidation resulting in more correct face-name recognitions after sleep than after a similar interval of wakefulness, and to determine if there is an association between the duration of sleep or any sleep stage and improvement in the number of correct face-name recognitions (compared with the waking condition).
Section snippets
Participants and screening. Main study
Data were obtained from fourteen healthy participants (six male, eight female; age range 21–28 years; mean age = 23.33). Each participant underwent an extensive screening procedure to ensure they were free from any medical or psychological disorders. The evaluation included biochemical tests on blood and urine, an electrocardiogram, a physical examination, psychological questionnaires (Beck Depression Inventory, MMPI-2), and an interview with a clinical psychologist. Only those participants who
Main study
The average number of correct responses was significantly greater after a 12-h interval between presentation and recognition that included sleep than after a similar interval that consisted of all wake, and this was true for all correct responses (Sleep = 34.14 ± 3.34; Wake = 31.57 ± 4.18; t(13) = 3.8, p = 0.002) as well as for the subset of responses where the participant rated their response as highly confident (Sleep = 27.36 ± 8.0; Wake = 24.57 ± 6.44; t(13) = 2.48, p = 0.028; see Table 1). An interval between
Discussion
The present study investigated the impact of post-learning sleep on recognition memory for face-name associations. In the main study we tested every subject twice, once with an eight-hour nocturnal opportunity to sleep in the 12-h interval between presentation and recognition and once when the 12-h interval between presentation and recognition occurred during the regular waking day. We found that recognition memory for face-name associations was enhanced when sleep occurred between presentation
Acknowledgments
We wish to thank the study participants; Ms. K. Ward for assistance with subject recruitment and data processing; the staff of the BWH CCI for assistance with carrying out the studies; Drs. R.A. Sperling, S.W. Cain, and M. Pomplun for advice and assistance in developing and implementing the face-name task in our laboratory. Many of the photographs in the Face-Name Task were used with permission from the Center for Vital Longevity Face Database at the University of Michigan. Support for the
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