A new face of sleep: The impact of post-learning sleep on recognition memory for face-name associations

https://doi.org/10.1016/j.nlm.2015.10.012Get rights and content

Highlights

  • We tested whether sleep influences the accuracy of remembering face-name associations.

  • Presentation and recall were 12 h apart, one time with 8 h sleep and once without.

  • More correct face-name pairs were recalled when there was a sleep opportunity.

  • Sleep duration or sleep stage was not associated with improvement between conditions.

Abstract

Sleep has been demonstrated to improve consolidation of many types of new memories. However, few prior studies have examined how sleep impacts learning of face-name associations. The recognition of a new face along with the associated name is an important human cognitive skill. Here we investigated whether post-presentation sleep impacts recognition memory of new face-name associations in healthy adults.

Fourteen participants were tested twice. Each time, they were presented 20 photos of faces with a corresponding name. Twelve hours later, they were shown each face twice, once with the correct and once with an incorrect name, and asked if each face-name combination was correct and to rate their confidence. In one condition the 12-h interval between presentation and recall included an 8-h nighttime sleep opportunity (“Sleep”), while in the other condition they remained awake (“Wake”).

There were more correct and highly confident correct responses when the interval between presentation and recall included a sleep opportunity, although improvement between the “Wake” and “Sleep” conditions was not related to duration of sleep or any sleep stage.

These data suggest that a nighttime sleep opportunity improves the ability to correctly recognize face-name associations. Further studies investigating the mechanism of this improvement are important, as this finding has implications for individuals with sleep disturbances and/or memory impairments.

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

References (53)

  • U. Wagner et al.

    The impact of post-learning sleep vs. wakefulness on recognition memory for faces with different facial expressions

    Neurobiology of Learning and Memory

    (2007)
  • L. Wang et al.

    Intrinsic connectivity between the hippocampus and posteromedial cortex predicts memory performance in cognitively intact older individuals

    Neuroimage

    (2010)
  • S. Ackermann et al.

    Differential effects of non-REM and REM sleep on memory consolidation?

    Current Neurology and Neuroscience Reports

    (2014)
  • D. Aeschbach et al.

    A role for non-rapid-eye-movement sleep homeostasis in perceptual learning

    Journal of Neuroscience

    (2008)
  • T. Allison et al.

    Face recognition in human extrastriate cortex

    Journal of Neurophysiology

    (1994)
  • T.R. Barrett et al.

    Effect of sleep on memory: III. Controlling for time-of-day effects

    Journal of Experimental Psychology

    (1972)
  • K. Benson et al.

    The beneficial effect of sleep in an extended Jenkins and Dallenbach paradigm

    Psychophysiology

    (1977)
  • J.R. Cooke et al.

    Sustained use of CPAP slows deterioration of cognition, sleep, and mood in patients with Alzheimer’s disease and obstructive sleep apnea: A preliminary study

    Journal of Clinical Sleep Medicine

    (2009)
  • S. Diekelmann

    Sleep for cognitive enhancement

    Frontiers in Systems Neuroscience

    (2014)
  • S. Drosopoulos et al.

    Sleep’s function in the spontaneous recovery and consolidation of memories

    Journal of Experimental Psychology

    (2007)
  • S. Drosopoulos et al.

    Sleep enhances explicit recollection in recognition memory

    Learning & Memory

    (2005)
  • S. Folkard et al.

    Circadian rhythms in human memory

    British Journal of Psychology

    (1980)
  • M.J. Fowler et al.

    Sleep and memory

    Science

    (1973)
  • S. Gais et al.

    Sleep transforms the cerebral trace of declarative memories

    Proceedings of the National academy of Sciences of the United States of America

    (2007)
  • S. Gais et al.

    Sleep after learning aids memory recall

    Learning & Memory

    (2006)
  • S. Gais et al.

    Learning-dependent increases in sleep spindle density

    Journal of Neuroscience

    (2002)
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