ReviewThe function of the sleep spindle: A physiological index of intelligence and a mechanism for sleep-dependent memory consolidation
Research highlights
▶ Spindles may be a physiological index of fluid and crystallized intelligence. ▶ Learning-dependent changes in spindles may reflect memory consolidation processes. ▶ Spindles are involved in hippocampal–neocortical dialogue and synaptic plasticity.
Introduction
What mechanisms are involved in the process of consolidating newly learned information into a more stable form of long-term memory? Sleep has been identified as one of the biological states necessary for efficient memory consolidation; the process of transforming a newly acquired, labile memory into an enduring long-term memory. A compelling body of research exists from both human (Smith, 1985, Smith, 1995, Stickgold and Walker, 2007) and animal studies (Hennevin et al., 1995, Smith, 2003) establishing a link between rapid eye movement (REM) sleep and memory. Despite this, an ongoing (and sometimes heated) debate continues about the many functions of sleep (Brawn et al., 2010, Maquet, 2001, Rickard et al., 2008, Siegel, 2001, Stickgold and Walker, 2005, Vertes and Siegel, 2005).
More recently, non-REM sleep has been implicated in the consolidation of new learning as well (Buzsáki, 1984, Buzsáki, 1989, Gais and Born, 2004, Nader and Smith, 2003, Smith and MacNeill, 1994). Here we summarize recent evidence which suggests that the sleep spindle – an electroencephalographic (EEG) event that characterizes and predominates non-REM sleep – reflects, at the electrophysiological level, a mechanism involved in the consolidation of memory during sleep. Moreover, it appears that native sleep spindles reflect intellectual ability as measured by aptitude batteries including intelligence quotient (IQ) tests, and may serve as a physiological index of intelligence. We propose that baseline inter-individual differences in sleep spindles are correlated with learning potential. On the other hand, we suggest that learning-related increases in sleep spindles reflect processes specific to memory consolidation and may involve different neural substrates. Furthermore, we suggest that important dissociations between sleep states and memory systems have been identified in humans (Fogel et al., 2007b, Plihal and Born, 1997). For example, REM sleep appears to be involved in procedural learning that is cognitively complex and involves the acquisition of new rules (Fogel et al., 2007b, Plihal and Born, 1997, Smith et al., 2004b), whereas Stage 2 sleep is involved in procedural learning that involves the refinement of existing skills (Fogel et al., 2007b). Recent findings in animals suggest learning-related increases in sleep spindles may indicate one step in a series of sequential steps of sleep-dependent memory consolidation processes during non-REM sleep that follow previously identified learning-related changes in REM sleep (originally suggested by Buzsáki, 1984, Buzsáki, 1989; for review see Smith, 1985; and for more recent findings Fogel et al., 2009). Before describing evidence implicating sleep spindles in memory consolidation and their relation to IQ, it is necessary to describe the memory systems and memory processes involved (Section 2), followed by a brief overview of sleep–wake states (Section 3) and factors related to sleep spindles (Section 4). This is not intended to be a comprehensive review of memory systems, nor sleep–wake states, but should provide adequate background for the reader to understand the role of the sleep spindle in intellectual ability (Section 5) and memory consolidation (Sections 6 Sleep spindles and procedural memory, 7 Learning-dependent changes in sleep spindles in the rat, 8 Sleep spindles and declarative memory, 9 Learning-dependent changes in sleep spindles during a daytime nap). Finally, we provide important future directions (Section 10) which we hope will lead us to a better understanding of the processes involved in sleep-related synaptic plasticity and memory consolidation.
Section snippets
Declarative memory
Human long-term memory is not dependent on a unitary system of brain structures and mechanisms and can be subdivided into a number of subtypes. Declarative memory has traditionally been subdivided into episodic and semantic memory. The paired associates task is one task commonly used to study declarative learning that is explicitly learned. In this task, pairs of words (or pictures) are visually presented, where the goal is to explicitly memorize the word pairs by either rehearsal, or some
Sleep–wake states
Over the course of a night, sleep varies in terms of brain activity and behavior in a regular cyclic pattern (Carskadon and Dement, 2000). In young adults, the first half of the night is composed of primarily non-REM sleep including Stage 2, Stages 3 and 4 (comprising slow wave sleep; SWS), but little REM sleep. The last half of the night is composed almost entirely of Stage 2 and REM sleep whereby the periods of REM sleep lengthen as the night progresses, while SWS is either minimal or absent.
Factors related to sleep spindles
A number of factors relate to the temporal and spatial variability in spindles including: scalp location (Jobert et al., 1992, Werth et al., 1997a, Werth et al., 1997b, Zeitlhofer et al., 1997), endogenous generators (Anderer et al., 2001, Merica, 2000), menstrual cycle (Driver, 1996, Driver et al., 1996, Huupponen et al., 2002, Ishizuka et al., 1994), age (Huupponen et al., 2002, Landolt and Borbély, 2001, Landolt et al., 1996, Nicolas et al., 2001) and sleep cycle (De Gennaro et al., 2005,
Sleep spindles and intellectual ability
The density of sleep spindles is very consistent for any individual from night-to-night (De Gennaro et al., 2005, Gaillard and Blois, 1981, Silverstein and Levy, 1976). It has been remarked that inter-individual characteristics in sleep spindles are reliable enough to serve as an “electrophysiological fingerprint” (De Gennaro et al., 2005). However, the functional significance of this ‘fingerprint’ has historically not been well understood. A number of studies reviewed here have shown that the
Sleep spindles and procedural memory
The most compelling evidence for the role of sleep spindles in memory consolidation comes from studies using procedural memory tasks. In one of the first studies investigating the link between Stage 2 sleep and procedural memory in humans, memory for the Pursuit Rotor task was found to be impaired following selective Stage 2 sleep deprivation (Smith and MacNeill, 1994). Studies from our group (Fogel and Smith, 2006, Nader and Smith, 2003) have shown that an intense period of procedural learning
Learning-dependent changes in sleep spindles in the rat
Steriade and colleagues have played an important role in characterizing the physiological characteristics and generating mechanisms of the sleep spindle, and have speculated that sleep spindles are involved in memory consolidation. Destexhe and Sejnowski (2001) have provided a detailed theoretical and computational background for the long-term synaptic changes sleep spindles may produce necessary for memory consolidation. Several recent studies in rats provide physiological evidence to support
Sleep spindles and declarative memory
Sleep spindles have also been implicated in the consolidation of declarative memory. The same pattern of hippocampal activation observed during wakefulness is reactivated during non-REM sleep in rats (Lee and Wilson, 2002, Wilson and McNaughton, 1994) and REM sleep (Kudrimoti et al., 1999, Nadasdy et al., 1999). Lee and Wilson (2002) recorded the activity of spatially receptive hippocampal place cells while running rats through a simple maze and found the same pattern repeated over consecutive
Learning-dependent changes in sleep spindles during a daytime nap
The benefits of a daytime nap on performance have been well documented (Broughton and Dinges, 1989) however, it is not clear what processes are involved in producing these benefits. The role of the sleep spindle in simple motor procedural memory performance improvement was investigated following a short daytime nap (Milner et al., 2006). Four groups were used to assess pre–post-nap changes in performance including habitual nappers and habitual non-nappers who both slept during a 20-min nap
Conclusions and future directions
The sleep spindle was one of the first electrophysiological features of sleep to be discovered (Loomis et al., 1935a, Loomis et al., 1935b), and is one of the identifying features of non-REM sleep (Rechtschaffen and Kales, 1968). Since that time and until recently, identifying the function of the sleep spindle has been elusive for neuroscientists. Many neurophysiological studies have suggested that the sleep spindle is ideal for memory consolidation (Destexhe and Sejnowski, 2001, Rosanova and
Acknowledgements
Research reviewed here conducted by authors SMF and CTS was in collaboration with Kimberly Cote, Department of Psychology, Brock University, St. Catharine's, Ontario, Canada and Richard Beninger, Department of Psychology & Psychiatry, Queen's University, Kingston, Ontario, Canada. SMF and CTS are funded by Natural Sciences and Engineering Research Council (NSERC) of Canada, and CTS by Canadian Institutes of Health Research (CIHR).
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