The Role of Sleep Spindles in Sleep-Dependent Memory Consolidation

Abstract

A well-established literature supports a critical role of sleep for learning and memory (Abel et al. in Curr Biol 23(17);R774–R788, 2013; Diekelmann and Born in Nat Rev Neurosci 11(2):114–126, 2010; Rasch and Born in Physiol Rev 93(2):681–766, 2013; Tononi and Cirelli in Sleep Med Rev 10(1):49–62, 2014). Studies have demonstrated memory improvements following a period of sleep compared to an equivalent time awake, and specific sleep features have been shown to correlate with improvements in discrete memory domains. For example, overnight procedural motor learning correlates with the amount of stage 2 sleep (Walker et al. in Neuron 35(1):205–211, 2002; Learn Mem 10(4):275–284, 2003), non-hippocampal dependent perceptual learning correlates with the product of the amount of slow wave sleep (SWS) and rapid eye movement (REM) sleep (Mednick et al. in Nat Neurosci 6(7):697–698, 2003; Stickgold et al. in J Cogn Neurosci 12(2):246–254, 2000), and implicit priming also appears to depend on REM sleep (Cai et al. in Proc Natl Acad Sci U S A 106(25);10130–10134, 2009). One feature of sleep that is widely implicated in memory processing is the sleep spindle, short (0.5–3 s) bursts of oscillatory activity in the frequency range of approximately 12–15 Hz (Spindles have also been defined as slow as 8–12 Hz, with some indication that these slow spindles may be physiologically distinct from alpha frequency, which oscillates in the same frequency range (8–12 Hz) but has a different spatial distribution (Manshanden et al. in Clin Neurophysiol 113(12):1937–1947, 2002). However, more data is required to determine the distinctiveness of these two signals. For the purpose of this chapter, we will primarily discuss spindles defined as ~12–15 Hz.). This chapter aims to (1) summarize correlational and causal evidence supporting the role of sleep spindles in memory processing; and (2) describe spindle dynamics and how they may be related to proposed mechanisms of sleep-dependent consolidation.

This work was supported by Bazhenov: Office of Naval Research/Multidisciplinary University Research Initiative Grant N000141310672 and National Institutes of Health Grants R01 EB009282, R01 MH099645; Mednick and Bazehnov: R01AG046646; Mednick: NSF BCS1439210; McDevitt: NSF fellowship.

Glossary

Declarative memory:

Conscious memory of facts and events. This type of memory is dependent on the hippocampus and other areas of the medial temporal lobe.

Non-declarative memory:

Unconscious memories such as habits or skills. This type of memory is typically not dependent on the hippocampus.

Rapid eye movement (REM) sleep:

A sleep stage characterized by rapid eye movements, low muscle tone, and rapid, low-voltage electroencephalogram (EEG) waveforms.

Slow wave sleep (SWS):

Also referred to as deep sleep; previously Stage 3 and Stage 4. Slow, high amplitude delta activity (1–4 Hz) predominates the EEG during SWS.

Slow oscillations:

Waveforms <1 Hz frequency with high voltage up and down states, which reflect periods of neuronal spiking and neuronal silence, respectively.

Spindles:

Bursts of oscillatory activity visible on an EEG that typically occur during NREM sleep. Spindles typically consist of 12–15 Hz waveforms that occur for at least 0.5 s. Spindle density refers to the number of spindles per minute of sleep.

Sharp-wave ripple complexes:

Composed of fast (~50–100 ms) bursts of spike activity (sharp waves) that are associated with high-frequency “ripples” (~150–200 Hz). These events are generated in the hippocampus.

Systems consolidation:

The process that refers to the time-limited role of the hippocampus in declarative memory storage. Information is originally encoded in both hippocampal and cortical regions. Successive reactivation of this hippocampal-cortical network is presumed to allow new memories to be gradually integrated with pre-existing memories and become independent of the hippocampus.

Spike-timing-dependent plasticity:

This refers to the process of change in synaptic weights, as a function of spike timing in pre- and post-synaptic neurons—there is an increase in synaptic weight when the pre-synaptic neuron fires prior to the post-synaptic neuron and a decrease in synaptic weight when the post-synaptic neuron fires prior to the pre-synaptic neuron.

Phase amplitude coupling:

This refers to modulation of the amplitude of one oscillation by the phase of another oscillation, and provides information about the temporal relationship between oscillations. For example, such coupling is observed between the peak amplitude of spindle frequency and slow oscillation phase.

Modulation index:

This index is one way to estimate the consistency of phase-amplitude coupling across various trials or events.