Transcranial electrical stimulation during sleep enhances declarative (but not procedural) memory consolidation: Evidence from a meta-analysis

Barham, Michael P.; Enticott, Peter G.; Conduit, Russell; Lum, Jarrad A. G.

doi:10.1016/j.neubiorev.2016.01.009

Cited by 68 publications

(66 citation statements)

References 81 publications

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“…auditory stimulation, pharmacology or slow-oscillatory direct current stimulation) were only successful in enhancing sleep spindles as a side effect of enhancing slow oscillations [9, 10, 12, 13] or the time spent in sleep stages, such as slow wave sleep [11]. In addition, tES approaches so far only enhanced declarative memory but failed to improve procedural tasks [43] even though one of the studies reported increases in sleep spindle measures along with enhanced slow oscillations/slow wave sleep [10]. A possible explanation for this missing effect on procedural memory is that the reported significant increase in sleep spindles were only found for slow-frequency spindles but not for the fast spindles [10].…”

Section: Discussionmentioning

confidence: 99%

“…A possible explanation for this missing effect on procedural memory is that the reported significant increase in sleep spindles were only found for slow-frequency spindles but not for the fast spindles [10]. In addition all studies using tES to modulate NREM sleep and enhance memory consolidation applied either slow-oscillatory tDCS/ACS (0.75 Hz) or tDCS [43] and were therefore not optimized to selectively target sleep spindles. We are the first here to selectively enhance sleep spindle activity along with motor memory consolidation using FB-tACS throughout nocturnal sleep and therefore provide a functional role of these oscillations in cognitive processes.…”

Section: Discussionmentioning

confidence: 99%

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Feedback-Controlled Transcranial Alternating Current Stimulation Reveals a Functional Role of Sleep Spindles in Motor Memory Consolidation

et al. 2016

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Summary Transient episodes of brain oscillations are a common feature of both the waking and sleeping brain. Sleep spindles represent a prominent example of a poorly understood transient brain oscillation that is impaired in disorders such as Alzheimer’s disease and schizophrenia. Yet, the causal role of these bouts of thalamo-cortical oscillations remains unknown. Demonstrating a functional role of sleep spindles in cognitive processes has so far been hindered by the lack of a tool to target transient brain oscillations in real-time. Here, we show for the first time selective enhancement of sleep spindles with non-invasive brain stimulation in humans. We developed a system that detects sleep spindles in real-time and applies oscillatory stimulation. Our stimulation selectively enhanced spindle activity as determined by increased sigma activity after tACS application. This targeted modulation caused significant enhancement of motor memory consolidation that correlated with the stimulation-induced change in fast spindle activity. Strikingly, we found a similar correlation between motor memory and spindle characteristics during the sham night for the same spindle frequencies and electrode locations. Therefore, our results directly demonstrate a functional relationship between oscillatory spindle activity and cognition.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Feedback-Controlled Transcranial Alternating Current Stimulation Reveals a Functional Role of Sleep Spindles in Motor Memory Consolidation

et al. 2016

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“…Though a direct demonstration is lacking, several studies have applied tDCS during waking rest at time periods when replay is thought to occur (Javadi and Cheng 2013;Sandrini et al 2014;Tecchio et al 2010) and subsequently demonstrated greater consolidation. Similarly, the application of slow-oscillating tDCS during slow-wave sleep has been shown to enhance declarative memory (reviewed in Barham et al 2016). These enhancements are also accompanied by an increase in slow-oscillating waves (<1Hz), a neural frequency band which is temporally associated with the onset of neural replay (Genzel and Robertson 2015).…”

Section: Neurobiology Of Consolidation and Tdcsmentioning

confidence: 99%

“…Similarly, reactivation of a previously learned word list hours or a day later led to better retention if stimulation was administered directly during this reactivation/reconsolidation period (Javadi and Cheng 2013;Sandrini et al 2014). Furthermore, stimulation during sleep seems especially fruitful for declarative memory enhancement if timed during the appropriate consolidation period during slow-wave sleep (Barham et al 2016). Therefore, it is possible that while online stimulation may promote LTP-related protein synthesis at the synapse (Gartside 1968), offline stimulation after task completion or during sleep may directly enhance learning-associated neural replay and system consolidation for long-term retention.…”

Section: Timing Of Stimulationmentioning

confidence: 99%

Optimizing Transcranial Direct Current Stimulation Protocols to Promote Long-Term Learning

Karsten

Buschkuehl

et al. 2017

J Cogn Enhanc

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Transcranial direct current stimulation (tDCS) is a form of non-invasive brain stimulation that has the potential to induce polarity-specific changes in neural activity within targeted brain regions. There is growing interest in the use of this technology for the enhancement of higher cognitive functions, and application of tDCS directly before or concomitant with task performance has shown promise in modulating a range of behavioral outcomes, including motor skill acquisition, working memory performance, and implicit and explicit learning. The proposed mechanism for the observed enhancements is a temporary and targeted shift in the excitability of the cortical regions that subserve the relevant tasks, lasting from minutes up to about an hour after cessation of stimulation. Although empirical work does support at least a partial role for this mechanism, an arguably more potent but relatively underexplored phenomenon is thought to occur in the hours or days after stimulation-that is, a facilitation of consolidative processes. Here, we review the literature describing the nature of tDCS-enhanced consolidation and argue that some of the mixed results among the single-session studies that currently dominate the extant literature may be explained by a failure to take advantage of these potentially powerful offline effects. Accordingly, we further contend that the full potential of tDCS cannot be truly realized without a longitudinal design which allows for tDCS to act directly upon learning by promoting consolidation between sessions. Finally, we review preliminary evidence that these consolidation effects can be even further enhanced via strategically spaced out stimulation sessions, which take advantage of a long-held tenet in the literature that distributed learning produces better outcomes than massed learning. We conclude by proposing potential study designs to encourage the use of tDCS as more than merely a method to promote temporary enhancement, but also a technique to enhance long-term learning.

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“…Anodal and cathodal tDCS modulate visual working memory but can also disrupt practice-dependent improvement during a verbal working memory task when the cerebellum is stimulated (Ferrucco et al, 2008). Anodal tDCS to the anterior temporal lobes influences memories, improves decision making, attention, learning, language and memory consolidation (Barham et al, 2016; Brunoni et al, 2012; Cappon et al, 2000; Fregni et al, 2015; Mattai et al, 2011; Paulus, 2011; Varga et al, 2011; Young et al, 2013). However, all of these phenomena are transient.…”

Section: Introductionmentioning

confidence: 99%

Extended Multiple-Field High-Definition transcranial direct current stimulation (HD-tDCS) is well tolerated and safe in healthy adults

Turski

Kessler-Jones

Chow

et al. 2017

RNN

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Background High definition transcranial direct current stimulation (HD-tDCS) has been administered over single brain regions for small numbers of sessions. Safety, feasibility and tolerability of HD-tDCS over multiple brain regions, multiple daily stimulations and long periods are not established. Objective We studied safety, feasibility and tolerability of daily HD-tDCS over 2–4 brain regions for 20 sessions in healthy adults. Methods Five healthy adults underwent physical and neurological examination, electrocardiogram (EKG), electroencephalogram (EEG) and cognitive screening (ImpACT) before, during and after HD-tDCS. Four networks (left/right temporoparietal and frontal) were stimulated in sequence (20 min each) using HD-tDCS in 20 daily sessions. Sessions 1–10 included sequential stimulation of both temporoparietal networks, sessions 11–15 stimulations of 4 networks and sessions 16–20 two daily stimulation cycles of 4 networks/cycle (1.5 mA/network). Side effects, ImpACT scores and EEG power spectrum were compared before and after HD-tDCS. Results All subjects completed the trial. Adverse events were tingling, transient redness at the stimulation site, perception of continuing stimulation after end of session and one self-resolving headache. EEG power spectrum showed decreased delta power in frontal areas several days after HD-tDCS. While at the group level ImpACT scores did not differ before and after stimulations, we found a trend for correlation between decreased EEG delta power and individual improvements in ImpACT scores after HD-tDCS. Conclusion Prolonged, repeat daily stimulation of multiple brain regions using HD-tDCS is feasible and safe in healthy adults. Preliminary EEG results suggest that HD-tDCS may induce long lasting changes in excitability in the brain.

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Transcranial electrical stimulation during sleep enhances declarative (but not procedural) memory consolidation: Evidence from a meta-analysis

Cited by 68 publications

References 81 publications

Feedback-Controlled Transcranial Alternating Current Stimulation Reveals a Functional Role of Sleep Spindles in Motor Memory Consolidation

Feedback-Controlled Transcranial Alternating Current Stimulation Reveals a Functional Role of Sleep Spindles in Motor Memory Consolidation

Optimizing Transcranial Direct Current Stimulation Protocols to Promote Long-Term Learning

Extended Multiple-Field High-Definition transcranial direct current stimulation (HD-tDCS) is well tolerated and safe in healthy adults

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