Rhythmically Modulating Neural Entrainment during Exposure to Regularities Influences Statistical Learning.

The ability to discover regularities in the environment, such as syllable patterns in speech, is known as statistical learning. Previous studies have shown that statistical learning is accompanied by neural entrainment, in which neural activity temporally aligns with repeating patterns over time. However, it is unclear whether these rhythmic neural dynamics play a functional role in statistical learning or whether they largely reflect the downstream consequences of learning, such as the enhanced perception of learned words in speech. To better understand this issue, we manipulated participants' neural entrainment during statistical learning using continuous rhythmic visual stimulation. Participants were exposed to a speech stream of repeating nonsense words while viewing either (1) a visual stimulus with a "congruent" rhythm that aligned with the word structure, (2) a visual stimulus with an incongruent rhythm, or (3) a static visual stimulus. Statistical learning was subsequently measured using both an explicit and implicit test. Participants in the congruent condition showed a significant increase in neural entrainment over auditory regions at the relevant word frequency, over and above effects of passive volume conduction, indicating that visual stimulation successfully altered neural entrainment within relevant neural substrates. Critically, during the subsequent implicit test, participants in the congruent condition showed an enhanced ability to predict upcoming syllables and stronger neural phase synchronization to component words, suggesting that they had gained greater sensitivity to the statistical structure of the speech stream relative to the incongruent and static groups. This learning benefit could not be attributed to strategic processes, as participants were largely unaware of the contingencies between the visual stimulation and embedded words. These results indicate that manipulating neural entrainment during exposure to regularities influences statistical learning outcomes, suggesting that neural entrainment may functionally contribute to statistical learning. Our findings encourage future studies using non-invasive brain stimulation methods to further understand the role of entrainment in statistical learning.

Eye movements during phasic versus tonic rapid eye movement sleep are biomarkers of dissociable electroencephalogram processes for the consolidation of novel problem-solving skills.

The hallmark eye movement (EM) bursts that occur during rapid eye movement (REM) sleep are markers of consolidation for procedural memory involving novel cognitive strategies and problem-solving skills. Examination of the brain activity associated with EMs during REM sleep might elucidate the processes involved in memory consolidation, and may uncover the functional significance of REM sleep and EMs themselves. Participants performed a REM-dependent, novel procedural problem-solving task (i.e. the Tower of Hanoi; ToH) before and after intervals of either overnight sleep (n = 20) or a daytime 8-hour wake period (n = 20). In addition, event-related spectral perturbation of the electroencephalogram (EEG) time-locked to EMs occurring either in bursts (i.e. phasic REM), or in isolation (i.e. tonic REM), were compared to sleep on a non-learning control night. ToH improvement was greater following sleep compared to wakefulness. During sleep, prefrontal theta (~2-8 Hz) and central-parietal-occipital sensorimotor rhythm (SMR) activity (~8-16 Hz) time-locked to EMs, were greater on the ToH night versus control night, and during phasic REM sleep, were both positively correlated with overnight memory improvements. Furthermore, SMR power during tonic REM increased significantly from the control night to ToH night, but was relatively stable from night to night during phasic REM. These results suggest that EMs are markers of learning-related increases in theta and SMR during phasic and tonic REM sleep. Phasic and tonic REM sleep may be functionally distinct in terms of their contribution to procedural memory consolidation.

Attention modulates neural measures associated with beat perception.

A growing body of evidence suggests that steady-state evoked potentials may be a useful measure of beat perception, particularly when obtaining traditional, explicit measures of beat perception is difficult, such as with infants or non-human animals. Although attending to a stimulus is not necessary for most traditional applications of steady-state evoked potentials, it is unknown how attention affects steady-state evoked potentials that arise in response to beat perception. Additionally, most applications of steady-state evoked potentials to measure beat perception have used repeating rhythms or real music. Therefore, it is unclear how the steady-state response relates to the robust beat perception that occurs with non-repeating rhythms. Here, we used electroencephalography to record participants' brain activity as they listened to non-repeating musical rhythms while either attending to the rhythms or while distracted by a concurrent visual task. Non-repeating auditory rhythms elicited steady-state evoked potentials at perceived beat frequencies (perception was validated in a separate sensorimotor synchronization task) that were larger when participants attended to the rhythms compared with when they were distracted by the visual task. Therefore, although steady-state evoked potentials appear to index beat perception to non-repeating musical rhythms, this technique may be limited to when participants are known to be attending to the stimulus.

Functional differences in cerebral activation between slow wave-coupled and uncoupled sleep spindles.

Spindles are often temporally coupled to slow waves (SW). These SW-spindle complexes have been implicated in memory consolidation that involves transfer of information from the hippocampus to the neocortex. However, spindles and SW, which are characteristic of NREM sleep, can occur as part of this complex, or in isolation. It is not clear whether dissociable parts of the brain are recruited when coupled to SW vs. when spindles or SW occur in isolation. Here, we tested differences in cerebral activation time-locked to uncoupled spindles, uncoupled SW and coupled SW-spindle complexes using simultaneous EEG-fMRI. Consistent with the "active system model," we hypothesized that brain activations time-locked to coupled SW-spindles would preferentially occur in brain areas known to be critical for sleep-dependent memory consolidation. Our results show that coupled spindles and uncoupled spindles recruit distinct parts of the brain. Specifically, we found that hippocampal activation during sleep is not uniquely related to spindles. Rather, this process is primarily driven by SWs and SW-spindle coupling. In addition, we show that SW-spindle coupling is critical in the activation of the putamen. Importantly, SW-spindle coupling specifically recruited frontal areas in comparison to uncoupled spindles, which may be critical for the hippocampal-neocortical dialogue that preferentially occurs during sleep.

Sleep and Second-Language Acquisition Revisited: The Role of Sleep Spindles and Rapid Eye Movements.

INTRODUCTION: Second-language learning (SLL) depends on distinct functional-neuroanatomical systems including procedural and declarative long-term memory. Characteristic features of rapid eye movement (REM) and non-REM sleep such as rapid eye movements and sleep spindles are electrophysiological markers of cognitively complex procedural and declarative memory consolidation, respectively. In adults, grammatical learning depends at first on declarative memory ("early SLL") then shifts to procedural memory with experience ("late SLL"). However, it is unknown if the shift from declarative to procedural memory in early vs late SLL is supported by sleep. Here, we hypothesized that increases in sleep spindle characteristics would be associated with early SLL, whereas increases in REM activity (eg, density and EEG theta-band activity time-locked to rapid eye movements) would be associated with late SLL. METHODS: Eight Anglophone (English first language) participants completed four polysomnographic recordings throughout an intensive 6-week French immersion course. Sleep spindle data and electroencephalographic spectral power time-locked to rapid eye movements were extracted from parietal temporal electrodes. RESULTS: As predicted, improvements in French proficiency were associated with changes in spindles during early SLL. Furthermore, we observed increased event-related theta power time-locked to rapid eye movements during late SLL compared with early SLL. The increases in theta power were significantly correlated with improvements in French proficiency. DISCUSSION: This supports the notion that sleep spindles are involved in early SLL when grammar depends on declarative memory, whereas cortical theta activity time-locked to rapid eye movements is involved in late SLL when grammar depends on procedural memory.