Aging-Related Changes in Cortical Sources of Sleep Oscillatory Neural Activity Following Motor Learning Reflect Contributions of Cortical Thickness and Pre-sleep Functional Activity

Oscillatory neural activity during sleep, such as that in the delta and sigma bands, is important for motor learning consolidation. This activity is reduced with typical aging, and this reduction may contribute to aging-related declines in motor learning consolidation. Evidence suggests that brain regions involved in motor learning contribute to oscillatory neural activity during subsequent sleep. However, aging-related differences in regional contributions to sleep oscillatory activity following motor learning are unclear. To characterize these differences, we estimated the cortical sources of consolidation-related oscillatory activity using individual anatomical information in young and older adults during non-rapid eye movement sleep after motor learning and analyzed them in light of cortical thickness and pre-sleep functional brain activation. High-density electroencephalogram was recorded from young and older adults during a midday nap, following completion of a functional magnetic resonance imaged serial reaction time task as part of a larger experimental protocol. Sleep delta activity was reduced with age in a left-weighted motor cortical network, including premotor cortex, primary motor cortex, supplementary motor area, and pre-supplementary motor area, as well as non-motor regions in parietal, temporal, occipital, and cingulate cortices. Sleep theta activity was reduced with age in a similar left-weighted motor network, and in non-motor prefrontal and middle cingulate regions. Sleep sigma activity was reduced with age in left primary motor cortex, in a non-motor right-weighted prefrontal-temporal network, and in cingulate regions. Cortical thinning mediated aging-related sigma reductions in lateral orbitofrontal cortex and frontal pole, and partially mediated delta reductions in parahippocampal, fusiform, and lingual gyri. Putamen, caudate, and inferior parietal cortex activation prior to sleep predicted frontal and motor cortical contributions to sleep delta and theta activity in an age-moderated fashion, reflecting negative relationships in young adults and positive or absent relationships in older adults. Overall, these results support the local sleep hypothesis that brain regions active during learning contribute to consolidation-related neural activity during subsequent sleep and demonstrate that sleep oscillatory activity in these regions is reduced with aging.

One-Year Follow-Up of Healthy Older Adults with Electroencephalographic Risk for Neurocognitive Disorder After Neurofeedback Training

Background: In healthy older adults, excess theta activity is an electroencephalographic (EEG) predictor of cognitive impairment. In a previous study, neurofeedback (NFB) treatment reinforcing reductions theta activity resulted in EEG reorganization and cognitive improvement. Objective: To explore the clinical applicability of this NFB treatment, the present study performed a 1-year follow-up to determine its lasting effects. Methods: Twenty seniors with excessive theta activity in their EEG were randomly assigned to the experimental or control group. The experimental group received an auditory reward when the theta absolute power (AP) was reduced. The control group received the reward randomly. Results: Both groups showed a significant decrease in theta activity at the training electrode. However, the EEG results showed that only the experimental group underwent global changes after treatment. These changes consisted of delta and theta decreases and beta increases. Although no changes were found in any group during the period between the posttreatment evaluation and follow-up, more pronounced theta decreases and beta increases were observed in the experimental group when the follow-up and pretreatment measures were compared. Executive functions showed a tendency to improve two months after treatment which became significant one year later. Conclusion: These results suggest that the EEG and behavioral benefits of this NFB treatment persist for at least one year, which adds up to the available evidence contributing to identifying factors that increase its efficacy level. The relevance of this study lies in its prophylactic features of addressing a clinically healthy population with EEG risk of cognitive decline.

Inhibitory Control in the Absence of Awareness: Interactions Between Frontal and Motor Cortex Oscillations Mediate Implicitly Learned Responses

Cognitive control of action is associated with conscious effort and is hypothesised to be reflected by increased frontal theta activity. However, the functional role of these increases in theta power, and how they contribute to cognitive control remains unknown. We conducted an MEG study to test the hypothesis that frontal theta oscillations interact with sensorimotor signals in order to produce controlled behaviour, and that the strength of these interactions will vary with the amount of control required. We measured neuromagnetic activity in 16 healthy adults performing a response inhibition (Go/Switch) task, known from previous work to modulate cognitive control requirements using hidden patterns of Go and Switch cues. Learning was confirmed by reduced reaction times (RT) to patterned compared to random Switch cues. Concurrent measures of pupil diameter revealed changes in subjective cognitive effort with stimulus probability, even in the absence of measurable behavioural differences, revealing instances of covert variations in cognitive effort. Significant theta oscillations were found in five frontal brain regions, with theta power in the right middle frontal and right premotor cortices parametrically increasing with cognitive effort. Similar increases in oscillatory power were also observed in motor cortical gamma, suggesting an interaction. Right middle frontal and right precentral theta activity predicted changes in pupil diameter across all experimental conditions, demonstrating a close relationship between frontal theta increases and cognitive control. Although no theta-gamma cross-frequency coupling was found, long-range theta phase coherence among the five significant sources between bilateral middle frontal, right inferior frontal, and bilateral premotor areas was found, thus providing a mechanism for the relay of cognitive control between frontal and motor areas via theta signalling. Furthermore, this provides the first evidence for the sensitivity of frontal theta oscillations to implicit motor learning and its effects on cognitive load. More generally these results present a possible a mechanism for this frontal theta network to coordinate response preparation, inhibition and execution.

Theta Neurofeedback Training Supports Motor Performance and Flow Experience

Flow is defined as a cognitive state that is associated with a feeling of automatic and effortless control, enabling peak performance in highly challenging situations. In sports, flow can be enhanced by mindfulness training, which has been associated with frontal theta activity (4-8 Hz). Moreover, frontal-midline theta oscillations were shown to subserve control processes in a large variety of cognitive tasks. Based on previous theta neurofeedback training studies, which revealed that one training session is sufficient to enhance motor performance, the present study investigated whether one 30-minute session of frontal-midline theta neurofeedback training (1) enhances flow experience additionally to motor performance in a finger tapping task, and (2) transfers to cognitive control processes in an n-back task. Participants, who were able to successfully upregulate their theta activity during neurofeedback training (responders), showed better motor performance and flow experience after training than participants, who did not enhance their theta activity (non-responders). Across all participants, increase of theta activity during training was associated with motor performance enhancement from pretest to posttest irrespective of pre-training performance. Interestingly, theta training gains were also linked to the increase of flow experience, even when corresponding increases in motor performance were controlled for. Results for the n-back task were not significant. Even though these findings are mainly correlational in nature and additional flow-promoting influences need to be investigated, the present findings suggest that frontal-midline theta neurofeedback training is a promising tool to support flow experience with additional relevance for performance enhancement.

Targeted memory reactivation in human REM sleep elicits recurrent, temporally compressed reactivation

Memories are reactivated during non-rapid eye movement (NREM) sleep, but the question of whether equivalent reactivation also occurs in rapid eye movement (REM) sleep is hotly debated. To examine this, we used a technique called targeted memory reactivation (TMR) in which sounds are paired with learned material in wake, and then re-presented in subsequent sleep to trigger reactivation. We then used machine learning classifiers to identify TMR-induced reactivation in REM. The reactivation we measured was temporally compressed by approximately five times during REM compared to wakeful performance of the task, and often occurred twice after a single TMR cue. Reactivation strength positively predicted overnight performance improvement and was only apparent in trials with high theta activity. These findings provide strong evidence for memory reactivation in human REM sleep after TMR as well as an initial characterisation of this reactivation.

Theta activity during encoding interacts with NREM sleep oscillations to predict memory generalization

Relatively little is known regarding the interaction between encoding-related neural activity and sleep-based memory consolidation. One suggestion is that a function of encoding-related theta power may be to 'tag' memories for subsequent processing during sleep. This study aimed to extend previous work on the relationships between sleep spindles, slow oscillation-spindle coupling and task-related theta activity with a combined Deese-Roediger-McDermott (DRM) and nap paradigm. This allowed us to examine the influence of task- and sleep-related oscillatory activity on the recognition of both encoded list words and associative theme words. Thirty-three participants (29 females, mean age = 23.2 years) learned and recognised DRM lists separated by either a 2hr wake or sleep period. Mixed-effects modelling revealed the sleep condition endorsed more associative theme words and fewer list words in comparison to the wake group. Encoding related theta power was also found to influence sleep spindle density, and this interaction was predictive of memory outcomes. The influence of encoding-related theta was specific to sleep spindle density, and did not appear to influence the strength of slow oscillation-spindle coupling as it relates to memory outcomes. The finding of interactions between wakeful and sleep oscillatory-related activity in promoting memory and learning has important implications for theoretical models of sleep-based memory consolidation.

Mirroring and brain connectivity of gesture observation

Non-verbal communication involves di rent channels, as gestures, to communicate different information. The present study aims investigating the electrophysiological (EEG) correlates underlying the use of affective, social, and informative gestures during gesture observation by an encoder (who observed to reproduce the gestures successively) and decoder (who simply observed the gestures). Mirroring mechanisms were considered for a gesture observation task. Results showed an increase of frontal alpha, delta, and theta brain responsiveness and intra-brain connectivity for affective and social gestures. and of posterior (temporo-parietal) alpha activity and alpha and delta intra-brain connectivity for informative ones. Concerning inter-agents' role, similar responses were found for all gestures. Regarding gesture valence, an increase of delta and theta activity was observed for positive gestures on the left cerebral side. This study, therefore, revealed the function of gestures' type and valence in influencing individuals' brain activity, showing the presence of mirroring mechanisms underlying gesture observation.