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Decoding hierarchical control of sequential behavior in oscillatory EEG activity.

ABSTRACT: Despite strong theoretical reasons for assuming that abstract representations organize complex action sequences in terms of subplans (chunks) and sequential positions, we lack methods to directly track such content-independent, hierarchical representations in humans. We applied time-resolved, multivariate decoding analysis to the pattern of rhythmic EEG activity that was registered while participants planned and executed individual elements from pre-learned, structured sequences. Across three experiments, the theta and alpha-band activity coded basic elements and abstract control representations, in particular, the ordinal position of basic elements, but also the identity and position of chunks. Further, a robust representation of higher level, chunk identity information was only found in individuals with above-median working memory capacity, potentially providing a neural-level explanation for working-memory differences in sequential performance. Our results suggest that by decoding oscillatory activity we can track how the cognitive system traverses through the states of a hierarchical control structure.

SUBMITTER: Kikumoto A

PROVIDER: S-EPMC6257819 | biostudies-literature | 2018 Nov

REPOSITORIES: biostudies-literature

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Decoding hierarchical control of sequential behavior in oscillatory EEG activity.

Kikumoto Atsushi A Mayr Ulrich U

eLife 20181114

Despite strong theoretical reasons for assuming that abstract representations organize complex action sequences in terms of subplans (chunks) and sequential positions, we lack methods to directly track such content-independent, hierarchical representations in humans. We applied time-resolved, multivariate decoding analysis to the pattern of rhythmic EEG activity that was registered while participants planned and executed individual elements from pre-learned, structured sequences. Across three ex ...[more]

PMID: 30426926

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Project description:Several findings underlined that the electrophysiological (EEG) background of the last segment of sleep before awakenings may predict the presence/absence of dream recall (DR) in young subjects. However, little is known about the EEG correlates of DR in elderly people. Only an investigation found differences between recall and non-recall conditions during NREM sleep EEG in older adults, while-surprisingly-no EEG predictor of DR was found for what concerns REM sleep. Considering REM sleep as a privileged scenario to produce mental sleep activity related to cognitive processes, our study aimed to investigate whether specific EEG topography and frequency changes during REM sleep in elderly people may predict a subsequent recall of mental sleep activity. Twenty-one healthy older volunteers (mean age 69.2 ± 6.07 SD) and 20 young adults (mean age 23.4 ± 2.76 SD) were recorded for one night from 19 scalp derivations. Dreams were collected upon morning awakenings from REM sleep. EEG signals of the last 5 min were analyzed by the Better OSCillation algorithm to detect the peaks of oscillatory activity in both groups. Statistical comparisons revealed that older as well as young individuals recall their dream experience when the last segment of REM sleep is characterized by frontal theta oscillations. No Recall (Recall vs. Non-Recall) × Age (Young vs. Older) interaction was found. This result replicated the previous evidence in healthy young subjects, as shown in within- and between-subjects design. The findings are completely original for older individuals, demonstrating that theta oscillations are crucial for the retrieval of dreaming also in this population. Furthermore, our results did not confirm a greater presence of the theta activity in healthy aging. Conversely, we found a greater amount of rhythmic theta and alpha activity in young than older participants. It is worth noting that the theta oscillations detected are related to cognitive functioning. We emphasize the notion that the oscillatory theta activity should be distinguished from the non-rhythmic theta activity identified in relation to other phenomena such as (a) sleepiness and hypoarousal conditions during the waking state and (b) cortical slowing, considered as an EEG alteration in clinical samples.

Project description:Background: Realization of online control of an artificial or virtual arm using information decoded from EEG normally occurs by classifying different activation states or voluntary modulation of the sensorimotor activity linked to different overt actions of the subject. However, using a more natural control scheme, such as decoding the trajectory of imagined 3D arm movements to move a prosthetic, robotic, or virtual arm has been reported in a limited amount of studies, all using offline feed-forward control schemes. Objective: In this study, we report the first attempt to realize online control of two virtual arms generating movements toward three targets/arm in 3D space. The 3D trajectory of imagined arm movements was decoded from power spectral density of mu, low beta, high beta, and low gamma EEG oscillations using multiple linear regression. The analysis was performed on a dataset recorded from three subjects in seven sessions wherein each session comprised three experimental blocks: an offline calibration block and two online feedback blocks. Target classification accuracy using predicted trajectories of the virtual arms was computed and compared with results of a filter-bank common spatial patterns (FBCSP) based multi-class classification method involving mutual information (MI) selection and linear discriminant analysis (LDA) modules. Main Results: Target classification accuracy from predicted trajectory of imagined 3D arm movements in the offline runs for two subjects (mean 45%, std 5%) was significantly higher (p < 0.05) than chance level (33.3%). Nevertheless, the accuracy during real-time control of the virtual arms using the trajectory decoded directly from EEG was in the range of chance level (33.3%). However, the results of two subjects show that false-positive feedback may increase the accuracy in closed-loop. The FBCSP based multi-class classification method distinguished imagined movements of left and right arm with reasonable accuracy for two of the three subjects (mean 70%, std 5% compared to 50% chance level). However, classification of the imagined arm movement toward three targets was not successful with the FBCSP classifier as the achieved accuracy (mean 33%, std 5%) was similar to the chance level (33.3%). Sub-optimal components of the multi-session experimental paradigm were identified, and an improved paradigm proposed.

Dataset Information

Decoding hierarchical control of sequential behavior in oscillatory EEG activity.

Publications

Decoding hierarchical control of sequential behavior in oscillatory EEG activity.

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