Author response: Decoding hierarchical control of sequential behavior in oscillatory EEG activity

AbstractDespite 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 independently 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 oscillations we can track how the cognitive system traverses through the states of a hierarchical control structure.

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Decoding hierarchical control of sequential behavior in oscillatory EEG activity

eLife ◽

10.7554/elife.38550 ◽

2018 ◽

Vol 7 ◽

Cited By ~ 4

Author(s):

Atsushi Kikumoto ◽

Ulrich Mayr

Keyword(s):

Working Memory ◽

Working Memory Capacity ◽

Hierarchical Control ◽

Oscillatory Activity ◽

Time Resolved ◽

Eeg Activity ◽

Action Sequences ◽

Oscillatory Eeg ◽

Hierarchical Representations ◽

Band Activity

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.

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Oscillatory EEG Activity During REM Sleep in Elderly People Predicts Subsequent Dream Recall After Awakenings

Frontiers in Neurology ◽

10.3389/fneur.2019.00985 ◽

2019 ◽

Vol 10 ◽

Cited By ~ 5

Author(s):

Serena Scarpelli ◽

Aurora D'Atri ◽

Chiara Bartolacci ◽

Anastasia Mangiaruga ◽

Maurizio Gorgoni ◽

...

Keyword(s):

Elderly People ◽

Rem Sleep ◽

Dream Recall ◽

Eeg Activity ◽

Oscillatory Eeg

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Oscillatory EEG activity induced by conditioning stimuli during fear conditioning reflects Salience and Valence of these stimuli more than Expectancy

Neuroscience ◽

10.1016/j.neuroscience.2016.12.047 ◽

2017 ◽

Vol 346 ◽

pp. 81-93 ◽

Cited By ~ 8

Author(s):

J.H. Chien ◽

L. Colloca ◽

A. Korzeniewska ◽

J.J. Cheng ◽

C.M. Campbell ◽

...

Keyword(s):

Fear Conditioning ◽

Eeg Activity ◽

Oscillatory Eeg ◽

Conditioning Stimuli

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Quantification of listening effort correlates in the oscillatory EEG activity: A feasibility study

2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society ◽

10.1109/embc.2012.6346995 ◽

2012 ◽

Cited By ~ 3

Author(s):

C. Bernarding ◽

D. J. Strauss ◽

R. Hannemann ◽

F. I. Corona-Strauss

Keyword(s):

Feasibility Study ◽

Listening Effort ◽

Eeg Activity ◽

Oscillatory Eeg

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Delta/Theta band EEG activity shapes the rhythmic perceptual sampling of auditory scenes

10.1101/2020.07.21.213694 ◽

2020 ◽

Author(s):

Cora Kubetschek ◽

Christoph Kayser

Keyword(s):

Time Scale ◽

Brain Activity ◽

Theta Band ◽

Eeg Activity ◽

Acoustic Information ◽

Power Prior ◽

Oscillatory Eeg ◽

Human Participants ◽

Frequency Sweeps ◽

Perceptual Weights

AbstractMany studies speak in favor of a rhythmic mode of listening, by which the encoding of acoustic information is structured by rhythmic neural processes at the time scale of about 1 to 4 Hz. Indeed, psychophysical data suggest that humans sample acoustic information in extended soundscapes not uniformly, but weigh the evidence at different moments for their perceptual decision at the time scale of about 2 Hz. We here test the critical prediction that such rhythmic perceptual sampling is directly related to the state of ongoing brain activity prior to the stimulus. Human participants judged the direction of frequency sweeps in 1.2 s long soundscapes while their EEG was recorded. Computing the perceptual weights attributed to different epochs within these soundscapes contingent on the phase or power of pre-stimulus oscillatory EEG activity revealed a direct link between the 4Hz EEG phase and power prior to the stimulus and the phase of the rhythmic component of these perceptual weights. Hence, the temporal pattern by which the acoustic information is sampled over time for behavior is directly related to pre-stimulus brain activity in the delta/theta band. These results close a gap in the mechanistic picture linking ongoing delta band activity with their role in shaping the segmentation and perceptual influence of subsequent acoustic information.

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Nigrostriatal Dopamine Signals Sequence-Specific Action-Outcome Prediction Errors

10.1101/2021.01.25.428032 ◽

2021 ◽

Author(s):

Nick G. Hollon ◽

Elora W. Williams ◽

Christopher D. Howard ◽

Hao Li ◽

Tavish I. Traut ◽

...

Keyword(s):

Reinforcement Learning ◽

Outcome Prediction ◽

Hierarchical Control ◽

Prediction Errors ◽

Sequential Behavior ◽

Nigrostriatal Dopamine ◽

Health And Disease ◽

Specific Prediction ◽

Goal Directed Behavior ◽

Self Stimulation

ABSTRACTDopamine has been suggested to encode cue-reward prediction errors during Pavlovian conditioning. While this theory has been widely applied to reinforcement learning concerning instrumental actions, whether dopamine represents action-outcome prediction errors and how it controls sequential behavior remain largely unknown. Here, by training mice to perform optogenetic intracranial self-stimulation, we examined how self-initiated goal-directed behavior influences nigrostriatal dopamine transmission during single as well as sequential instrumental actions. We found that dopamine release evoked by direct optogenetic stimulation was dramatically reduced when delivered as the consequence of the animal’s own action, relative to non-contingent passive stimulation. This action-induced dopamine suppression was specific to the reinforced action, temporally restricted to counteract the expected outcome, and exhibited sequence-selectivity consistent with hierarchical control of sequential behavior. Together these findings demonstrate that nigrostriatal dopamine signals sequence-specific prediction errors in action-outcome associations, with fundamental implications for reinforcement learning and instrumental behavior in health and disease.

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