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.
Data availability
All data and analysis scripts have been deposited at OSF (https://osf.io/6hmrz/).
Article and author information
Author details
Funding
National Science Foundation (1734264)
- Ulrich Mayr
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Ethics
Human subjects: We obtained informed consent from human subjects. Consent and study procedures were approved by the University of Oregon's Human Subjects Institutional Review Board (Protocol 10272010.016).
Reviewing Editor
- David Badre, Brown University, United States
Version history
- Received: May 22, 2018
- Accepted: November 8, 2018
- Accepted Manuscript published: November 14, 2018 (version 1)
- Version of Record published: November 27, 2018 (version 2)
Copyright
© 2018, Kikumoto & Mayr
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
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- Genetics and Genomics
- Neuroscience
In the fruit fly Drosophila melanogaster, gustatory sensory neurons express taste receptors that are tuned to distinct groups of chemicals, thereby activating neural ensembles that elicit either feeding or avoidance behavior. Members of a family of ligand -gated receptor channels, the Gustatory receptors (Grs), play a central role in these behaviors. In general, closely related, evolutionarily conserved Gr proteins are co-expressed in the same type of taste neurons, tuned to chemically related compounds, and therefore triggering the same behavioral response. Here, we report that members of the Gr28 subfamily are expressed in largely non-overlapping sets of taste neurons in Drosophila larvae, detect chemicals of different valence, and trigger opposing feeding behaviors. We determined the intrinsic properties of Gr28 neurons by expressing the mammalian Vanilloid Receptor 1 (VR1), which is activated by capsaicin, a chemical to which wild-type Drosophila larvae do not respond. When VR1 is expressed in Gr28a neurons, larvae become attracted to capsaicin, consistent with reports showing that Gr28a itself encodes a receptor for nutritious RNA. In contrast, expression of VR1 in two pairs of Gr28b.c neurons triggers avoidance to capsaicin. Moreover, neuronal inactivation experiments show that the Gr28b.c neurons are necessary for avoidance of several bitter compounds. Lastly, behavioral experiments of Gr28 deficient larvae and live Ca2+ imaging studies of Gr28b.c neurons revealed that denatonium benzoate, a synthetic bitter compound that shares structural similarities with natural bitter chemicals, is a ligand for a receptor complex containing a Gr28b.c or Gr28b.a subunit. Thus, the Gr28 proteins, which have been evolutionarily conserved over 260 million years in insects, represent the first taste receptor subfamily in which specific members mediate behavior with opposite valence.