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Review, Cognition and Behavior

Beyond the Status Quo: A Role for Beta Oscillations in Endogenous Content (Re)Activation

Bernhard Spitzer and Saskia Haegens
eNeuro 21 July 2017, 4 (4) ENEURO.0170-17.2017; https://doi.org/10.1523/ENEURO.0170-17.2017
Bernhard Spitzer
1Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom
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Saskia Haegens
2Department of Neurological Surgery, Columbia University College of Physicians and Surgeons, New York, NY 10032
3Centre for Cognitive Neuroimaging, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen 6500 HB, The Netherlands
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    Figure 1.

    Beyond motor control. Schematic overview of oscillatory beta-band effects across cortex. A, Overall beta activity changes (in-/decreases) associated with different cognitive functions (NB, nonexhaustive schematic). B, Content-specific modulations of beta-band activity; see text for details. For convenience, findings from human- and nonhuman primate studies are illustrated on a common template. Unless specified (L, left; R, right; C, contralateral), effects were not systematically lateralized.

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    Figure 2.

    Content-specific beta activity during WM processing. A, During WM maintenance of vibrotactile frequency information, prefrontal EEG beta power is parametrically modulated by the frequency of the to-be-maintained stimulus (f1). Adapted with permission from Spitzer et al. (2010). B, Similar beta power modulations were found in LFP recordings in monkey PFC during WM maintenance of visual motion information. Adapted with permission from Wimmer et al. (2016). Note that in standard delay tasks, beta modulations occurred mostly late in the WM delay period. C, In contrast, when participants were retro-cued to focus on a given WM content for further maintenance, beta was modulated early after the cue. Adapted with permission from Spitzer and Blankenburg (2011). D, Similar transient modulations were observed during WM processing of the approximate number of previously presented inputs (three to eight pulses in rapid sequence, illustrated in purple). Adapted with permission from Spitzer et al. (2014a). E, Content-specific fronto-parietal beta-synchronization during WM maintenance of visual object information in monkeys. As in A–D, these effects were absent during stimulus encoding. Adapted with permission from Salazar et al. (2012). Reprinted with permission from AAAS. F, Rule-dependent beta-synchronization in monkey PFC at the time of the to-be-evaluated stimulus (see also Fig. 4C). Adapted with permission from Buschman et al. (2012). Reprinted with permission from Elsevier.

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    Figure 3.

    Content-specific beta activity during decision making. A, Source reconstruction showing lateralized, effector-selective beta activity (left- vs right-hand response) before button press, in human subjects performing a visual motion detection task (left panel). Time courses of lateralized beta activity in motor cortex indicate accumulative updating of the motor plan as a decision evolves (right panel). Adapted with permission from Donner et al. (2009). Reprinted with permission from Elsevier. B, Beta power modulation in monkey medial premotor cortex before motor response in vibrotactile discrimination task reflects binary decision outcome, also on error trials. Spectra on the right are averaged over the time window indicated by dashed box in the left panel, per stimulus class (sorted by f2-f1 difference), for correct and incorrect trials separately. Adapted with permission from Haegens et al. (2011b). C, Remarkably similar observation as in B, in human EEG recordings using the same paradigm. Adapted with permission from Herding et al. (2016). © 2016 by the Massachusetts Institute of Technology, published by the MIT Press.

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    Figure 4.

    A framework for content-specific beta activity. A, Content-specific beta-synchronization as endogenously driven transition from latent to active cortical representation. Left, Active cortical representations (e.g., of currently perceived, task-relevant information) are characterized by spiking activity (symbolized in red) in content-specific neuronal ensembles. Second from left, In the absence of perceptual input and/or attentional prioritization, information can be retained in latent memory representations, without spiking activity in the content-specific ensemble, e.g., in patterns of synaptic weights. Second from right, Endogenously driven (re)activation of a content-coding ensemble is characterized by a brief period of beta-synchronization, involving both local and long-range (top-down) interactions (see text for details). Right, (Re)activated content representations may again be characterized by spiking ensemble activity, similar (but not necessarily exactly identical) to representations of just perceived information (compare with left). B, Local beta activity appears content specific when population-level recordings register the synchronization of individual subpopulations (symbolized in blue and red) with differential sensitivity (e.g., red > blue, by spatial proximity to recording site). C, Transient network-level beta coherence in monkey PFC during application of different task rules (Fig. 2F, dashed rectangle). Adapted with permission from Buschman et al. (2012). Reprinted with permission from Elsevier.

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Beyond the Status Quo: A Role for Beta Oscillations in Endogenous Content (Re)Activation
Bernhard Spitzer, Saskia Haegens
eNeuro 21 July 2017, 4 (4) ENEURO.0170-17.2017; DOI: 10.1523/ENEURO.0170-17.2017

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Beyond the Status Quo: A Role for Beta Oscillations in Endogenous Content (Re)Activation
Bernhard Spitzer, Saskia Haegens
eNeuro 21 July 2017, 4 (4) ENEURO.0170-17.2017; DOI: 10.1523/ENEURO.0170-17.2017
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  • Article
    • Abstract
    • Significance Statement
    • Introduction
    • Beta-band oscillations in WM
    • Beta-band oscillations in decision making
    • A role for beta oscillations in endogenous content (re)activation
    • Conclusion
    • Acknowledgments
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Keywords

  • beta rhythm
  • decision making
  • network interactions
  • neural oscillations
  • top-down control
  • working memory

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