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      Theta Dynamics Contribute to Retrieving Motor Plans after Interruptions in the Primate Premotor Area

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          Abstract

          To achieve a behavioral goal, we often need to maintain an internal action plan against external interruption and thereafter retrieve the action plan. We recently found that the maintenance and updating of motor plans are reflected by reciprocal changes in the beta and gamma power of the local field potential (LFP) of the primate medial motor areas. In particular, the maintenance of the immediate motor plan is supported by enhanced beta oscillations. However, it is unclear how the brain manages to maintain and retrieve the internal action plan against interruptions. Here, we show that dynamic theta changes contribute to the maintenance of the action plan. Specifically, the power of the theta frequency band (4–10 Hz) of LFPs increased before and during the interruption in the dorsal premotor areas in two monkeys. Without theta enhancement before the interruption, retrieval of the internal action plan was impaired. Theta and beta oscillations showed distinct changes depending on the behavioral context. Our results demonstrate that immediate and suspended motor plans are supported by the beta and theta oscillatory components of LFPs. Motor cortical theta oscillations may contribute to bridging motor plans across behavioral interruptions in a prospective manner.

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          Most cited references49

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          Neuronal oscillations in cortical networks.

          G Buzsáki (2004)
          Clocks tick, bridges and skyscrapers vibrate, neuronal networks oscillate. Are neuronal oscillations an inevitable by-product, similar to bridge vibrations, or an essential part of the brain's design? Mammalian cortical neurons form behavior-dependent oscillating networks of various sizes, which span five orders of magnitude in frequency. These oscillations are phylogenetically preserved, suggesting that they are functionally relevant. Recent findings indicate that network oscillations bias input selection, temporally link neurons into assemblies, and facilitate synaptic plasticity, mechanisms that cooperatively support temporal representation and long-term consolidation of information.
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            Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action.

            We show that while a primate chooses between two reaching actions, its motor system first represents both options and later reflects selection between them. When two potential targets appeared, many (43%) task-related, directionally tuned cells in dorsal premotor cortex (PMd) discharged if one of the targets was near their preferred direction. At the population level, this generated two simultaneous sustained directional signals corresponding to the current reach options. After a subsequent nonspatial cue identified the correct target, the corresponding directional signal increased, and the signal for the rejected target was suppressed. The PMd population reliably predicted the monkey's response choice, including errors. This supports a planning model in which multiple reach options are initially specified and then gradually eliminated in a competition for overt execution, as more information accumulates.
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              Working Memory 2.0

              Working memory is the fundamental function by which we break free from reflexive input-output reactions to gain control over our own thoughts. It has two types of mechanisms: online maintenance of information and its volitional or executive control. Classic models proposed persistent spiking for maintenance but have not explicitly addressed executive control. We review recent theoretical and empirical studies that suggest updates and additions to the classic model. Synaptic weight changes between sparse bursts of spiking strengthen working memory maintenance. Executive control acts via interplay between network oscillations in gamma (30-100 Hz) in superficial cortical layers (layers 2 and 3) and alpha and beta (10-30 Hz) in deep cortical layers (layers 5 and 6). Deep-layer alpha and beta are associated with top-down information and inhibition. It regulates the flow of bottom-up sensory information associated with superficial layer gamma. We propose that interactions between different rhythms in distinct cortical layers underlie working memory maintenance and its volitional control.
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                Author and article information

                Contributors
                Journal
                Cereb Cortex Commun
                Cereb Cortex Commun
                cercorcomms
                Cerebral Cortex Communications
                Oxford University Press
                2632-7376
                2021
                07 October 2021
                07 October 2021
                : 2
                : 4
                : tgab059
                Affiliations
                Department of Applied Mathematics , Fukuoka University , Fukuoka 814-0180, Japan
                Department of Physiology , Tohoku University School of Medicine , Sendai 980-8575, Japan
                Department of Integrative Neuroscience , Faculty of Medicine, University of Toyama , Toyama 930-0194, Japan
                Department of Physiology , Tohoku University School of Medicine , Sendai 980-8575, Japan
                Author notes
                Address correspondence to Hajime Mushiake, MD & PhD, Department of Physiology, Tohoku University School of Medicine, 2-1 Seiryo-cho, Aoba-ku, Sendai 980-8575, Japan. Email: hmushiak@ 123456med.tohoku.ac.jp
                Author information
                https://orcid.org/0000-0002-7045-5217
                Article
                tgab059
                10.1093/texcom/tgab059
                8597970
                1e1c2a8c-6f42-4d96-ab3d-c612b2af043b
                © The Author(s) 2021. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 8 July 2021
                : 10 September 2021
                : 17 September 2021
                : 11 November 2021
                Page count
                Pages: 13
                Funding
                Funded by: Japan Society for the Promotion of Science, DOI 10.13039/501100001691;
                Award ID: 15K21561
                Award ID: 18K11486
                Award ID: 21H03514
                Award ID: 21H05163
                Award ID: 15K01854
                Award ID: 17KK0140
                Award ID: 19H03337
                Award ID: JP16H0627
                Funded by: Ministry of Education, Culture, Sports, Science and Technology, DOI 10.13039/501100001700;
                Award ID: 15H05879
                Funded by: Japan Agency for Medical Research and Development, DOI 10.13039/100009619;
                Award ID: JP19dm0207001
                Funded by: Fukuoka University Fund;
                Award ID: 177102
                Award ID: 195004
                Categories
                Original Article

                action plan,beta oscillation,dorsal premotor area,interrupting task,theta oscillation

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