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And Large-Scale Synchronization in Cognitive Control and Inhibition: a Review Research Collection Review Article Patterns of Focal- and Large-Scale Synchronization in Cognitive Control and Inhibition: A Review Author(s): Beppi, Carolina; Violante, Ines R.; Hampshire, Adam; Grossman, Nir; Sandrone, Stefano Publication Date: 2020-06 Permanent Link: https://doi.org/10.3929/ethz-b-000426886 Originally published in: Frontiers in Human Neuroscience 14, http://doi.org/10.3389/fnhum.2020.00196 Rights / License: Creative Commons Attribution 4.0 International This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library MINI REVIEW published: 25 June 2020 doi: 10.3389/fnhum.2020.00196 Patterns of Focal- and Large-Scale Synchronization in Cognitive Control and Inhibition: A Review Carolina Beppi 1,2*, Ines R. Violante 3,4, Adam Hampshire 3, Nir Grossman 5 and Stefano Sandrone 3 1Neuroscience Center Zürich (ZNZ), University of Zürich (UZH) and Swiss Federal Institute of Technology in Zürich (ETH), Zurich, Switzerland, 2Department of Neurology, University Hospital Zürich, University of Zürich, Zurich, Switzerland, 3Computational, Cognitive and Clinical Neuroscience Laboratory (C3NL), Department of Brain Sciences, Imperial College London, London, United Kingdom, 4School of Psychology, Faculty of Health and Medical Sciences, University of Surrey, Guildford, United Kingdom, 5Department of Brain Sciences, Imperial College London, London, United Kingdom Neural synchronization patterns are involved in several complex cognitive functions and constitute a growing trend in neuroscience research. While synchrony patterns in working memory have been extensively discussed, a complete understanding of Edited by: their role in cognitive control and inhibition is still elusive. Here, we provide an up-to- Seiki Konishi, Juntendo University, Japan date review on synchronization patterns underlying behavioral inhibition, extrapolating Reviewed by: common grounds, and dissociating features with other inhibitory functions. Moreover, we Junichi Chikazoe, suggest a schematic conceptual framework and highlight existing gaps in the literature, National Institute for Physiological Sciences (NIPS), Japan current methodological challenges, and compelling research questions for future studies. Weidong Cai, Keywords: neural oscillations, de(synchronization), stop-signal task, Go/No-go task, response inhibition, cognitive Stanford University School of inhibition, interference suppression, rule inhibition Medicine, United States *Correspondence: Carolina Beppi [email protected] INTRODUCTION Specialty section: This article was submitted to Investigating the relationship between cognitive function and underlying cerebral activity has Cognitive Neuroscience, a section of been, and still is, one of the greatest neuroscientific challenges. Functional magnetic resonance the journal Frontiers in Human imaging (fMRI) is a leading imaging method for quantifying and mapping the geographical Neuroscience distribution of metabolic changes associated with brain activity, while resting (Riedl et al., 2016) or actively processing information (Chen and Glover, 2015). Electroencephalography (EEG) is Received: 09 March 2020 a well-established electrophysiological technique providing a temporally accurate recording of Accepted: 30 April 2020 postsynaptic superficial brain activity (Burle et al., 2015), safely and non-invasively (Cohen, Published: 25 June 2020 2017), at rest or during task performance (Zani and Proverbio, 2003). Together with magneto- Citation: electroencephalography (MEG), EEG has extensively contributed to the understanding of how the Beppi C, Violante IR, Hampshire A, brain’s oscillations at different frequencies relate to specific mental states and processes (Benedek Grossman N and Sandrone S (2020) et al., 2014). Moreover, it permits to measure local alterations in amplitude, phase, and synchrony, Patterns of Focal- and Large-Scale Synchronization in Cognitive Control and to explore spatial and temporal distributions associated with specific cognitive functions and Inhibition: A Review. (Perfetti et al., 2011; Groppe et al., 2013; Roux and Uhlhaas, 2014), such as attention and memory. Front. Hum. Neurosci. 14:196. This article will review the current knowledge of the patterns of focal and large-scale coordination doi: 10.3389/fnhum.2020.00196 supporting cognitive control and inhibition. Frontiers in Human Neuroscience| www.frontiersin.org 1 June 2020 | Volume 14 | Article 196 Beppi et al. Synchronization, Cognitive Control and Inhibition The Importance of Large-Scale Sauseng et al., 2004; Schack et al., 2005). The contribution of Synchronization in Complex different network components in a given task is dynamic in time Cognitive Functions and extent and depends on the specific cognitive requirement. Cross-frequency phase-phase/amplitude coupling dynamics Increased EEG/MEG amplitude, power and event-related have been described in working memory processes. However, synchronization (ERS), or desynchronization (ERD), within it is yet to be established how they apply to behavioral local circuits and specific frequencies support distinct cognitive inhibition, a complex function that relies on a combination processes, including sensory processing and memory (reviewed of cognitive processes, including attention, working memory, in Uhlhaas et al., 2008; Roohi-Azizi et al., 2017). However, action selection (Hampshire et al., 2007; Stokes et al., 2013; functional connectivity reports suggest that more complex Provenza et al., 2019; Widge et al., 2019a), and that is cognitive tasks, involving a dynamic combination of cognitive likewise distributed across brain networks (Erika-Florence et al., processes, require a fast and adjustable information exchange 2014; Hampshire and Sharp, 2015). Existing knowledge and between brain circuits of large scale (Hampshire et al., evidence in this regard will be reviewed and elucidated in the 2012). More emphasis is thus now given to investigating following sections. coordination processes between long-range neural networks and the underlying neurobiological mechanisms during more FOCAL AND DISTRIBUTED PATTERNS OF demanding cognitive functions (Fries, 2005; Fell and Axmacher, 2011; Kazanovich, 2019; Wang et al., 2019). NEURAL SYNCHRONY IN BEHAVIORAL Phase-synchronization processes ease the information INHIBITION exchange within distributed brain networks, increasing network efficiency, and facilitating synaptic plasticity (Varela et al., 2001; Control and Inhibition—Brief Conceptual Fries, 2005, 2015; Womelsdorf et al., 2007; Deco et al., 2011; Definitions Fell and Axmacher, 2011; Parkin et al., 2015; Constantinidis Executive control is a major cognitive function comprising and Klingberg, 2016; Violante et al., 2017). The importance several sub-functions (Jewsbury et al., 2016; Purpura et al., of intact long-range synchronization dynamics is evident 2017), including attentional control and working memory. But in clinical contexts, where cognitively impaired Alzheimer’s it encompasses also inhibitory control or inhibition (Jones et al., patients display significantly decreased phase-coordination 2016), which regulates flexible and adaptive overt responses between most cortical regions in the delta band, relative to as well as purpose-directed mental processes (Stuphorn and controls (Hata et al., 2016). This calls for the need for further Emeric, 2012). The ability to inhibit an internal process, or investigations and the development of methods (e.g., Pesaran to interfere with external information is generally referred to et al., 2018; Widge et al., 2019a) to study synchronization as inhibitory control or, simply, inhibition (Xie et al., 2017). patterns between large-scale networks and the underlying The latter is, in turn, distinguished between behavioral or synaptic mechanisms, as well as their alterations in different response inhibition, which refers to the process of suppressing neuropsychiatric diseases. an ongoing motor action, whenever necessary (e.g., to implement an alternative response; Aron, 2007). The most established The study of large-scale synchronization implies recording paradigms used to study behavioral inhibition are summarized neural activity contemporaneously from distributed brain in Box 1. Cognitive inhibition (Bari and Robbins, 2013), locations before assessing whether the activity at different instead, involves the blockade of a mental process, such as loci alters in a synchronous fashion (Nowak et al., 2017). selective attention or memory retrieval (MacLeod, 2007), either Activity within single voxels or region-of-interests is tracked intentionally or unconsciously (Harnishfeger, 1995). A schematic measuring the correlation across them over time series (Harris representation of the different inhibitory subfunctions is shown and Gordon, 2015). Long-range phase-synchronization in Figure 1. dynamics between large-scale circuits can be explored Cognitive inhibition can be further distinguished into sub- within the same, or between a broad span of, different types. The act of preventing irrelevant sensory information from frequencies in EEG/MEG. Phase-coordination in different undergoing further processing in working memory (Wilson and frequencies is a type of cross-frequency coupling (CFC), called Kipp, 1998; Diamond et al., 2013) is known as interference ‘‘cross-frequency phase-phase coupling’’ (Palva et al., 2005). suppression (Nigg, 2000), and can be assessed through the Phase-amplitude
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