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      Recursion in action: An fMRI study on the generation of new hierarchical levels in motor sequences

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          Abstract

          Generation of hierarchical structures, such as the embedding of subordinate elements into larger structures, is a core feature of human cognition. Processing of hierarchies is thought to rely on lateral prefrontal cortex (PFC). However, the neural underpinnings supporting active generation of new hierarchical levels remain poorly understood. Here, we created a new motor paradigm to isolate this active generative process by means of fMRI. Participants planned and executed identical movement sequences by using different rules: a Recursive hierarchical embedding rule, generating new hierarchical levels; an Iterative rule linearly adding items to existing hierarchical levels, without generating new levels; and a Repetition condition tapping into short term memory, without a transformation rule. We found that planning involving generation of new hierarchical levels (Recursive condition vs. both Iterative and Repetition) activated a bilateral motor imagery network, including cortical and subcortical structures. No evidence was found for lateral PFC involvement in the generation of new hierarchical levels. Activity in basal ganglia persisted through execution of the motor sequences in the contrast Recursive versus Iteration, but also Repetition versus Iteration, suggesting a role of these structures in motor short term memory. These results showed that the motor network is involved in the generation of new hierarchical levels during motor sequence planning, while lateral PFC activity was neither robust nor specific. We hypothesize that lateral PFC might be important to parse hierarchical sequences in a multi‐domain fashion but not to generate new hierarchical levels.

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          Most cited references51

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          An information theoretical approach to prefrontal executive function.

          The prefrontal cortex subserves executive control--that is, the ability to select actions or thoughts in relation to internal goals. Here, we propose a theory that draws upon concepts from information theory to describe the architecture of executive control in the lateral prefrontal cortex. Supported by evidence from brain imaging in human subjects, the model proposes that action selection is guided by hierarchically ordered control signals, processed in a network of brain regions organized along the anterior-posterior axis of the lateral prefrontal cortex. The theory clarifies how executive control can operate as a unitary function, despite the requirement that information be integrated across multiple distinct, functionally specialized prefrontal regions.
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            Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes.

            Cognitive control supports flexible behavior by selecting actions that are consistent with our goals and appropriate for our environment. The prefrontal cortex (PFC) has an established role in cognitive control, and research on the functional organization of PFC promises to contribute to our understanding of the architecture of control. A recently popular hypothesis is that the rostro-caudal axis of PFC supports a control hierarchy whereby posterior-to-anterior PFC mediates progressively abstract, higher-order control. This review discusses evidence for a rostro-caudal gradient of function in PFC and the theories proposed to account for these results, including domain generality in working memory, relational complexity, the temporal organization of behavior and abstract representational hierarchy. Distinctions among these frameworks are considered as a basis for future research.
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              A parametric study of prefrontal cortex involvement in human working memory.

              Although recent neuroimaging studies suggest that prefrontal cortex (PFC) is involved in working memory (WM), the relationship between PFC activity and memory load has not yet been well-described in humans. Here we use functional magnetic resonance imaging (fMRI) to probe PFC activity during a sequential letter task in which memory load was varied in an incremental fashion. In all nine subjects studied, dorsolateral and left inferior regions of PFC were identified that exhibited a linear relationship between activity and WM load. Furthermore, these same regions were independently identified through direct correlations of the fMRI signal with a behavioral measure that indexes WM function during task performance. A second experiment, using whole-brain imaging techniques, both replicated these findings and identified additional brain regions showing a linear relationship with load, suggesting a distributed circuit that participates with PFC in subserving WM. Taken together, these results provide a "dose-response curve" describing the involvement of both PFC and related brain regions in WM function, and highlight the benefits of using graded, parametric designs in neuroimaging research.
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                Author and article information

                Contributors
                diasmarm@hu-berlin.de
                Journal
                Hum Brain Mapp
                Hum Brain Mapp
                10.1002/(ISSN)1097-0193
                HBM
                Human Brain Mapping
                John Wiley & Sons, Inc. (Hoboken, USA )
                1065-9471
                1097-0193
                05 March 2019
                15 June 2019
                : 40
                : 9 ( doiID: 10.1002/hbm.v40.9 )
                : 2623-2638
                Affiliations
                [ 1 ] Berlin School of Mind and Brain Humboldt‐Universität zu Berlin Berlin Germany
                [ 2 ] Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences Leipzig Germany
                [ 3 ] Clinic for Cognitive Neurology University Hospital Leipzig Germany
                [ 4 ] Ear Institute, University College London London UK
                Author notes
                [*] [* ] Correspondence

                Mauricio Dias Martins, Berlin School of Mind and Brain, Humboldt Universität zu Berlin, Luisenstrasse 56, Berlin 10117, Germany.

                Email: diasmarm@ 123456hu-berlin.de

                Author information
                https://orcid.org/0000-0003-0247-8473
                https://orcid.org/0000-0001-9613-8933
                https://orcid.org/0000-0001-7458-0229
                Article
                HBM24549
                10.1002/hbm.24549
                6865530
                30834624
                42758fe0-e09f-4196-9fbb-16594c3658e1
                © 2019 The Authors. Human Brain Mapping published by Wiley Periodicals, Inc.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.

                History
                : 02 September 2018
                : 17 January 2019
                : 30 January 2019
                Page count
                Figures: 7, Tables: 2, Pages: 16, Words: 12656
                Categories
                Research Article
                Research Articles
                Custom metadata
                2.0
                June 15, 2019
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.7.2 mode:remove_FC converted:15.11.2019

                Neurology
                fmri,hierarchy,motor,prefrontal cortex,recursion
                Neurology
                fmri, hierarchy, motor, prefrontal cortex, recursion

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