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Behavioral flexibility is associated with changes in structure and function distributed across a frontal cortical network in macaques

View ORCID ProfileJérôme Sallet, View ORCID ProfileMaryAnn P Noonan, Adam Thomas, Jill X O’Reilly, Jesper Anderson, Georgios K Papageorgiou, Franz X Neubert, Bashir Ahmed, Jackson Smith, Andrew H Bell, Mark J Buckley, Léa Roumazeilles, Steven Cuell, Mark E Walton, Kristine Krug, Rogier B Mars, Matthew FS Rushworth
doi: https://doi.org/10.1101/603530
Jérôme Sallet
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
2Wellcome Centre for Integrative Neuroimaging, Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom
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  • ORCID record for Jérôme Sallet
  • For correspondence: jerome.sallet@psy.ox.ac.uk
MaryAnn P Noonan
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
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Adam Thomas
2Wellcome Centre for Integrative Neuroimaging, Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom
3National Institute of Mental Health, Magnuson Clinical Center, Bethesda, MD, USA
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Jill X O’Reilly
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
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Jesper Anderson
2Wellcome Centre for Integrative Neuroimaging, Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom
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Georgios K Papageorgiou
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
4McGovern Institute for Brain Research and Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, USA
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Franz X Neubert
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
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Bashir Ahmed
5Department of Physiology, Anatomy and Genetics, University of Oxford, United Kingdom
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Jackson Smith
5Department of Physiology, Anatomy and Genetics, University of Oxford, United Kingdom
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Andrew H Bell
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
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Mark J Buckley
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
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Léa Roumazeilles
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
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Steven Cuell
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
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Mark E Walton
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
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Kristine Krug
5Department of Physiology, Anatomy and Genetics, University of Oxford, United Kingdom
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Rogier B Mars
2Wellcome Centre for Integrative Neuroimaging, Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom
6Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands
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Matthew FS Rushworth
1Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, United Kingdom
2Wellcome Centre for Integrative Neuroimaging, Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, University of Oxford, John Radcliffe Hospital, Oxford, United Kingdom
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Abstract

One of the most influential accounts of central orbitofrontal cortex– that it mediates behavioral flexibility – has been challenged by the finding that discrimination reversal in macaques –the classic test of behavioral flexibility –is unaffected when lesions are made by excitotoxin injection rather than aspiration. This suggests the critical brain circuit mediating behavioral flexibility in reversal tasks lies beyond the central orbitofrontal cortex. To determine its identity a group of nine macaques were taught discrimination reversal learning tasks and its impact on grey matter was measured. Magnetic resonance imaging scans were taken before and after learning and compared with scans from two control groups each comprising ten animals. One control group learned similar discrimination tasks but which lacked any reversal component and the other control group engaged in no learning. Grey matter changes were prominent in posterior orbitofrontal cortex/anterior insula but also were found in three other frontal cortical regions: lateral orbitofrontal cortex (12o), cingulate cortex, and lateral prefrontal cortex. In a second analysis, neural activity in posterior orbitofrontal cortex/anterior insula was measured at rest and its pattern of coupling with the other frontal cortical regions was assessed. Activity coupling increased significantly in the reversal learning group in comparison to controls. In a final set of experiments we used similar structural imaging procedures and analyses to demonstrate that aspiration lesion of central orbitofrontal cortex, of the type known to affect discrimination learning, affected structure and activity in the same frontal cortical circuit. The results identify a distributed frontal cortical circuit associated with behavioral flexibility.

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Posted April 10, 2019.
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Behavioral flexibility is associated with changes in structure and function distributed across a frontal cortical network in macaques
Jérôme Sallet, MaryAnn P Noonan, Adam Thomas, Jill X O’Reilly, Jesper Anderson, Georgios K Papageorgiou, Franz X Neubert, Bashir Ahmed, Jackson Smith, Andrew H Bell, Mark J Buckley, Léa Roumazeilles, Steven Cuell, Mark E Walton, Kristine Krug, Rogier B Mars, Matthew FS Rushworth
bioRxiv 603530; doi: https://doi.org/10.1101/603530
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Behavioral flexibility is associated with changes in structure and function distributed across a frontal cortical network in macaques
Jérôme Sallet, MaryAnn P Noonan, Adam Thomas, Jill X O’Reilly, Jesper Anderson, Georgios K Papageorgiou, Franz X Neubert, Bashir Ahmed, Jackson Smith, Andrew H Bell, Mark J Buckley, Léa Roumazeilles, Steven Cuell, Mark E Walton, Kristine Krug, Rogier B Mars, Matthew FS Rushworth
bioRxiv 603530; doi: https://doi.org/10.1101/603530

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