Disentangling the Component Processes in Complex Planning Impairments Following Ventromedial Prefrontal Lesions

Journal of Neuroscience, vol. 45, pp. e1814242025

Abstract

Damage to the ventromedial prefrontal cortex (vmPFC) in humans disrupts planning abilities in naturalistic settings. However, it is unknown which components of planning are affected in these patients, including selecting the relevant information, simulating future states, or evaluating between these states. To address this question, we leveraged computational paradigms to investigate the role of vmPFC in planning, using the board game task "Four-in-a-Row" (18 lesion patients, 9 female; 30 healthy control participants, 16 female) and the simpler "Two-Step" task measuring model-based reasoning (49 lesion patients, 27 female; 20 healthy control participants, 13 female). Damage to vmPFC disrupted performance in Four-in-a-Row compared with both control lesion patients and healthy age-matched controls. We leveraged a computational framework to assess different component processes of planning in Four-in-a-Row and found that impairments following vmPFC damage included shallower planning depth and a tendency to overlook game-relevant features. In the "Two-Step" task, which involves binary choices across a short future horizon, we found little evidence of planning in all groups and no behavioral differences between groups. Complex yet computationally tractable tasks such as "Four-in-a-Row" offer novel opportunities for characterizing neuropsychological planning impairments, which in vmPFC patients we find are associated with oversights and reduced planning depth.

Authors 8

1. Eleanor Holton

   University of Oxford

   Affiliation as printed

   Department of Experimental Psychology, University of Oxford, Oxford OX2 6GG, United Kingdom eleanor.holton@psy.ox.ac.uk

   Department of Experimental Psychology, University of Oxford

2. Bas van Opheusden
   Affiliation as printed

   Imbue, Inc., San Francisco, California 94114

   2Imbue Inc., San Francisco, CA, 94114, USA

3. Jan Grohn

   University of Oxford · Wellcome Centre for Integrative Neuroimaging

   Affiliation as printed

   Department of Experimental Psychology, University of Oxford, Oxford OX2 6GG, United Kingdom

   Wellcome Centre for Integrative Neuroimaging (WIN), University of Oxford, Oxford OX3 9DA, United Kingdom

   Department of Experimental Psychology, University of Oxford

   Wellcome Centre for Integrative Neuroimaging (WIN), University of Oxford

4. John Patrick Grogan

   Trinity College Dublin

   Affiliation as printed

   Trinity Institute of Neuroscience, Trinity College Dublin, Dublin D02 PX31, Ireland

   Trinity College Institute of Neuroscience, Trinity College Dublin

5. Patricia L. Lockwood

   University of Birmingham

   Affiliation as printed

   Centre for Human Brain Health, Institute for Mental Health and Centre for Developmental Science, School of Psychology, University of Birmingham, Birmingham B15 2TT, United Kingdom

   Centre for Human Brain Health, Institute for Mental Health and Centre for Developmental Science, School of Psychology, University of Birmingham

6. Ili Ma Aachen Department of Developmental and Educational Psychology Institute of Psychology, Leiden University Leiden Institute for Brain and Cognition

   Leiden University

   Affiliation as printed

   Department of Developmental and Educational Psychology, Institute of Psychology, Leiden University, Leiden 2300, The Netherlands

   Leiden Institute for Brain and Cognition, Leiden 2333, The Netherlands

   Department of Developmental and Educational Psychology, Institute of Psychology, Leiden University

   Leiden Institute for Brain and Cognition

7. Wei Ji Ma

   New York University

   Affiliation as printed

   Center for Neural Science and Department of Psychology, New York University, New York 10003

   Center for Neural Science and Department of Psychology, New York University

8. Sanjay George Manohar

   University of Oxford

   Affiliation as printed

   Department of Experimental Psychology, University of Oxford, Oxford OX2 6GG, United Kingdom

   Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 7JX, United Kingdom

   Department of Experimental Psychology, University of Oxford

   Nuffield Department of Clinical Neurosciences, University of Oxford