Your perspective and my benefit: multiple lesion models of self-other integration strategies during social bargaining.

Recursive social decision-making requires the use of flexible, context-sensitive long-term strategies for negotiation. To succeed in social bargaining, participants' own perspectives must be dynamically integrated with those of interactors to maximize self-benefits and adapt to the other's preferences, respectively. This is a prerequisite to develop a successful long-term self-other integration strategy. While such form of strategic interaction is critical to social decision-making, little is known about its neurocognitive correlates. To bridge this gap, we analysed social bargaining behaviour in relation to its structural neural correlates, ongoing brain dynamics (oscillations and related source space), and functional connectivity signatures in healthy subjects and patients offering contrastive lesion models of neurodegeneration and focal stroke: behavioural variant frontotemporal dementia, Alzheimer's disease, and frontal lesions. All groups showed preserved basic bargaining indexes. However, impaired self-other integration strategy was found in patients with behavioural variant frontotemporal dementia and frontal lesions, suggesting that social bargaining critically depends on the integrity of prefrontal regions. Also, associations between behavioural performance and data from voxel-based morphometry and voxel-based lesion-symptom mapping revealed a critical role of prefrontal regions in value integration and strategic decisions for self-other integration strategy. Furthermore, as shown by measures of brain dynamics and related sources during the task, the self-other integration strategy was predicted by brain anticipatory activity (alpha/beta oscillations with sources in frontotemporal regions) associated with expectations about others' decisions. This pattern was reduced in all clinical groups, with greater impairments in behavioural variant frontotemporal dementia and frontal lesions than Alzheimer's disease. Finally, connectivity analysis from functional magnetic resonance imaging evidenced a fronto-temporo-parietal network involved in successful self-other integration strategy, with selective compromise of long-distance connections in frontal disorders. In sum, this work provides unprecedented evidence of convergent behavioural and neurocognitive signatures of strategic social bargaining in different lesion models. Our findings offer new insights into the critical roles of prefrontal hubs and associated temporo-parietal networks for strategic social negotiation.

[1]  K. Ochsner,et al.  The Need for a Cognitive Neuroscience of Naturalistic Social Cognition , 2009, Annals of the New York Academy of Sciences.

[2]  F. Manes,et al.  Bridging psychiatry and neurology through social neuroscience , 2014, World psychiatry : official journal of the World Psychiatric Association.

[3]  Pablo Billeke,et al.  Oscillatory brain activity correlates with risk perception and predicts social decisions. , 2013, Cerebral cortex.

[4]  Hugues Duffau,et al.  The left inferior fronto-occipital fasciculus subserves language semantics: a multilevel lesion study , 2014, Brain Structure and Function.

[5]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[6]  M. Folstein,et al.  Clinical diagnosis of Alzheimer's disease: Report of the NINCDS—ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease , 2011, Neurology.

[7]  Etienne Koechlin,et al.  Foundations of human reasoning in the prefrontal cortex , 2014, Science.

[8]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[9]  M. Chavez,et al.  Functional Cortical Network in Alpha Band Correlates with Social Bargaining , 2014, PloS one.

[10]  M. Mendez,et al.  Altered emotional morality in frontotemporal dementia , 2009, Cognitive neuropsychiatry.

[11]  N. Schuff,et al.  Different regional patterns of cortical thinning in Alzheimer's disease and frontotemporal dementia. , 2006, Brain : a journal of neurology.

[12]  A. Ibanez,et al.  Detaching from the negative by reappraisal: the role of right superior frontal gyrus (BA9/32) , 2014, Front. Behav. Neurosci..

[13]  J R Hodges,et al.  The prevalence of frontotemporal dementia , 2002, Neurology.

[14]  Sandra E Black,et al.  Salience network resting-state activity: prediction of frontotemporal dementia progression. , 2013, JAMA neurology.

[15]  Daniel Fraiman,et al.  Brain Network Organization and Social Executive Performance in Frontotemporal Dementia , 2016, Journal of the International Neuropsychological Society.

[16]  David Huepe,et al.  Comparing moral judgments of patients with frontotemporal dementia and frontal stroke. , 2014, JAMA neurology.

[17]  Olivier Piguet,et al.  Right anterior temporal lobe dysfunction underlies theory of mind impairments in semantic dementia. , 2014, Brain : a journal of neurology.

[18]  R. Castellani,et al.  Alzheimer disease. , 2010, Disease-a-month : DM.

[19]  D. Tranel,et al.  Irrational Economic Decision-Making after Ventromedial Prefrontal Damage: Evidence from the Ultimatum Game , 2007, The Journal of Neuroscience.

[20]  Théodore Papadopoulo,et al.  The symmetric BEM: bringing in more variables for better accuracy , 2010 .

[21]  Daeyeol Lee Game theory and neural basis of social decision making , 2008, Nature Neuroscience.

[22]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[23]  R. Faber,et al.  Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. , 1999, Neurology.

[24]  J. Hodges,et al.  Behavioural-variant frontotemporal dementia: diagnosis, clinical staging, and management , 2011, The Lancet Neurology.

[25]  O. Sporns Structure and function of complex brain networks , 2013, Dialogues in clinical neuroscience.

[26]  T. Robbins,et al.  Specific cognitive deficits in mild frontal variant frontotemporal dementia. , 1999, Brain : a journal of neurology.

[27]  Théodore Papadopoulo,et al.  Forward Field Computation with OpenMEEG , 2011, Comput. Intell. Neurosci..

[28]  B L Miller,et al.  Patterns of brain atrophy in frontotemporal dementia and semantic dementia , 2002, Neurology.

[29]  J. Hodges,et al.  Common and unique gray matter correlates of episodic memory dysfunction in frontotemporal dementia and alzheimer's disease , 2014, Human brain mapping.

[30]  James K Rilling,et al.  The neural correlates of theory of mind within interpersonal interactions , 2004, NeuroImage.

[31]  J. Morris,et al.  The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer's disease , 2011, Alzheimer's & Dementia.

[32]  D. Cosmelli,et al.  Paradoxical Expectation: Oscillatory Brain Activity Reveals Social Interaction Impairment in Schizophrenia , 2015, Biological Psychiatry.

[33]  Luke Clark,et al.  The contributions of lesion laterality and lesion volume to decision-making impairment following frontal lobe damage , 2003, Neuropsychologia.

[34]  Peter Bossaerts,et al.  Neural correlates of mentalizing-related computations during strategic interactions in humans , 2008, Proceedings of the National Academy of Sciences.

[35]  Adolfo M García,et al.  The Social Context Network Model in Psychiatric and Neurological Diseases. , 2016, Current topics in behavioral neurosciences.

[36]  H. Obrig,et al.  Lesion correlates of patholinguistic profiles in chronic aphasia: comparisons of syndrome-, modality- and symptom-level assessment. , 2014, Brain : a journal of neurology.

[37]  Philipp Kanske,et al.  Integration of Intention and Outcome for Moral Judgment in Frontotemporal Dementia: Brain Structural Signatures , 2016, Neurodegenerative Diseases.

[38]  Timothy Edward John Behrens,et al.  Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour , 2007, Trends in Cognitive Sciences.

[39]  S. Petersen,et al.  A dual-networks architecture of top-down control , 2008, Trends in Cognitive Sciences.

[40]  Alfonso Caramazza,et al.  Distinct Regions of Right Temporal Cortex Are Associated with Biological and Human–Agent Motion: Functional Magnetic Resonance Imaging and Neuropsychological Evidence , 2013, The Journal of Neuroscience.

[41]  Ana Solodkin,et al.  Pathology of the Insular Cortex in Alzheimer Disease Depends on Cortical Architecture , 2005, Journal of neuropathology and experimental neurology.

[42]  M. Delgado,et al.  Perceptions of moral character modulate the neural systems of reward during the trust game , 2005, Nature Neuroscience.

[43]  E. Bullmore,et al.  Brain mechanisms of successful compensation during learning in Alzheimer disease , 2006, Neurology.

[44]  Agustín Ibáñez,et al.  Cortical dynamics and subcortical signatures of motor-language coupling in Parkinson’s disease , 2015, Scientific Reports.

[45]  Daniel Fraiman,et al.  Stroke and Neurodegeneration Induce Different Connectivity Aberrations in the Insula , 2015, Stroke.

[46]  Andrew N. Meltzoff,et al.  The neural bases of cooperation and competition: an fMRI investigation , 2004, NeuroImage.

[47]  G. Fink,et al.  Connectivity-based approaches in stroke and recovery of function , 2014, The Lancet Neurology.

[48]  Facundo Manes,et al.  A neuropsychological battery to detect specific executive and social cognitive impairments in early frontotemporal dementia. , 2009, Brain : a journal of neurology.

[49]  Colin Camerer,et al.  Empathic choice involves vmPFC value signals that are modulated by social processing implemented in IPL. , 2013, Social cognitive and affective neuroscience.

[50]  A. Bechara Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective , 2005, Nature Neuroscience.

[51]  P. Montague,et al.  Neuroeconomic Approaches to Mental Disorders , 2010, Neuron.

[52]  M. Shadlen,et al.  Representation of Confidence Associated with a Decision by Neurons in the Parietal Cortex , 2009, Science.

[53]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[54]  Timothy E. J. Behrens,et al.  An Agent Independent Axis for Executed and Modeled Choice in Medial Prefrontal Cortex , 2013, Neuron.

[55]  Daeyeol Lee,et al.  Ubiquity and Specificity of Reinforcement Signals throughout the Human Brain , 2011, Neuron.

[56]  Daniel T. Knoepfle,et al.  Value Computations in Ventral Medial Prefrontal Cortex during Charitable Decision Making Incorporate Input from Regions Involved in Social Cognition , 2010, The Journal of Neuroscience.

[57]  H. Karnath,et al.  Using human brain lesions to infer function: a relic from a past era in the fMRI age? , 2004, Nature Reviews Neuroscience.

[58]  Facundo Manes,et al.  Contextual social cognition and the behavioral variant of frontotemporal dementia , 2012, Neurology.

[59]  B. Miller,et al.  Neurodegenerative Diseases Target Large-Scale Human Brain Networks , 2009, Neuron.

[60]  T. Robbins,et al.  Risk-Sensitive Decision-Making in Patients with Posterior Parietal and Ventromedial Prefrontal Cortex Injury , 2013, Cerebral cortex.

[61]  J. Decety,et al.  Integrating intention and context: assessing social cognition in adults with Asperger syndrome , 2012, Front. Hum. Neurosci..

[62]  Michael P. Milham,et al.  Distinct neural mechanisms of risk and ambiguity: A meta-analysis of decision-making , 2006, NeuroImage.

[63]  M. Stallen,et al.  The Cooperative Brain , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[64]  Mark D'Esposito,et al.  The salience network causally influences default mode network activity during moral reasoning. , 2013, Brain : a journal of neurology.

[65]  Srivas Chennu,et al.  Predictive coding in autism spectrum disorder and attention deficit hyperactivity disorder. , 2015, Journal of neurophysiology.

[66]  E. Fehr,et al.  The neurobiology of rewards and values in social decision making , 2014, Nature Reviews Neuroscience.

[67]  P. Montague,et al.  Neuroeconomics: A Bridge for Translational Research , 2012, Biological Psychiatry.

[68]  P. Glimcher,et al.  The Neurobiology of Decision: Consensus and Controversy , 2009, Neuron.

[69]  Facundo Manes,et al.  Orbitofrontal and limbic signatures of empathic concern and intentional harm in the behavioral variant frontotemporal dementia , 2016, Cortex.

[70]  Laura Moretti,et al.  Reward and Social Valuation Deficits following Ventromedial Prefrontal Damage , 2009, Journal of Cognitive Neuroscience.

[71]  Anders M. Dale,et al.  The Challenge of Connecting the Dots in the B.R.A.I.N. , 2013, Neuron.

[72]  S. Baez,et al.  Feeling, learning from and being aware of inner states: interoceptive dimensions in neurodegeneration and stroke , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[73]  R. Buckner Memory and Executive Function in Aging and AD Multiple Factors that Cause Decline and Reserve Factors that Compensate , 2004, Neuron.

[74]  C. Derouesné [Mini-mental state examination]. , 2001, Revue neurologique.

[75]  J. Hodges,et al.  Fair play: social norm compliance failures in behavioural variant frontotemporal dementia. , 2016, Brain : a journal of neurology.

[76]  Colin Camerer,et al.  Neural signatures of strategic types in a two-person bargaining game , 2010, Proceedings of the National Academy of Sciences.

[77]  Matthew F S Rushworth,et al.  The Computation of Social Behavior , 2009, Science.

[78]  Monique Ernst,et al.  Decision-making in a Risk-taking Task: A PET Study , 2002, Neuropsychopharmacology.

[79]  Nick C Fox,et al.  Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. , 2011, Brain : a journal of neurology.

[80]  Giorgio Coricelli,et al.  The neuroeconomics of strategic interaction , 2015, Current Opinion in Behavioral Sciences.

[81]  Jonathan D. Power,et al.  Multi-task connectivity reveals flexible hubs for adaptive task control , 2013, Nature Neuroscience.

[82]  Daniel L. Rubin,et al.  Network Analysis of Intrinsic Functional Brain Connectivity in Alzheimer's Disease , 2008, PLoS Comput. Biol..

[83]  M. Albert,et al.  Medial temporal lobe function and structure in mild cognitive impairment , 2004, Annals of neurology.

[84]  T. Torralva,et al.  Impairments of Social Cognition and Decision Making in Alzheimer's Disease , 2000, International Psychogeriatrics.

[85]  Houeto Jean-Luc [Parkinson's disease]. , 2022, La Revue du praticien.

[86]  G. Glover,et al.  Methods and Software for fMRI Analysis of Clinical Subjects , 2009, NeuroImage.

[87]  E. Fehr,et al.  Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice , 2011, Nature Neuroscience.

[88]  J. Gläscher,et al.  Lesion mapping of cognitive control and value-based decision making in the prefrontal cortex , 2012, Proceedings of the National Academy of Sciences.

[89]  T. Robbins,et al.  Decision-making processes following damage to the prefrontal cortex. , 2002, Brain : a journal of neurology.

[90]  Hervé Abdi,et al.  Optimizing preprocessing and analysis pipelines for single‐subject fMRI. I. Standard temporal motion and physiological noise correction methods , 2012, Human brain mapping.

[91]  Jason P. Mitchell,et al.  Equitable decision making is associated with neural markers of intrinsic value , 2011, Proceedings of the National Academy of Sciences.

[92]  Rodrigo Ortega,et al.  From neural signatures of emotional modulation to social cognition: individual differences in healthy volunteers and psychiatric participants. , 2014, Social cognitive and affective neuroscience.

[93]  Colin Camerer,et al.  Economic Games Quantify Diminished Sense of Guilt in Patients with Damage to the Prefrontal Cortex , 2009, The Journal of Neuroscience.

[94]  S. Huettel,et al.  Functional connectivity with ventromedial prefrontal cortex reflects subjective value for social rewards. , 2014, Social cognitive and affective neuroscience.

[95]  A. Reiss,et al.  Aberrant face and gaze habituation in fragile x syndrome. , 2014, American Journal of Psychiatry.

[96]  G. Busatto,et al.  Neurostructural predictors of Alzheimer's disease: A meta-analysis of VBM studies , 2011, Neurobiology of Aging.

[97]  Charles DeCarli,et al.  Diagnostic Criteria for the Behavioral Variant of Frontotemporal Dementia (bvFTD): Current Limitations and Future Directions , 2007, Alzheimer disease and associated disorders.

[98]  J. Hodges,et al.  Money for nothing — Atrophy correlates of gambling decision making in behavioural variant frontotemporal dementia and Alzheimer's disease☆ , 2013, NeuroImage: Clinical.

[99]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[100]  U. Fischbacher,et al.  The Neural Signature of Social Norm Compliance , 2007, Neuron.

[101]  M. Delazer,et al.  Impact of ambiguity and risk on decision making in mild Alzheimer's disease , 2008, Neuropsychologia.

[102]  S. Baez,et al.  The effects of context processing on social cognition impairments in adults with Asperger's syndrome , 2014, Front. Neurosci..

[103]  F. Aboitiz,et al.  Temporal Constraints of Behavioral Inhibition: Relevance of Inter-stimulus Interval in a Go-Nogo Task , 2014, PloS one.

[104]  H. Seo,et al.  Neural Basis of Strategic Decision Making , 2016, Trends in Neurosciences.

[105]  R. Nagel,et al.  Neural correlates of depth of strategic reasoning in medial prefrontal cortex , 2009, Proceedings of the National Academy of Sciences.

[106]  E. Brunner,et al.  The Nonparametric Behrens‐Fisher Problem: Asymptotic Theory and a Small‐Sample Approximation , 2000 .

[107]  T. Shallice,et al.  Response suppression, initiation and strategy use following frontal lobe lesions , 1996, Neuropsychologia.

[108]  Robert T. Knight,et al.  Selective impairment of reasoning about social exchange in a patient with bilateral limbic system damage , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[109]  F. Manes,et al.  The role of social cognition in moral judgment in frontotemporal dementia , 2011, Social neuroscience.

[110]  Alan C. Evans,et al.  Focal decline of cortical thickness in Alzheimer's disease identified by computational neuroanatomy. , 2004, Cerebral cortex.

[111]  James B. Rowe,et al.  Magnetoencephalography of frontotemporal dementia: spatiotemporally localized changes during semantic decisions. , 2011, Brain : a journal of neurology.

[112]  J R Hodges,et al.  Understanding social dysfunction in the behavioural variant of frontotemporal dementia: the role of emotion and sarcasm processing. , 2009, Brain : a journal of neurology.

[113]  D. Cosmelli,et al.  Someone has to give in: theta oscillations correlate with adaptive behavior in social bargaining. , 2014, Social cognitive and affective neuroscience.

[114]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[115]  Matthew L Senjem,et al.  Distinct anatomical subtypes of the behavioural variant of frontotemporal dementia: a cluster analysis study. , 2009, Brain : a journal of neurology.

[116]  J. Mattingley,et al.  Dynamic cooperation and competition between brain systems during cognitive control , 2013, Trends in Cognitive Sciences.

[117]  Matthias Brand,et al.  Neuropsychological correlates of decision-making in ambiguous and risky situations , 2006, Neural Networks.

[118]  David Huepe,et al.  What event-related potentials (ERPs) bring to social neuroscience? , 2012, Social neuroscience.

[119]  J. Decety,et al.  Primary empathy deficits in frontotemporal dementia , 2014, Front. Aging Neurosci..

[120]  Laura Moretti,et al.  Theta signal as the neural signature of social exclusion. , 2013, Cerebral cortex.

[121]  John R Hodges,et al.  The Addenbrooke's Cognitive Examination Revised (ACE‐R): a brief cognitive test battery for dementia screening , 2006, International journal of geriatric psychiatry.

[122]  Michael W. Weiner,et al.  Neural basis of interpersonal traits in neurodegenerative diseases , 2009, Neuropsychologia.

[123]  A. Sanfey Social Decision-Making : Insights from Game Theory and Neuroscience , 2022 .

[124]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[125]  R. Saxe Uniquely human social cognition , 2006, Current Opinion in Neurobiology.

[126]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[127]  Daeyeol Lee,et al.  Neural basis of learning and preference during social decision-making , 2012, Current Opinion in Neurobiology.

[128]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[129]  C. Oppenheim,et al.  Diffusion tensor imaging in early Alzheimer's disease , 2006, Psychiatry Research: Neuroimaging.

[130]  Fabricio Baglivo,et al.  Early detection of intentional harm in the human amygdala. , 2016, Brain : a journal of neurology.

[131]  Richard M. Leahy,et al.  Electromagnetic brain mapping , 2001, IEEE Signal Process. Mag..

[132]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[133]  Chris Rorden,et al.  Improving Lesion-Symptom Mapping , 2007, Journal of Cognitive Neuroscience.

[134]  Karalyn Patterson,et al.  Taking both sides: do unilateral anterior temporal lobe lesions disrupt semantic memory? , 2010, Brain : a journal of neurology.

[135]  Facundo Manes,et al.  Decision-making cognition in neurodegenerative diseases , 2010, Nature Reviews Neurology.

[136]  Pablo López,et al.  INECO Frontal Screening (IFS): A brief, sensitive, and specific tool to assess executive functions in dementia–CORRECTED VERSION , 2009, Journal of the International Neuropsychological Society.

[137]  Cendri A. C. Hutcherson,et al.  A Neurocomputational Model of Altruistic Choice and Its Implications , 2015, Neuron.

[138]  F. Manes,et al.  Decision-Making in Frontotemporal Dementia: Clinical, Theoretical and Legal Implications , 2011, Dementia and Geriatric Cognitive Disorders.

[139]  H. Braak,et al.  Neuropathological stageing of Alzheimer-related changes , 2004, Acta Neuropathologica.

[140]  Seppo P. Ahlfors,et al.  Assessing and improving the spatial accuracy in MEG source localization by depth-weighted minimum-norm estimates , 2006, NeuroImage.

[141]  Jonathan D. Cohen,et al.  The Neural Basis of Economic Decision-Making in the Ultimatum Game , 2003, Science.

[142]  S. Baez,et al.  Structural neuroimaging of social cognition in progressive non-fluent aphasia and behavioral variant of frontotemporal dementia , 2013, Front. Hum. Neurosci..

[143]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .