Social and Nonsocial Relational Reasoning in Adolescence and Adulthood

Reasoning during social interactions requires the individual manipulation of mental representations of one's own traits and those of other people as well as their joint consideration (relational integration). Research using nonsocial paradigms has linked relational integration to activity in the rostrolateral PFC. Here, we investigated whether social reasoning is supported by the same general system or whether it additionally relies on regions of the social brain network, such as the medial PFC. We further assessed the development of social reasoning. In the social task, participants evaluated themselves or a friend, or compared themselves with their friend, on a series of traits. In the nonsocial task, participants evaluated their hometown or another town or compared the two. In a behavioral study involving 325 participants (11–39 years old), we found that integrating relations, compared with performing single relational judgments, improves during adolescence, both for social and nonsocial information. Thirty-nine female participants (10–31 years old) took part in a neuroimaging study using a similar task. Activation of the relational integration network, including the rostrolateral PFC, was observed in the comparison condition of both the social and nonsocial tasks, whereas the medial PFC showed greater activation when participants processed social as opposed to nonsocial information across conditions. Developmentally, the right anterior insula showed greater activity in adolescents compared with adults during the comparison of nonsocial versus social information. This study shows parallel recruitment of the social brain and the relational reasoning network during the relational integration of social information in adolescence and adulthood.

[1]  T. Robbins,et al.  Decision-making in the adolescent brain , 2012, Nature Neuroscience.

[2]  Iroise Dumontheil,et al.  Social cognition and abstract thought in adolescence: the role of structural and functional development in rostral prefrontal cortex , 2012 .

[3]  Iroise Dumontheil,et al.  Development of rostral prefrontal cortex and cognitive and behavioural disorders , 2008, Developmental medicine and child neurology.

[4]  Armin Raznahan,et al.  How Does Your Cortex Grow? , 2011, The Journal of Neuroscience.

[5]  J. Decety,et al.  Effect of subjective perspective taking during simulation of action: a PET investigation of agency , 2001, Nature Neuroscience.

[6]  K. Sundet,et al.  PSYCHOMETRIC PROPERTIES OF A NORWEGIAN RESEARCH VERSION OF THE 'WECHSLER ABBREVIATED SCALE OF INTELLIGENCE' (WASI) , 2001 .

[7]  S. Blakemore,et al.  Developmental changes in the structure of the social brain in late childhood and adolescence. , 2014, Social cognitive and affective neuroscience.

[8]  Nadim Joni Shah,et al.  Neural Representations of Self versus Other: Visual-Spatial Perspective Taking and Agency in a Virtual Ball-tossing Game , 2006, Journal of Cognitive Neuroscience.

[9]  S. Blakemore The social brain in adolescence , 2008, Nature Reviews Neuroscience.

[10]  K. Zilles,et al.  Neural Correlates of First-Person Perspective as One Constituent of Human Self-Consciousness , 2004, Journal of Cognitive Neuroscience.

[11]  Carter Wendelken,et al.  Left, but not right, rostrolateral prefrontal cortex meets a stringent test of the relational integration hypothesis , 2009, NeuroImage.

[12]  Stephen Lawrie,et al.  Functional Specialization within Rostral Prefrontal Cortex (Area 10): A Meta-analysis , 2006, Journal of Cognitive Neuroscience.

[13]  Matthew D. Lieberman,et al.  Social working memory and its distinctive link to social cognitive ability: an fMRI study. , 2015, Social cognitive and affective neuroscience.

[14]  Iroise Dumontheil,et al.  Development of relational reasoning during adolescence. , 2010, Developmental science.

[15]  John O. Willis,et al.  Wechsler Abbreviated Scale of Intelligence , 2014 .

[16]  Iroise Dumontheil,et al.  Developmental changes in effective connectivity associated with relational reasoning , 2014, Human brain mapping.

[17]  Deborah A Yurgelun-Todd,et al.  Cognitive and Emotional Components of Frontal Lobe Functioning in Childhood and Adolescence , 2004, Annals of the New York Academy of Sciences.

[18]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[19]  Bonnie J Nagel,et al.  The impact of sex, puberty, and hormones on white matter microstructure in adolescents. , 2012, Cerebral cortex.

[20]  David Badre,et al.  Analogical reasoning and prefrontal cortex: evidence for separable retrieval and integration mechanisms. , 2004, Cerebral cortex.

[21]  Carter Wendelken,et al.  Transitive Inference: Distinct Contributions of Rostrolateral Prefrontal Cortex and the Hippocampus , 2010, Journal of Cognitive Neuroscience.

[22]  Meghan L. Meyer,et al.  Preliminary investigation of the influence of dopamine regulating genes on social working memory , 2014, Social neuroscience.

[23]  E. Crone,et al.  Understanding adolescence as a period of social–affective engagement and goal flexibility , 2012, Nature Reviews Neuroscience.

[24]  Iroise Dumontheil,et al.  Influence of the COMT Genotype on Working Memory and Brain Activity Changes During Development , 2011, Biological Psychiatry.

[25]  Kalina Christoff,et al.  Localizing the rostrolateral prefrontal cortex at the individual level , 2007, NeuroImage.

[26]  Carter Wendelken,et al.  Neurocognitive development of relational reasoning. , 2009, Developmental science.

[27]  Emilio Ferrer,et al.  Neural Correlates of Fluid Reasoning in Children and Adults , 2007, Frontiers in human neuroscience.

[28]  C. Wendelken,et al.  Rostrolateral prefrontal cortex: Domain‐general or domain‐sensitive? , 2012, Human brain mapping.

[29]  Cameron S. Carter,et al.  Brain Is to Thought as Stomach Is to ??: Investigating the Role of Rostrolateral Prefrontal Cortex in Relational Reasoning , 2008, Journal of Cognitive Neuroscience.

[30]  James K. Kroger,et al.  Rostrolateral Prefrontal Cortex Involvement in Relational Integration during Reasoning , 2001, NeuroImage.

[31]  Sarah-Jayne Blakemore,et al.  The development of social cognition in adolescence: An integrated perspective , 2016, Neuroscience & Biobehavioral Reviews.

[32]  Paul Irwing,et al.  Sex differences on the progressive matrices: A meta-analysis. , 2004 .

[33]  Emilio Ferrer,et al.  Fluid Reasoning and the Developing Brain , 2009, Frontiers in neuroscience.

[34]  Sarah-Jayne Blakemore,et al.  Is there heightened sensitivity to social reward in adolescence? , 2016, Current Opinion in Neurobiology.

[35]  Tony Charman,et al.  Is there a Gender Difference in False Belief Development , 2002 .

[36]  Ana Raposo,et al.  Contributions of frontopolar cortex to judgments about self, others and relations. , 2011, Social cognitive and affective neuroscience.

[37]  J. Grafman,et al.  Human prefrontal cortex: processing and representational perspectives , 2003, Nature Reviews Neuroscience.

[38]  Gereon R Fink,et al.  Differential involvement of the posterior temporal cortex in mentalizing but not perspective taking. , 2008, Social cognitive and affective neuroscience.

[39]  Perrine Ruby,et al.  Distinct Regions of the Medial Prefrontal Cortex Are Associated with Self-referential Processing and Perspective Taking , 2007, Journal of Cognitive Neuroscience.

[40]  J. Decety,et al.  How Would You Feel versus How Do You Think She Would Feel? A Neuroimaging Study of Perspective-Taking with Social Emotions , 2004, Journal of Cognitive Neuroscience.

[41]  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.

[42]  Jonathan D. Power,et al.  Statistical improvements in functional magnetic resonance imaging analyses produced by censoring high‐motion data points , 2014, Human brain mapping.

[43]  Josef Perner,et al.  Do visual perspective tasks need theory of mind? , 2006, NeuroImage.

[44]  Hanneke E. M. den Ouden,et al.  Thinking about intentions , 2005, NeuroImage.

[45]  Sarah-Jayne Blakemore,et al.  Development of the social brain in adolescence , 2012, Journal of the Royal Society of Medicine.

[46]  Jessica A. Sommerville,et al.  Shared representations between self and other: a social cognitive neuroscience view , 2003, Trends in Cognitive Sciences.

[47]  Evelyn C. Ferstl,et al.  Functional specialization within the anterior medial prefrontal cortex: a functional magnetic resonance imaging study with human subjects , 2003, Neuroscience Letters.

[48]  Elliot T. Berkman,et al.  Evidence for social working memory from a parametric functional MRI study , 2012, Proceedings of the National Academy of Sciences.

[49]  Mark H. Davis,et al.  A Multidimensional Approach to Individual Differences in Empathy , 1980 .

[50]  Iroise Dumontheil,et al.  Influence of COMT genotype and affective distractors on the processing of self-generated thought , 2014, Social cognitive and affective neuroscience.

[51]  Matthew D. Lieberman,et al.  The neural correlates of implicit and explicit self-relevant processing , 2010, NeuroImage.

[52]  J. Raven,et al.  Manual for Raven's progressive matrices and vocabulary scales , 1962 .

[53]  Kirstie J. Whitaker,et al.  Increased Functional Selectivity over Development in Rostrolateral Prefrontal Cortex , 2011, The Journal of Neuroscience.

[54]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[55]  C. Frith,et al.  Development and neurophysiology of mentalizing. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[56]  Iroise Dumontheil,et al.  Development of abstract thinking during childhood and adolescence: The role of rostrolateral prefrontal cortex , 2014, Developmental Cognitive Neuroscience.

[57]  Emilio Ferrer,et al.  Fronto-Parietal Network Reconfiguration Supports the Development of Reasoning Ability. , 2016, Cerebral cortex.

[58]  Debra A. Gusnard,et al.  Being a self: Considerations from functional imaging , 2005, Consciousness and Cognition.

[59]  James K. Kroger,et al.  Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: a parametric study of relational complexity. , 2002, Cerebral cortex.

[60]  Iroise Dumontheil,et al.  Developmental Differences in the Control of Action Selection by Social Information , 2012, Journal of Cognitive Neuroscience.

[61]  F. Overwalle Social cognition and the brain: a meta-analysis. , 2009 .