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A common neural system mediating two different forms of social judgement

Published online by Cambridge University Press:  08 October 2009

J. Hall*
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
H. C. Whalley
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
J. W. McKirdy
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
R. Sprengelmeyer
Affiliation:
School of Psychology, University of St Andrews, St Andrews, UK
I. M. Santos
Affiliation:
Department of Educational Sciences, University of Aveiro, Campus Universitario de Santiago, Aveiro, Portugal
D. I. Donaldson
Affiliation:
Psychology Department, University of Stirling, Stirling, UK
D. J. McGonigle
Affiliation:
Schools of Psychology and Biosciences, University of Cardiff, Cardiff, UK
A. W. Young
Affiliation:
Department of Psychology and York Neuroimaging Centre, University of York, York, UK
A. M. McIntosh
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
E. C. Johnstone
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
S. M. Lawrie
Affiliation:
Division of Psychiatry, University of Edinburgh, Edinburgh, UK
*
*Address for correspondence: Dr J. Hall, Division of Psychiatry, University of Edinburgh, Kennedy Tower, Royal Edinburgh Hospital, EdinburghEH10 5HF, UK. (Email: [email protected])

Abstract

Background

A wide range of neuropsychiatric conditions, including schizophrenia and autistic spectrum disorder (ASD), are associated with impairments in social function. Previous studies have shown that individuals with schizophrenia and ASD have deficits in making a wide range of social judgements from faces, including decisions related to threat (such as judgements of approachability) and decisions not related to physical threat (such as judgements of intelligence). We have investigated healthy control participants to see whether there is a common neural system activated during such social decisions, on the basis that deficits in this system may contribute to the impairments seen in these disorders.

Method

We investigated the neural basis of social decision making during judgements of approachability and intelligence from faces in 24 healthy participants using functional magnetic resonance imaging (fMRI). We used conjunction analysis to identify common brain regions activated during both tasks.

Results

Activation of the amygdala, medial prefrontal cortex, inferior prefrontal cortex and cerebellum was seen during performance of both social tasks, compared to simple gender judgements from the same stimuli. Task-specific activations were present in the dorsolateral prefrontal cortex in the intelligence task and in the inferior and middle temporal cortex in the approachability task.

Conclusions

The present study identified a common network of brain regions activated during the performance of two different forms of social judgement from faces. Dysfunction of this network is likely to contribute to the broad-ranging deficits in social function seen in psychiatric disorders such as schizophrenia and ASD.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2009

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References

Abdi, Z, Sharma, T (2004). Social cognition and its neural correlates in schizophrenia and autism. CNS Spectrums 9, 335343.CrossRefGoogle ScholarPubMed
Adolphs, R (2003). Cognitive neuroscience of human social behaviour. Nature Reviews Neuroscience 4, 165178.CrossRefGoogle ScholarPubMed
Adolphs, R, Baron-Cohen, S, Tranel, D (2002). Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience 14, 12641274.CrossRefGoogle ScholarPubMed
Adolphs, R, Sears, L, Piven, J (2001). Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience 13, 232240.CrossRefGoogle ScholarPubMed
Adolphs, R, Spezio, M (2006). Role of the amygdala in processing visual social stimuli. Progress in Brain Research 156, 363378.CrossRefGoogle ScholarPubMed
Adolphs, R, Tranel, D, Damasio, AR (1998). The human amygdala in social judgment. Nature 393, 470474.CrossRefGoogle ScholarPubMed
Adolphs, R, Tranel, D, Damasio, H, Damasio, A (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature 372, 669672.CrossRefGoogle Scholar
Adolphs, R, Tranel, D, Hamann, S, Young, AW, Calder, AJ, Phelps, EA, Anderson, A, Lee, GP, Damasio, AR (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia 37, 11111119.CrossRefGoogle ScholarPubMed
Amaral, DG, Schumann, CM, Nordahl, CW (2008). Neuroanatomy of autism. Trends in Neurosciences 31, 137145.CrossRefGoogle ScholarPubMed
Amodio, DM, Frith, CD (2006). Meeting of minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience 7, 268277.CrossRefGoogle ScholarPubMed
APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Press: Washington, DC.Google Scholar
Baas, D, Aleman, A, Vink, M, Ramsey, NF, de Haan, EHF, Kahn, RS (2008 a). Evidence of altered cortical and amygdala activation during social decision-making in schizophrenia. NeuroImage 40, 719727.CrossRefGoogle ScholarPubMed
Baas, D, van't Wout, M, Aleman, A, Kahn, RS (2008 b). Social judgement in clinically stable patients with schizophrenia and healthy relatives: behavioural evidence of social brain dysfunction. Psychological Medicine 38, 747754.CrossRefGoogle ScholarPubMed
Baron-Cohen, S, Ring, HA, Wheelwright, S, Bullmore, ET, Brammer, MJ, Simmons, A, Williams, SC (1999). Social intelligence in the normal and autistic brain: an fMRI study. European Journal of Neuroscience 11, 18911898.CrossRefGoogle Scholar
Baron-Cohen, S, Wheelwright, S, Hill, J, Raste, Y, Plumb, I (2001). The ‘Reading the Mind in the Eyes’ Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry 42, 241251.CrossRefGoogle ScholarPubMed
Breiter, HC, Etcoff, NL, Whalen, PJ, Kennedy, WA, Rauch, SL, Buckner, RL, Strauss, MM, Hyman, SE, Rosen, BR (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron 17, 875887.CrossRefGoogle ScholarPubMed
Brothers, L (1990). The social brain: a project for integrating primate behaviour and neurophysiology in a new domain. Concepts in Neuroscience 1, 2751.Google Scholar
Brunet, E, Sarfati, Y, Hardy-Bayle, M-C, Decety, J (2000). A PET investigation of the attribution of intentions with a nonverbal task. NeuroImage 11, 157166.CrossRefGoogle ScholarPubMed
Brunet-Gouet, E, Decety, J (2006). Social brain dysfunctions in schizophrenia: a review of neuroimaging studies. Psychiatry Research: Neuroimaging 148, 7592.CrossRefGoogle ScholarPubMed
Bush, G, Luu, P, Posner, MI (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Sciences 4, 215222.CrossRefGoogle ScholarPubMed
Calarge, C, Andreasen, NC, O'Leary, DS (2003). Visualizing how one brain understands another: a PET study of theory of mind. American Journal of Psychiatry 160, 19541964.CrossRefGoogle ScholarPubMed
Carr, L, Iacoboni, M, Dubeau, M-C, Mazziotta, JC, Lenzi, GL (2003). Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Sciences USA 100, 54975502.Google Scholar
Celani, G, Battacchi, MW, Arcidiacono, L (1999). The understanding of the emotional meaning of facial expressions in people with autism. Journal of Autism and Developmental Disorders 29, 5766.CrossRefGoogle ScholarPubMed
Craig, AD (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nature Reviews Neuroscience 3, 655666.CrossRefGoogle Scholar
Darwin, C (1872). The Expression of the Emotions in Man and Animals. John Murray: London.CrossRefGoogle Scholar
Decety, J, Chaminade, T (2003). Neural correlates of feeling sympathy. Neuropsychologia 41, 127138.CrossRefGoogle ScholarPubMed
Dolan, RJ, Vuilleumier, P (2003). Amygdala automaticity in emotional processing. Annals of the New York Academy of Sciences 985, 348355.CrossRefGoogle ScholarPubMed
Edwards, J, Jackson, HJ, Pattison, PE (2002). Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clinical Psychology Review 22, 789832.CrossRefGoogle ScholarPubMed
Fine, C, Lumsden, J, Blair, RJR (2001). Dissociation between ‘theory of mind’ and executive functions in a patient with early left amygdala damage. Brain 124, 287298.Google Scholar
Gallagher, HL, Frith, CD (2003). Functional imaging of ‘theory of mind’. Trends in Cognitive Sciences 7, 7783.Google Scholar
Gallese, V, Keysers, C, Rizzolatti, G (2004). A unifying view of the basis of social cognition. Trends in Cognitive Sciences 8, 396403.CrossRefGoogle ScholarPubMed
Hall, J, Harris, JM, Sprengelmeyer, R, Sprengelmeyer, A, Young, AW, Santos, IM, Johnstone, EC, Lawrie, SM (2004). Social cognition and face processing in schizophrenia. British Journal of Psychiatry 185, 169170.CrossRefGoogle ScholarPubMed
Haxby, JV, Hoffman, EA, Gobbini, MI (2000). The distributed human neural system for face perception. Trends in Cognitive Sciences 4, 223233.CrossRefGoogle ScholarPubMed
Haxby, JV, Hoffman, EA, Gobbini, MI (2002). Human neural systems for face recognition and social communication. Biological Psychiatry 51, 5967.CrossRefGoogle ScholarPubMed
Hobson, RP, Ouston, J, Lee, A (1988). What's in a face? The case of autism. British Journal of Psychology 79, 441453.CrossRefGoogle Scholar
Howard, MA, Cowell, PE, Boucher, J, Broks, P, Mayes, A, Farrant, A, Roberts, N (2000). Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport 11, 29312935.Google Scholar
Kim, J-W, Kim, J-J, Jeong, BS, Ki, SW, Im, D-M, Lee, SJ, Lee, HS (2005). Neural mechanism for judging the appropriateness of facial affect. Cognitive Brain Research 25, 659667.CrossRefGoogle ScholarPubMed
Kling, AS, Brothers, L (1992). The amygdala and social behaviour. In The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction (ed. Aggleton, J.), pp. 353377. Wiley-Liss: New York.Google Scholar
Mah, L, Arnold, MC, Grafman, J (2004). Impairment of social perception associated with lesions of the prefrontal cortex. American Journal of Psychiatry 161, 12471255.CrossRefGoogle ScholarPubMed
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19, 12331239.Google Scholar
Mandal, MK, Pandey, R, Prasad, AB (1998). Facial expressions of emotions and schizophrenia: a review. Schizophrenia Bulletin 24, 399412.CrossRefGoogle ScholarPubMed
Marwick, K, Hall, J (2008). Social cognition in schizophrenia: a review of face processing. British Medical Bulletin 88, 4358.CrossRefGoogle ScholarPubMed
Morris, JS, Frith, CD, Perrett, DI, Rowland, D, Young, AW, Calder, AJ, Dolan, RJ (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 383, 812815.Google Scholar
Nichols, T, Brett, M, Andersson, J, Wager, T, Poline, J-B (2005). Valid conjunction inference with the minimum statistic. NeuroImage 25, 653660.CrossRefGoogle ScholarPubMed
Pelphrey, KA, Sasson, NA, Reznick, JS, Paul, G, Goldman, BD, Piven, J (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders 32, 249261.Google Scholar
Philip, RCM, Whalley, HC, Stanfield, AC, Sprengelmeyer, R, Santos, I, Young, AW, Atkinson, AP, Dittrich, WH, Calder, AJ, Johnstone, EC, Lawrie, SM, Hall, J (in press). Deficits in facial, body movement and vocal emotional processing in autistic spectrum disorder. Psychological Medicine.Google Scholar
Pinkham, AE, Hopfinger, JB, Pelphrey, KA, Piven, J, Penn, DL (2008). Neural bases for impaired social cognition in schizophrenia and autism spectrum disorders. Schizophrenia Research 99, 164175.Google Scholar
Pinkham, AE, Penn, DL, Perkins, DO, Lieberman, J (2003). Implications for the neural basis of social cognition for the study of schizophrenia. American Journal of Psychiatry 160, 815824.Google Scholar
Rizzolatti, G, Craighero, L (2004). The mirror-neuron system. Annual Review of Neuroscience 27, 169192.CrossRefGoogle ScholarPubMed
Russell, TA, Rubia, K, Bullmore, ET, Soni, W, Suckling, J, Brammer, MJ, Simmons, A, Williams, SCR, Sharma, T (2000). Exploring the social brain in schizophrenia: left prefrontal underactivation during mental state attribution. American Journal of Psychiatry 157, 20402042.Google Scholar
Santos, I (2003). Perception of social characteristics from faces. PhD thesis, University of York, UK.Google Scholar
Santos, I, Young, AW (2008). Effects of inversion and negation on social inferences from faces. Perception 37, 10611078.Google Scholar
Schmahmann, JD (2004). Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. Journal of Neuropsychiatry and Clinical Neurosciences 16, 367378.Google Scholar
Schmahmann, JD, Sherman, JC (1998). The cerebellar cognitive affective syndrome. Brain 121, 561579.Google Scholar
Shaw, P, Bramham, J, Lawrence, EJ, Morris, R, Baron-Cohen, S, David, AS (2005). Differential effects of lesions of the amygdala and prefrontal cortex on recognizing facial expressions of complex emotions. Journal of Cognitive Neuroscience 17, 14101419.CrossRefGoogle ScholarPubMed
Singer, T, Kiebel, SJ, Winston, JS, Dolan, RJ, Frith, CD (2004). Brain responses to the acquired moral status of faces. Neuron 41, 653662.CrossRefGoogle Scholar
Steele, JD, Lawrie, SM (2004). Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis. NeuroImage 21, 868875.Google Scholar
Stone, VE, Baron-Cohen, S, Calder, A, Keane, J, Young, A (2003). Acquired theory of mind impairments in individuals with bilateral amygdala lesions. Neuropsychologia 41, 209220.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273289.CrossRefGoogle ScholarPubMed
Vollm, BA, Taylor, ANW, Richardson, P, Corcoran, R, Stirling, J, McKie, S, Deakin, JFW, Elliott, R (2006). Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. NeuroImage 29, 9098.CrossRefGoogle Scholar
Winston, JS, O'Doherty, J, Kilner, JM, Perrett, DI, Dolan, RJ (2007). Brain systems for assessing facial attractiveness. Neuropsychologia 45, 195206.CrossRefGoogle ScholarPubMed
Winston, JS, Strange, BA, O'Doherty, J, Dolan, RJ (2002). Automatic and intentional brain responses during evaluation of trustworthiness of faces. Nature Neuroscience 5, 277283.CrossRefGoogle ScholarPubMed