OJPsych  Vol.3 No.2 A , April 2013
Autism, social cognition and superior temporal sulcus

Results on brain imaging studies have led to a better understanding of the neural circuits involved in social cognition and its implication in autism spectrum disorders(ASD). It has been shown that the superior temporal sulcus(STS)is highly implicated in social processes, from perception of socially relevant information, such as body movements or eye gaze, to more complex social cognition processes. Furthermore, several multimodal brain imaging results point to anatomo-functional abnormalities in the STS in both children and adults with ASD. These results are highly consistent with social impairments in ASD, among which eye gaze perception is particularly relevant. Gaze abnormalities can now be objectively measured using eye-tracking methodology, leading to a better characterization of social perception impairments in autism. Moreover, these gaze abnormalities have been associated with STS abnormalities in ASD. Based on these results, our hypothesis is that anatomo-functional anomalies in the STS occurring early across brain development could constitute the first step in the cascade of neural dysfunction underlying autism. In the present work, we’ll review recent data of STS contribution to normal social cognition and it’s implication in autism.

Cite this paper
Zilbovicius, M. , Saitovitch, A. , Popa, T. , Rechtman, E. , Diamandis, L. , Chabane, N. , Brunelle, F. , Samson, Y. and Boddaert, N. (2013) Autism, social cognition and superior temporal sulcus. Open Journal of Psychiatry, 3, 46-55. doi: 10.4236/ojpsych.2013.32A008.
[1]   Brothers, L., Ring, B. and Kling, A. (1990) Response of neurons in the macaque amygdala to complex social stimuli. Behavioural Brain Research, 41, 199-213. doi:10.1016/0166-4328(90)90108-Q

[2]   Kaiser, M.D., Hudac, C.M., Shultz, S., Lee, S.M., Cheung, C., et al. (2010) Neural signatures of autism. Proceedings of the National Academy of Sciences of the United States of America, 107, 21223-21228. doi:10.1073/pnas.1010412107

[3]   Adolphs, R. (2003) Cognitive neuroscience of human social behaviour. Nature Reviews Neuroscience, 4, 165-178. doi:10.1038/nrn1056

[4]   Thompson, J. and Parasuraman, R. (2012) Attention, biological motion, and action recognition. Neuroimage, 59, 4-13. doi:10.1016/j.neuroimage.2011.05.044

[5]   Allison, T., Puce, A. and McCarthy, G. (2000) Social perception from visual cues, role of the STS region. Trends in Cognitive Sciences, 4, 267-278. doi:10.1016/S1364-6613(00)01501-1

[6]   Bonda, E., Petrides, M., Ostry, D. and Evans, A. (1996) Specific involvement of human parietal systems and the amygdala in the perception of biological motion. Journal of Neuroscience, 16, 3737-3744.

[7]   Pelphrey, K.A., Morris, J.P. and McCarthy, G. (2005) Neural basis of eye gaze processing deficits in autism. Brain, 128, 1038-1048. doi:10.1093/brain/awh404

[8]   Mosconi, M.W., Mack, P.B., McCarthy, G. and Pelphrey, K.A. (2005) Taking an “intentional stance” on eye-gaze shifts: A functional neuroimaging study of social perception in children. Neuroimage, 27, 247-252. doi:10.1016/j.neuroimage.2005.03.027

[9]   Pelphrey, K.A., Morris, J.P., Michelich, C.R., Allison, T. and McCarthy, G. (2005) Functional anatomy of biological motion perception in posterior temporal cortex: An FMRI study of eye, mouth and hand movements. Cereb Cortex, 15, 1866-1876. doi:10.1093/cercor/bhi064

[10]   Ohnishi, T., Matsuda, H., Hashimoto, T., Kunihiro, T., Nishikawa, M., et al. (2000) Abnormal regional cerebral blood flow in childhood autism. Brain, 123, 1838-1844. doi:10.1093/brain/123.9.1838

[11]   Boddaert, N., Chabane, N., Gervais, H., Good, C.D., Bourgeois, M., et al. (2004) Superior temporal sulcus anatomical abnormalities in childhood autism: A voxelbased morphometry MRI study. Neuroimage, 23, 364-369. doi:10.1016/j.neuroimage.2004.06.016

[12]   Castelli, F., Frith, C., Happe, F. and Frith, U. (2002) Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. Brain, 125, 1839-1849. doi:10.1093/brain/awf189

[13]   Pelphrey, K.A., Shultz, S., Hudac, C.M. and Vander Wyk, B.C. (2011) Research review: Constraining heterogeneity, the social brain and its development in autism spectrum disorder. Journal of Child Psychology and Psychiatry, 52, 631-644. doi:10.1111/j.1469-7610.2010.02349.x

[14]   Zilbovicius, M., Boddaert, N., Belin, P., Poline, J.B., Remy, P., et al. (2000) Temporal lobe dysfunction in childhood autism: A PET study. Positron emission tomogramphy. American Journal of Psychiatry, 157, 1988-1993. doi:10.1176/appi.ajp.157.12.1988

[15]   Zilbovicius, M., Meresse, I., Chabane, N., Brunelle, F., Samson, Y., et al. (2006) Autism, the superior temporal sulcus and social perception. Trends in Neuroscience, 29, 359-366. doi:10.1016/j.tins.2006.06.004

[16]   Baron-Cohen, S., Ring, H., Moriarty, J., Schmitz, B., Costa, D., et al. (1994) Recognition of mental state terms. Clinical findings in children with autism and a functional neuroimaging study of normal adults. British Journal of Psychiatry, 165, 640-649. doi:10.1192/bjp.165.5.640

[17]   Frith, C.D. and Frith, U. (1999) Interacting minds—A biological basis. Science, 286, 1692-1695. doi:10.1126/science.286.5445.1692

[18]   Bardi, L., Regolin, L. and Simion, F. (2011) Biological motion preference in humans at birth, role of dynamic and configural properties. Developmental Science, 14, 353-359.

[19]   Klin, A., Lin, D.J., Gorrindo, P., Ramsay, G. and Jones, W. (2009) Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature, 459, 257-261. doi:10.1038/ nature07868

[20]   Jones, W., Carr, K. and Klin, A. (2008) Absence of preferential looking to the eyes of approaching adults predicts level of social disability in 2-year-old toddlers with autism spectrum disorder. Archives of General Psychiatry, 65, 946-954. doi:10.1001/archpsyc.65.8.946

[21]   Pavlova, M.A. (2012) Biological motion processing as a hallmark of social cognition. Cereb Cortex, 22, 981-995. doi:10.1093/cercor/bhr156

[22]   Farroni, T., Csibra, G., Simion, F. and Johnson, M.H. (2002) Eye contact detection in humans from birth. Proceedings of the National Academy of Sciences of the United States of America, 99, 9602-9605. doi:10.1073/pnas.152159999

[23]   Klin, A., Jones, W., Schultz, R. and Volkmar, F. (2003) The enactive mind, or from actions to cognition, lessons from autism. Philosophical Transactions of the Royal Society B: Biological Sciences, 358, 345-360. doi:10.1098/rstb.2002.1202

[24]   Senju, A., Kikuchi, Y., Hasegawa, T., Tojo, Y. and Osanai, H. (2008) Is anyone looking at me? Direct gaze detection in children with and without autism. Brain and Cognition, 67, 127-139. doi:10.1016/j.bandc.2007.12.001

[25]   Frith, C.D. and Frith, U. (2012) Mechanisms of social cognition. Annual Review of Psychology, 63, 287-313. doi:10.1146/annurev-psych-120710-100449

[26]   Frith, U., Morton, J. and Leslie, A.M. (1991) The cognitive basis of a biological disorder, autism. Trends in Neuroscience, 14, 433-438. doi:10.1016/0166-2236(91)90041-R

[27]   Baron-Cohen, S., Ring, H.A., Wheelwright, S., Bullmore, E.T., Brammer, M.J., et al. (1999) Social intelligence in the normal and autistic brain: An fMRI study. European Journal of Neuroscience, 11, 1891-1898. doi:10.1046/j.1460-9568.1999.00621.x

[28]   Klin, A., Jones, W., Schultz, R., Volkmar, F. and Cohen, D. (2002) Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59, 809-816. doi:10.1001/archpsyc.59.9.809

[29]   Speer, L.L., Cook, A.E., McMahon, W.M. and Clark, E. (2007) Face processing in children with autism, effects of stimulus contents and type. Autism, 11, 265-277. doi:10.1177/1362361307076925

[30]   Chawarska, K., Klin, A., Paul, R., Macari, S. and Volkmar, F. (2009) A prospective study of toddlers with ASD: Short-term diagnostic and cognitive outcomes. Journal of Child Psychology and Psychiatry, 50, 1235-1245. doi:10.1111/j.1469-7610.2009.02101.x

[31]   Falck-Ytter, T. and von Hofsten, C. (2011) How special is social looking in ASD: A review. Progress in Brain Research, 189, 209-222. doi:10.1016/B978-0-444-53884-0.00026-9

[32]   Boraston, Z. and Blakemore, S.J. (2007) The application of eye-tracking technology in the study of autism. Journal of Physiology, 581, 893-898. doi:10.1113/jphysiol.2007.133587

[33]   Pierce, K., Conant, D., Hazin, R., Stoner, R. and Desmond, J. (2011) Preference for geometric patterns early in life as a risk factor for autism. Archives of General Psychiatry, 68, 101-109. doi:10.1001/archgenpsychiatry.2010.113

[34]   Rice, K., Moriuchi, J.M., Jones, W. and Klin, A. (2012) Parsing heterogeneity in autism spectrum disorders, visual scanning of dynamic social scenes in school-aged children. Journal of the American Academy of Child and Adolescent Psychiatry, 51, 238-248. doi:10.1016/j.jaac.2011.12.017

[35]   Noris, B., Nadel, J., Barker, M., Hadjikhani, N. and Billard, A. (2012) Investigating gaze of children with ASD in naturalistic settings. PLoS One, 7, e44144. doi:10.1371/journal.pone.0044144

[36]   Saitovitch, A., Bargiacchi, A., Chabane, N., Philippe, A., Samson, Y. and Zilbovicius, M. (2013) Studying Gaze abnormalities in autism, Which type of stimulus to use? Submitted.

[37]   Pelphrey, K.A., Sasson, N.J., Reznick, J.S., Paul, G., Goldman, B.D., et al. (2002) Visual scanning of faces in autism. Journal of Autism and Developmental Disorders, 32, 249-261. doi:10.1023/A:1016374617369

[38]   Bal, E., Harden, E., Lamb, D., Van Hecke, A.V., Denver, J.W., et al. (2010) Emotion recognition in children with autism spectrum disorders, relations to eye gaze and autonomic state. Journal of Autism and Developmental Disorders, 40, 358-370. doi:10.1007/s10803-009-0884-3

[39]   Keysers, C. and Perrett, D.I. (2004) Demystifying social cognition: A Hebbian perspective. Trends in Cognitive Science, 8, 501-507. doi:10.1016/j.tics.2004.09.005

[40]   Howard, R.J., Brammer, M., Wright, I., Woodruff, P.W., Bullmore, E.T., et al. (1996) A direct demonstration of functional specialization within motion-related visual and auditory cortex of the human brain. Current Biology, 6, 1015-1019. doi:10.1016/S0960-9822(02)00646-2

[41]   Belin, P., Zatorre, R.J., Lafaille, P., Ahad, P. and Pike, B. (2000) Voice-selective areas in human auditory cortex. Nature, 403, 309-312. doi:10.1038/35002078

[42]   Herrington, J.D., Nymberg, C. and Schultz, R.T. (2011) Biological motion task performance predicts superior temporal sulcus activity. Brain and Cognition, 77, 372-381. doi:10.1016/j.bandc. 2011.09.001

[43]   Neuhaus, E., Beauchaine, T.P. and Bernier, R. (2010) Neurobiological correlates of social functioning in autism. Clinical Psychology Review, 30, 733-748. doi:10.1016/j.cpr.2010.05.007

[44]   Pavlova, M., Sokolov, A.N., Birbaumer, N. and Krageloh-Mann, I. (2008) Perception and understanding of others’ actions and brain connectivity. Journal of Cognitive Neuroscience, 20, 494-504. doi:10.1162/jocn.2008.20034

[45]   Wyk, B.C., Hudac, C.M., Carter, E.J., Sobel, D.M. and Pelphrey, K.A. (2009) Action understanding in the superior temporal sulcus region. Psychological Science, 20, 771-777. doi:10.1111/j.1467-9280.2009.02359.x

[46]   Stevens, J.A., Fonlupt, P., Shiffrar, M. and Decety, J. (2000) New aspects of motion perception, selective neural encoding of apparent human movements. Neuroreport, 11, 109-115. doi:10.1097/00001756-200001170-00022

[47]   Decety, J., Grezes, J., Costes, N., Perani, D., Jeannerod, M., et al. (1997) Brain activity during observation of actions. Influence of action content and subject’s strategy. Brain, 120, 1763-1777. doi:10.1093/brain/120.10.1763

[48]   Pelphrey, K.A., Morris, J.P. and McCarthy, G. (2004) Grasping the intentions of others, the perceived intentionality of an action influences activity in the superior temporal sulcus during social perception. Journal of Cognitive Neuroscience, 16, 1706-1716. doi:10.1162/0898929042947900

[49]   Pelphrey, K.A., Singerman, J.D., Allison, T. and McCarthy, G. (2003) Brain activation evoked by perception of gaze shifts: The influence of context. Neuropsychologia, 41, 156-170. doi:10.1016/S0028 -3932(02)00146-X

[50]   Pelphrey, K.A., Viola, R.J. and McCarthy, G. (2004) When strangers pass, processing of mutual and averted social gaze in the superior temporal sulcus. Psychological Science, 15, 598-603. doi:10.1111/j.0956-7976.2004.00726.x

[51]   Kriegstein, K.V. and Giraud, A.L. (2004) Distinct functional substrates along the right superior temporal sulcus for the processing of voices. Neuroimage, 22, 948-955. doi:10.1016/j.neuro image.2004.02.020

[52]   Lewis, J.W., Frum, C., Brefczynski-Lewis, J.A., Talkington, W.J., Walker, N.A., et al. (2011) Cortical network differences in the sighted versus early blind for recognition of human-produced action sounds. Human Brain Mapping, 32, 2241-2255. doi:10.1002/hbm.21185

[53]   Castelli, F., Happe, F., Frith, U. and Frith, C. (2000) Movement and mind: A functional imaging study of perception and interpretation of complex intentional movement patterns. Neuroimage, 12, 314-325. doi:10.1006/nimg.2000.0612

[54]   Schultz, J., Imamizu, H., Kawato, M. and Frith, C.D. (2004) Activation of the human superior temporal gyrus during observation of goal attribution by intentional objects. Journal of Cognitive Neuroscience, 16, 1695-1705. doi:10.1162/0898929042947874

[55]   Zacks, J.M., Braver, T.S., Sheridan, M.A., Donaldson, D.I., Snyder, A.Z., et al. (2001) Human brain activity time-locked to perceptual event boundaries. Nature Neuroscience, 4, 651-655. doi:10.1038/88486

[56]   Wallace, G.L., Shaw, P., Lee, N.R., Clasen, L.S., Raznahan, A., et al. (2012) Distinct cortical correlates of autistic versus antisocial traits in a longitudinal sample of typically developing youth. Journal of Neuroscience, 32, 4856-4860. doi:10.1523/JNEUROSCI.6214-11.2012

[57]   von dem Hagen, E.A., Nummenmaa, L., Yu, R., Engell, A.D., Ewbank, M.P., et al. (2011) Autism spectrum traits in the typical population predict structure and function in the posterior superior temporal sulcus. Cereb Cortex, 21, 493-500. doi:10.1093/cercor/bhq062

[58]   Nummenmaa, L., Engell, A.D., von dem Hagen, E., Henson, R.N. and Calder, A.J. (2012) Autism spectrum traits predict the neural response to eye gaze in typical individuals. Neuroimage, 59, 3356-3363. doi:10.1016/j.neuroimage.2011.10.075

[59]   Kanai, R., Bahrami, B., Roylance, R. and Rees, G. (2012) Online social network size is reflected in human brain structure. Proceedings of the Royal Society B: Biological Sciences, 279, 1327-1334. doi:10.1098/rspb.2011.1959

[60]   Lord, C., Rutter, M. and Le Couteur, A. (1994) Autism diagnostic interview-revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659-685. doi:10.1007/BF02172145

[61]   Gendry Meresse, I., Zilbovicius, M., Boddaert, N., Robel, L., Philippe, A., et al. (2005) Autism severity and temporal lobe functional abnormalities. Annals of Neurology, 58, 466-469. doi:10.1002/ ana.20597

[62]   Duchesnay, E., Cachia, A., Boddaert, N., Chabane, N., Mangin, J.F., et al. (2011) Feature selection and classification of imbalanced datasets, application to PET images of children with autistic spectrum disorders. Neuroimage, 57, 1003-1014. doi:10.1016/j.neuroimage.2011.05.011

[63]   Levitt, J.G., Blanton, R.E., Smalley, S., Thompson, P.M., Guthrie, D., et al. (2003) Cortical sulcal maps in autism. Cereb Cortex, 13, 728-735. doi:10.1093/cercor/13.7.728

[64]   Hadjikhani, N., Joseph, R.M., Snyder, J. and TagerFlusberg, H. (2006) Anatomical differences in the mirror neuron system and social cognition network in autism. Cereb Cortex, 16, 1276-1282. doi:10.1093/cercor/bhj069

[65]   Abell, F., Krams, M., Ashburner, J., Passingham, R., Friston, K., et al. (1999) The neuroanatomy of autism: A voxel-based whole brain analysis of structural scans. Neuroreport, 10, 1647-1651. doi:10.1097/00001756-199906030-00005

[66]   McAlonan, G.M., Cheung, V., Cheung, C., Suckling, J., Lam, G.Y., et al. (2005) Mapping the brain in autism: A voxel-based MRI study of volumetric differences and intercorrelations in autism. Brain, 128, 268-276. doi:10.1093/brain/awh332

[67]   Barnea-Goraly, N., Lotspeich, L.J. and Reiss, A.L. (2010) Similar white matter aberrations in children with autism and their unaffected siblings: A diffusion tensor imaging study using tract-based spatial statistics. Archives of General Psychiatry, 67, 1052-1060. doi:10.1001/archgenpsychiatry.2010.123

[68]   Just, M.A., Cherkassky, V.L., Keller, T.A. and Minshew, N.J. (2004) Cortical activation and synchronization during sentence comprehension in high-functioning autism, evidence of underconnectivity. Brain, 127, 1811-1821. doi:10.1093/brain/awh199

[69]   Fouque, A.L., Fillard, P., Bargiacchi, A., Cachia, A., Zilbovicius, M., et al. (2011) Voxelwise multivariate statistics and brain-wide machine learning using the full diffusion tensor. Medical Image Computing and Computer Assisted Intervention, 14, 9-16.

[70]   Mori, S., Oishi, K., Jiang, H., Jiang, L., Li, X., et al. (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage, 40, 570-582. doi:10.1016/j.neur oimage.2007.12.035

[71]   Bargiacchi, A., Cachia, A., Chabane, N., Boddaert, N., Philippe, A., Brunelle, F., Poupon, C., Mouren, M.C., Samson, Y., Laurier, L. and Zilbovicius, M. (2013) Correlation of white matter integrity and autism clinical symptomatology: A whole-brain diffusion MRI study. Submitted.

[72]   Philip, R.C., Dauvermann, M.R., Whalley, H.C., Baynham, K., Lawrie, S.M., et al. (2011) A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neuroscience & Biobehavioral Reviews, 36, 901-942.

[73]   Gervais, H., Belin, P., Boddaert, N., Leboyer, M., Coez, A., et al. (2004) Abnormal cortical voice processing in autism. Nature Neuroscience, 7, 801-802. doi:10.1038/nn1291

[74]   Haxby, J.V., Hoffman, E.A. and Gobbini, M.I. (2002) Human neural systems for face recognition and social communication. Biological Psychiatry, 51, 59-67. doi:10.1016/S0006-3223(01)01330-0

[75]   Philip, R.C., Dauvermann, M.R., Whalley, H.C., Baynham, K., Lawrie, S.M., et al. (2012) A systematic review and meta-analysis of the fMRI investigation of autism spectrum disorders. Neuroscience & Biobehavioral Reviews, 36, 901-942. doi:10.1016/j.neubiorev.2011.10.008

[76]   Schultz, R.T., Gauthier, I., Klin, A., Fulbright, R.K., Anderson, A.W., et al. (2000) Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Archives of General Psychiatry, 57, 331-340. doi:10.1001/archpsyc.57.4.331

[77]   Pierce, K., Muller, R.A., Ambrose, J., Allen, G. and Courchesne, E. (2001) Face processing occurs outside the fusiform “face area” in autism, evidence from functional MRI. Brain, 124, 2059-2073. doi:10.1093/brain/124.10.2059

[78]   Critchley, H.D., Daly, E.M., Bullmore, E.T., Williams, S.C., Van Amelsvoort, T., et al. (2000) The functional neuroanatomy of social behaviour, changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain, 123, 2203-2212. doi:10.1093/brain/123.11.2203

[79]   Hubl, D., Bolte, S., Feineis-Matthews, S., Lanfermann, H., Federspiel, A., et al. (2003) Functional imbalance of visual pathways indicates alternative face processing strategies in autism. Neurology, 61, 1232-1237. doi:10.1212/01.WNL.0000091862.22033.1A

[80]   Critchley, H., Daly, E., Phillips, M., Brammer, M., Bullmore, E., et al. (2000) Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study. Human Brain Mapping, 9, 93-105. doi:10.1002/(SICI)1097-0193(200002)9:2<93::AID-HBM4>3.0.CO;2-Z

[81]   Otsuka, Y., Osaka, N., Ikeda, T. and Osaka, M. (2009) Individual differences in the theory of mind and superior temporal sulcus. Neuroscience Letters, 463, 150-153. doi:10.1016/j.neulet.2009.07.064