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Intact emotion facilitation for nonsocial stimuli in autism: Is amygdala impairment in autism specific for social information?

  • MIKLE SOUTH (a1) (a2), SALLY OZONOFF (a3), YANA SUCHY (a1) (a4), RAYMOND P. KESNER (a1) (a4), WILLIAM M. McMAHON (a2) (a4) and JANET E. LAINHART (a2) (a4)...


Atypical amygdala development may play a key role in the emergence of social disability and other symptoms of autism (Baron-Cohen et al., 2000; Schultz, 2005). The mechanisms by which this may occur have received little attention, however, and most support from behavioral and imaging studies has been concerned with socially relevant stimuli such as faces. Given the complexity of amygdala function and its known role in many other emotional tasks, we examined whether individuals with autism would demonstrate impaired performance on several tasks that have been shown to require activation of the amygdala but that do not have any explicit social meaning. Relative to a typical comparison group matched for age and IQ, our sample of 37 adolescents and adults with autism (mean age = 19.7 years) demonstrated equivalent facilitation for perception and learning of emotionally relevant stimuli. On each of four tasks, there were significant main effects of emotion condition on performance for both groups. Future research regarding atypical amygdala function and emotion processing in autism should consider whether the response to nonsocial emotion factors (including negative valence or high arousal) may be intact, despite difficulties in responding to socially relevant stimuli. (JINS, 2008, 14, 42–54.)

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Corresponding author

Correspondence and reprint requests to: Mikle South, Brigham Young University, Department of Psychology, 1001 Kimball Tower, P.O. Box 25543, Provo, UT 84602-5543. E-mail:


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Abell, F., Krams, M., Ashburner, J., Passingham, R., Friston, K., Frackowiak, R., Happe, F., Frith, C., & Frith, U. (1999). The neuroanatomy of autism: A voxel-based whole brain analysis of structural scans. Neuroreport, 10, 16471651.
Adolphs, R., Gosselin, F., Buchanan, T.W., Tranel, D., Schyns, P., & Damasio, A.R. (2005). A mechanism for impaired fear recognition after amygdala damage. Nature, 433, 6872.
Adolphs, R. & Tranel, D. (1999). Preferences for visual stimuli following amygdala damage. Journal of Cognitive Neuroscience, 11, 610616.
Adolphs, R., Tranel, D., Hamann, S., Young, A.W., Calder, A.J., Phelps, E.A., Anderson, A., Lee, G.P., & Damasio, A.R. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damage. Neuropsychologia, 37, 11111117.
Amaral, D.G. (2002). The primate amygdala and the neurobiology of social behavior: Implications for understanding social anxiety. Biological Psychiatry, 51, 711.
Amaral, D.G. & Corbett, B.A. (2003). The amygdala, autism, and anxiety. Novartis Foundation Symposium, 251, 177187.
Ashwin, S., Wheelwright, S., & Baron-Cohen, S. (2006). Finding a face in the crowd: Testing the anger superiority effect in Asperger Syndrome. Brain and Cognition, 61, 7895.
Bachevalier, J. (1996). Brief report: Medial temporal lobe and autism: A putative animal model in primates. Journal of Autism and Developmental Disorders, 26, 217220.
Bachevalier, J. & Loveland, K.A. (2006). Orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism. Neuroscience and Biobehavioral Reviews, 30, 97117.
Balleine, B.W. & Killcross, S. (2006). Parallel incentive processing: An integrated view of amygdala function. Trends in Neuroscience, 29, 272279.
Bauman, M.L. & Kemper, T.L. (1985). Histoanatomic observations of the brain in early infantile autism. Neurology, 35, 866874.
Bauman, M.L. & Kemper, T.L. (1988). Limbic and cerebellar abnormalities: Consistent findings in infantile autism. Journal of Neuropathology and Experimental Neurology, 47, 369.
Baron-Cohen, S., Ring, H.A., Bullmore, E.T., Wheelwright, S., Ashwin, C., & Williams, S.C.R. (2000). The amygdala theory of autism. Neuroscience & Biobehavioral Reviews, 24, 355364.
Baron-Cohen, S., Ring, H.A., Wheelwright, S., Bullmore, E.T., Brammer, M.J., Simmons, A., & Williams, S.C. (1999). Social intelligence in the normal and autistic brain: An fMRI study. European Journal of Neuroscience, 11, 18911898.
Baxter, M.G. & Murray, E.A. (2002). The amygdala and reward. Nature Reviews Neuroscience, 3, 563573.
Bechara, A., Damasio, A.R., Damasio, H., & Anderson, S.W. (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition, 50, 715.
Bechara, A., Damasio, H., Damasio, A.R., & Lee, G.P. (1999). Different contributions of the human amygdala and ventromedial prefrontal cortex to decision making. Journal of Neuroscience, 19, 54735481.
Bechara, A., Tranel, D., Damasio, H., Adolphs, R., Rockland, C., & Damasio, A.R. (1995). Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans. Science, 269, 11151118.
Bernier, R., Dawson, G., Panagiotides, H., & Webb, S. (2005). Individuals with autism spectrum disorders show normal responses to a fear potential startle paradigm. Journal of Autism and Developmental Disorders, 35, 575583.
Bigler, E.D., Tate, D.F., Neely, E.S., Wolfson, L.J., Miller, M.J., Rice, S.A., Cleavinger, H., Anderson, C., Coon, H., Ozonoff, S., Johnson, M., Dinh, E., Lu, J., McMahon, W.M., & Lainhart, J.E. (2003). Temporal lobe, autism, and macrocephaly. American Journal of Neuroradiology, 24, 20662076.
Bradley, M.M. & Lang, P.J. (1999). Affective norms for English words (ANEW): Instruction manual and affective ratings (technical report C-1). Gainesville, FL: NIMH Center for the Study of Emotion and Attention.
Brand, M., Grabenhorst, F., Starcke, K., Vanderkerckhove, M.M., & Markowitsch, H.J. (2007). Role of the amygdala in decisions under ambiguity and decisions under risk: Evidence from patients with Urbach-Wiethe disease. Neuropsychologia, 45, 13051317.
Brothers, L. (1996). Brain mechanisms of social cognition. Journal of Psychopharmacology, 10, 28.
Cheng, D.T., Knight, D.C., Smith, C.N., & Helmstetter, F.J. (2006). Human amygdala activity during the expression of fear responses. Behavioral Neuroscience, 120, 11871195.
Chiba, A.A., Kesner, R.P., Matsuo, F., Heilbrun, M.P., & Madden, K.L. A dissociation between affect and recognition following unilateral temporal lobectomy including the amygdala. ( in preparation).
Colgan, S.E., Lanter, E., McComish, C., Watson, L.R., Crais, E.R., & Baranek, G.T. (2006). Analysis of social interaction gestures in infants with autism. Child Neuropsychology, 12, 307319.
Crone, E.A. & van der Molen, M.W. (2004). Developmental changes in real life decision making: Performance on a gambling task previously shown to depend on the ventromedial prefrontal cortex. Developmental Neuropsychology, 25, 251279.
Dalton, K.M., Nacewicz, B.M., Johnstone, T., Schaefer, H.S., Gernsbacher, M.A., Goldsmith, H.H., Alexander, A.L., & Davidson, R.J. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8, 519526.
Davis, M. & Whalen, P.J. (2001). The amygdala: Vigilance and emotion. Molecular Psychiatry, 6, 1324.
Empirisoft Corporation (2003). DirectRT [computer software]. New York: Empirisoft Corporation.
Flykt, A. (2005). Visual search with biological threat stimuli: Accuracy, reaction times, and heart rate changes. Emotion, 5, 349353.
Giedd, J.N., Snell, J.W., Lange, N., Rajapakse, J.C., Casey, B.J., Kozuch, P.L., Vaituzis, A.C., Vauss, Y.C., Hamburger, S.D., Kaysen, D., & Rapoport, J.L. (1996). Quantitative magnetic resonance imaging of human brain development: Ages 4–18. Cerebral Cortex, 6, 551560.
Gilbert, P.E., Campbell, A., & Kesner, R.P. (2003). The role of the amygdala in conditioned flavor preference. Neurobiology of Learning and Memory, 79, 118121.
Golan, O., Baron-Cohen, S., Hill, J.J., & Rutherford, M.D. (2006). The ‘Reading the Mind in the Voice’ Test-Revised: A study of complex emotion recognition in adults with and without autism spectrum conditions. Journal of Autism and Developmental Disorders, 37, 10961106.
Grelotti, D.J., Klin, A.J., Gauthier, I., Skudlarski, P., Cohen, D.J., Gore, J.C., Volkmar, F.R., & Schultz, R.T. (2005). fMRI activation of the fusiform gyrus and amygdala to cartoon characters but not to faces in a boy with autism. Neuropsychologia, 43, 373385.
Hadjikhani, N., Joseph, R.M., Snyder, J., Chabris, C.F., Clark, J., Steele, S., McGrath, L., Vangel, M., Aharon, I., Feczko, E., Harris, G.J., & Tager-Flusber, H. (2004). Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. NeuroImage, 22, 11411150.
Hannula, D.E., Simons, D.J., & Cohen, N.J. (2005). Imaging implicit perception: Promise and pitfalls. Nature Reviews Neuroscience, 6, 247255.
Haznedar, M.M., Buchsbaum, M.S., Wei, T.C., Hof, P.R., Cartwright, C., Bienstock, C.A., & Hollander, E. (2000). Limbic circuitry in patients with autism spectrum disorders studied with positron emission tomography and magnetic resonance imaging. American Journal of Psychiatry, 157, 19942001.
Hobson, R.P. & Meyer, J.A. (2005). Foundations for self and other: A study in autism. Developmental Science, 8, 481491.
Howard, M.A., Cowell, P.E., 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.
Humphreys, K., Minshew, N., Leonard, G.L., & Behrmann, M. (2007). A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia, 45, 685695.
Johnson, S.A., Yechiam, E., Murphy, R.R., Queller, S., & Stout, J.C. (2006). Motivational processes and autonomic responsivity in Asperger's disorder: Evidence from the Iowa Gambling Task. Journal of the International Neuropsychological Society, 12, 668676.
Kelly, D.J., Quinn, P.C., Slater, A.M., Lee, K., Gibson, A., Smith, M., Ge, L., & Pascalis, O. (2005). Three-month-olds, but not newborns, prefer own-race faces. Developmental Science, 8, F31F36.
Killgore, W.D. & Yurgelun-Todd, D.A. (2004). Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces. Neuroimage, 21, 12151223.
Klin, A., Jones, W., Schultz, R., Volkmar, F., & 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, 809816.
Larson, C.L., Schaefer, H.S., Seigle, G.J., Jackson, C.A., Anderle, M.J., & Davidson, R.J. (2006). Fear is fast in phobic individuals: Amygdala activation in response to fear-relevant stimuli. Biological Psychiatry, 60, 410417.
LeDoux, J.E. (1994). Emotion, memory and the brain. Scientific American, 270, 5057.
LeDoux, J.E. (2000). The amygdala and emotion: A view through fear. In J.P. Aggleton (Ed.), The amygdala: A functional analysis (2nd ed., pp. 289310). Oxford: Oxford University Press.
Lewis, P.A., Critchley, H.D., Rothstein, P., & Dolan, R.J. (2007). Neural correlates of processing valence and arousal in affective words. Cerebral Cortex, 17, 742748.
Lord, C., Risi, S., Lambrecht, L., Cook, E.H., Leventhal, B.L., DiLavore, P., Pickles, A., & Rutter, M. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205223.
Lord, C., Rutter, M., & 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 & Developmental Disorders, 24, 659685.
Loveland, K. (2001). Toward an ecological theory of autism. In J.A. Burack, T. Charman, N. Yirmiya, & P.R. Zelazo (Eds.), The development of autism: Perspectives from theory and research. Mahwah, NJ: Lawrence Erlbaum.
Merckelbach, H., De Jong, P., Leeuw, I., & van den Hout, M.A. (1995). Startle responses of spider phobics to masked stimuli: A pilot study. International Journal of Neuroscience, 81, 169175.
Morris, J.S., Scott, S.K., & Dolan, R.J. (1999). Saying it with feeling: Neural responses to emotional vocalizations. Neuropsychologia, 37, 11551163.
Munson, J., Dawson, G., Abbott, R., Faja, S., Webb, S.J., Friedman, S.D., Shaw, D., Artru, A., & Dager, S.R. (2006). Amygdalar volume and behavioral development in autism. Archives of General Psychiatry, 63, 686693.
Nakic, M., Smith, B.W., Busis, S., Vythilingam, M., & Blair, R.J. (2006). The impact of affect and frequency on lexical decision: The role of the amygdala and inferior frontal cortex. Neuroimage, 31, 17521761.
Nelson, C.A., Bloom, F.E., Cameron, J.L., Amaral, D., Dahl, R.E., & Pine, D. (2002). An integrative, multidisiplinary approach to the study of brain-behavior relations in the context of typical and atypical development. Development and Psychopathology, 14, 499520.
Ohman, A. (2005). The role of the amygdala in human fear: Automatic detection of threat. Psychoneuroendocrinology, 30, 953958.
Ohman, A., Flykt, A., & Esteves, F. (2001). Emotion drives attention: Detecting the snake in the grass. Journal of Experimental Psychology: General, 130, 466478.
Ohman, A. & Mineka, S. (2001). Fears, phobias, and preparedness: Toward an evolved module of fear and fear learning. Psychological Review, 108, 482522.
Pasley, B.N., Mayes, L.C., & Schultz, R.T. (2004). Subcortical discrimination of unperceived objects during binocular rivalry. Neuron, 42, 163172.
Paul, R., Augustyn, A., Klin, A., & Volkmar, F.R. (2005). Perception and production of prosody by speakers with autism spectrum disorders. Journal of Autism and Developmental Disorders, 35, 205220.
Pelphrey, K.A., Sasson, N.J., Reznick, J.S., Paul, G., Goldman, B.D., & Piven, J. (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders, 32, 249261.
Phelps, E.A. & LeDoux, J.E. (2005). Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron, 48, 175187.
Pierce, K., Haist, F., Sedaghat, F., & Courschesne, E. (2004). The brain response to personally familiar faces in autism: Findings of fusiform activity and beyond. Brain, 127, 27032716.
Pierce, K., Muller, R.A., Ambrose, J., Allen, G., & Courchesne, E. (2001). Face processing occurs outside the “fusiform face area” in autism: Evidence from functional MRI. Brain, 124, 20592073.
Pine, D.S., Lissek, S., Klein, R.G., Mannuzza, S., Moulton, J.L., III, Guardino, M., & Woldehawariat, G. (2004). Face-memory and emotion: Associations with major depression in children and adolescents. Journal of Child Psychiatry and Psychology, 45, 11991208.
Rauch, S.L., Shin, L.M., & Phelps, E.A. (2006). Neurocircuitry models of posttraumatic stress disorder and extinction: Human neuroimaging research-past, present, and future. Biological Psychiatry, 60, 376382.
Reinders, A.A., Glascher, J., de Jong, J.R., Willemsen, A.T., den Boer, J.A., & Buchel, C. (2006). Detecting fearful and neutral faces: BOLD latency differences in amygdala-hippocampal junction. Neuroimage, 33, 805814.
Rutherford, M.D., Young, G.S., Hepburn, S., & Rogers, S.J. (2006). A longitudinal study of pretend play in autism. Journal of Autism and Developmental Disorders, 37, 10241039.
Sabatinelli, D., Bradley, M.M., Fitzsimmons, J.R., & Lang, P.J. (2005). Parallel amygdala and inferotemporal activation reflect emotional intensity and fear relevance. Neuroimage, 24, 12651270.
Sabbagh, M.A. (2004). Understanding orbitofrontal contributions to theory-of-mind reasoning: Implications for autism. Brain and Cognition, 55, 209219.
Sander, K., Brechmann, A., & Scheich, H. (2003). Audition of laughing and crying leads to right amygdala activation in a low-noise setting. Brain Research Protocols, 11, 8191.
Schultz, R.T. (2005). Developmental deficits in social perception in autism: The role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience, 23, 125141.
Schultz, R.T., Gauthier, I., Klin, A., Fulbright, R.K., Anderson, A.W., Volkmar, F., Skudlarski, P., Lacadie, C., Cohen, D.J., & Gore, J.C. (2000). Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Archives of General Psychiatry, 57, 331340.
Schultz, R.T., Grelotti, D.J., Klin, A., Kleinman, J., Van der Gaag, C., Marois, R., & Skudlarski, P. (2003). The role of the fusiform face area in social cognition: Implications for the pathobiology of autism. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 358, 415427.
Schultz, R.T., Hunyadi, E., Connors, C., & Pasley, B. (2005). fMRI study of facial expression perception in autism: The amygdala, fusiform face area and their functional connectivity. Paper presented at the annual meeting of the Organization for Human Brain Mapping, June 12–16, 2005, Toronto, CA.
Schumann, C.M., Hamstra, J., Goodlin-Jones, B.L., Lotspeich, L.J., Kwon, H., Buonocore, M.H., Lammers, C.R., Reiss, A.L., & Amaral, D.G. (2004). The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. Journal of Neuroscience, 24, 63926401.
Skuse, D., Morris, J., & Lawrence, K. (2003). The amygdala and the development of the social brain. Annals of the New York Academy of Sciences, 1008, 91101.
Sotres-Bayon, F., Bush, D.E., & LeDoux, J.E. (2004). Emotional perseveration: An update on prefrontal-amygdala interactions in fear extinction. Learning and Memory, 11, 525535.
Sparks, B.F., Friedman, S.D., Shaw, D.W., Aylward, E.H., Echelard, D., Artru, A.A., Maravilla, K.R., Giedd, J.N., Munson, J., Dawson, G., & Dager, S.R. (2002). Brain structural abnormalities in young children with autism spectrum disorder. Neurology, 59, 184192.
Speer, L.L., Cook, A.E., McMahon, W.M., & Clark, E. (2007). Face processing in children with autism: Effects of stimulus contents and type. Autism, 11, 265277.
Suomi, S.J. & Harlow, H.F. (1971). Abnormal social behavior in young monkeys. In J. Helmuth (Ed.), The exceptional infant (Vol. 2). New York: Bruner-Mazel.
Turati, C., Simion, F., Milani, I., & Umilta, C. (2002). Newborns' preference for faces: What is crucial? Developmental Psychology, 38, 875882.
van der Geest, J.N., Kemner, C., Camfferman, G., Verbaten, M.N., & van Engeland, H. (2002). Gaze behavior of children with pervasive developmental disorder toward human faces: A fixation time study. Journal of Child Psychology and Psychiatry, 43, 669678.
Vollm, B.A., Taylor, A.N., Richardson, P., Corcoran, R., Stirling, J., McKie, S., Deakin, J.F., & Elliot, R. (2006). Neuronal correlates of theory of mind and empathy: A functional magnetic resonance imaging study in a nonverbal task. Neuroimage, 20, 9098.
Vuilleumier, P. & Pourtois, G. (2007). Distributed and interactive brain mechanisms during emotion face perception: Evidence from functional neuroimaging. Neuropsychologia, 45, 174194.
Wang, A.T., Dapretto, M., Hariri, A.R., Sigman, M., & Bookheimer, S.Y. (2004). Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 43, 481490.
Waterhouse, L., Fein, D., & Modahl, C. (1996). Neurofunctional mechanisms in autism. Psychological Review, 103, 457489.
Willems, S., Adam, S., & van der Linden, M. (2002). Normal mere exposure effect with impaired recognition in Alzheimer's disease. Cortex, 38, 7786.
Winston, J.S., Gottfried, J.A., Kilner, J.M., & Dolan, R.J. (2005). Integrated neural representations of odor intensity and affective valence in human amygdala. Journal of Neuroscience, 25, 89038907.
Zajonc, R.B. (1968). Attitudinal effects of mere exposure. Journal of Personality and Social Psychology, 9, 127.
Zajonc, R.B. (2001). Mere exposure: A gateway to the subliminal. Current Directions in Psychological Science, 10, 224.
Zirlinger, M. & Anderson, D. (2003). Molecular dissection of the amygdala and its relevance to autism. Genes, Brain, and Behavior, 2, 282294.



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