Skip to main content
SpringerLink
Log in

Individuals with Autism Spectrum Disorder Show Normal Responses to a Fear Potential Startle Paradigm

  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

The present study utilized a fear potentiated startle paradigm to examine amygdala function in individuals with autism spectrum disorder. Two competing hypotheses regarding amygdala dysfunction in autism have been proposed: (1) The amygdala is under-responsive, in which case it would be predicted that, in a fear potentiated startle experiment, individuals with autism would exhibit decreased fear conditioning and/or potentiation, and (2) The amygdala is over responsive, in which case an exaggerated potentiation of the startle response would be predicted. Fourteen adolescents and adults diagnosed with autism spectrum disorder and 14 age, gender, IQ, and anxiety level-matched typical adolescents and adults participated. Both participants with autism and typical participants potentiated the startle response following fear conditioning and no group differences in the latency or amplitude of the potentiated startle response were found. These results suggest that this aspect of amygdala function, namely fear conditioning and potentiation of the startle response, is intact in individuals with autism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

References

  • 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 scansNeuroreport 10(8): 1647–1651

    Article  PubMed  CAS  Google Scholar 

  • Adolphs, R., Tranel, D., Damasio, H., Damasio, A. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdalaNature 372: 669–672

    Article  PubMed  CAS  Google Scholar 

  • Adolphs, R., Tranel, D., hamann, S., Young, A., Calder, A., Phelps, E., Lee, G., Damasio, A. (1999). Recognition of facial emotion in nine individuals with bilateral amygdala damageNeuropsychologia 37: 1111–1117

    Article  PubMed  CAS  Google Scholar 

  • Aitken, C., Siddle, D., Lipp, O. (1999). The effects of threat and nonthreat word lead stimuli on blink modification Psychophysiology, 36: 699–705

    Article  PubMed  CAS  Google Scholar 

  • Amaral, D., Baumann, M., Schumann, C. (2003). The Amygdala and autism: Implications from non-human primate studies. Genes, Brain and Behavior, 2: 295–302

    Article  CAS  Google Scholar 

  • Ameli, R., Ip, C., Grillon, C. (2001). Contextual fear-potentiated startle conditioning in humans: Replication and extensionPsychophysiology 38: 383–390

    Article  PubMed  CAS  Google Scholar 

  • American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., Text Revision). APA, Washington DC

    Google Scholar 

  • Anderson, A., Spencer, D., Fulbright, R., Phelps, E. A. (2000). Contribution of the anteromedial temporal lobes to the evaluation of facial emotion Neuropsychology 14(4): 526–536

    Article  PubMed  CAS  Google Scholar 

  • Bachevalier J. (1994). Medial temporal lobe structures and autism: A review of clinical and experimental findings Neuropsychologia 36: 627–648

    Article  Google Scholar 

  • Baron-Cohen, S., Ring, H., Bullmore, E., Wheelwright, S., Ashwin, C., Williams, S. (2000). The amygdala theory of autism Neuroscience and Biobehavioral Reviews 24: 355–364

    Article  PubMed  CAS  Google Scholar 

  • Baron-Cohen, S., Ring, H., Wheelwright, S., Bullmore, E., Brammer, M., Simmons, A., Williams, S. (1999). Social intelligence in the normal and autistic brain: An fMRI studyEuropean Journal of Neuroscience 11: 1891–1898

    Article  PubMed  CAS  Google Scholar 

  • Basso M. (2001). Neurobiological relationships between ambient lighting and the startle response to acoustic stress in humansInternational Journal of Neuroscience 110(3–4): 147–157

    Article  PubMed  Google Scholar 

  • Bauman M., T. Kemper (1994). Neuroanatomic observations of the brain in autism. In M. Bauman, T. Kemper (eds), The neurobiology of autism. Baltimore, Johns Hopkins University Press, pp. 119–145

    Google Scholar 

  • Bechara, A., Tranel, H., Adolphs, R., Rockland, C., Damasio, A. (1995). Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans Science269 1115–1118

    Article  PubMed  CAS  Google Scholar 

  • Bradley, M., Cuthbert, B., Lang, P. (1990). Startle reflex modification: Emotion or attention?Psychophysiology 27(5): 513–522

    Article  PubMed  CAS  Google Scholar 

  • Bradley, M., Cuthbert, B., Lang, P. (1999). Affect and the startle reflex In M. Dawson, A. Schell, A. Bohmelt (eds), Startle modification: Implications for neuroscience, cognitive science, and clinical science. Cambridge University Press, Cambridge, UK, pp. 157–183

    Google Scholar 

  • Buchel, C., Dolan, R., Armony, J., Friston, K. (1999). Amygdala-hippocampal involvement in human aversive trace conditioning revealed through event-related functional magnetic resonance imagingJournal of Neuroscience 19(24): 10869–10876

    PubMed  CAS  Google Scholar 

  • Buchel, C., Morris, J., Dolan, R., Friston, K. (1998). Brain systems mediating aversive conditioning Neuron 20: 947–957

    Article  PubMed  CAS  Google Scholar 

  • Bucher, K., Myers, R., Southwick, C. (1970). Anterior temporal cortex and maternal behavior in monkeysNeurology 20: 415

    PubMed  CAS  Google Scholar 

  • Calder, A., Young, A., Rowland, D., Hodges, J., Etcoff, N. (1996). Facial emotion recognition after bilateral amygdala damage: Differentially severe impairment of fearCognitive Neuropsychology 13: 699–745

    Article  Google Scholar 

  • Fridlund, A., Cacioppo, J. (1986). Guidelines for human electromyographic research. Psychophysiology, 23: 567–589

    Article  PubMed  CAS  Google Scholar 

  • Funayama, E., Grillon, C., Davis, M., Phelps, E. (2001). A double dissociation in the affective modulation of startle in humans: Effects of unilateral temporal lobectomyJournal of Cognitive Neuroscience 13(6): 721–729

    Article  PubMed  CAS  Google Scholar 

  • Gillott, A., Furniss, F., Walter, A. (2001). Anxiety in high functioning children with autismAutism 5: 277–286

    Article  PubMed  CAS  Google Scholar 

  • Grillon, C., R. Ameli (1998). Effects of threat and safety signals on startle during anticipation of aversive shocks, sounds or airblastsJournal of Psychophysiology 12(4): 329–337

    Google Scholar 

  • Grillon, C., Dierker, L., Merikangas, K. (1997). Startle modulation in children at risk for anxiety disorders and/or alcoholismJournal of the American Academy of Child and Adolescent Psychiatry 36(7): 925–932

    Article  PubMed  CAS  Google Scholar 

  • Grillon, C., Dierker, L., Merikangas, K. (1998). Fear potentiated startle in adolescent offspring of parents with anxiety disordersBiological Psychiatry 44: 990–997

    Article  PubMed  CAS  Google Scholar 

  • Grillon, C., Merikangas, K., Dierker, L., Snidman, N., Arriaga, R., Kagan, J., Donzella, B., Dikel, T., Nelson, C. (1999). Startle potentiation by threat of aversive stimuli and darkness in adolescents: A multi-site studyInternational Journal of Psychophysiology 32: 63–73

    Article  PubMed  CAS  Google Scholar 

  • Grillon, C., C. Morgan (1999). Fear-potentiated startle conditioning to explicit and contextual cues in Gulf war veterans with posttraumatic stress disorderJournal of Abnormal Psychology 108: 134–142

    Article  PubMed  CAS  Google Scholar 

  • Grillon, C., Morgan, C., Southwick, S., Davis, M., Charney, D. (1996). Baseline startle amplitude and prepulse inhibition in Vietnam veterans with PTSDPsychiatry Research 64: 169–178

    Article  PubMed  CAS  Google Scholar 

  • Hamann, S., Stefanacci, L., Squire, L., Adolphs, R., Tranel, D., Damasio, H., Damasio, A. (1996). Recognizing facial emotionNature 379(6565): 497

    Article  PubMed  CAS  Google Scholar 

  • Kawashima, R., Sugiura, M., Kato, T., Nakamura, A., Hatano, K., Ito, K., Fukuda, H., Kojima, S., Nakamura, K. (1999). The human amygdala plays an important role in gaze monitoring: A PET studyBrain 122: 779–783

    Article  PubMed  Google Scholar 

  • Kling, A., L. Brothers (1992). The amygdala and social behavior. neurobiological aspects of emotion, memory, and mental dysfunction J. Aggleton, WileyNew York

    Google Scholar 

  • Kling, A., Lancaster, J., Bentone, J. (1970). Amygdalectomy in the free ranging vervet Journal of Psychiatric Research 7: 191–199

    Article  PubMed  CAS  Google Scholar 

  • Kluver H., P. Bucy (1937). “Psychic Blindness” and other symptoms following bilateral temporal lobectomy in rhesus monkeysAmerican Journal of Physiology 119: 352–353

    Google Scholar 

  • LaBar, K., Gatenby, J., Gore, J., LeDoux, J., Phelps, E. (1998). Human amygdala activation during conditioned fear acquisition and extinction: A mixed trial studyNeuron 20: 937–945

    Article  PubMed  CAS  Google Scholar 

  • LaBar, K., LeDoux, J., Spencer, D., Phelps, E. (1995). Impaired fear conditioning following unilateral temporal lobectomyJournal of Neuroscience 15: 6846–6855

    PubMed  CAS  Google Scholar 

  • Lang, P., Bradley, M., Cuthbert, B. (1990). Emotion, attention, and the startle reflex Psychological Review 97(3): 377–395

    Article  PubMed  CAS  Google Scholar 

  • LeDoux J. (1996). The Emotional Brain. Simon & Schuster, New York

    Google Scholar 

  • Lord, C., Rutter M., LeCouteur A. (1994). Autism Diagnostic Interview – Revised: A revised versions of a diagnostic interview for caregivers of individuals with possible pervasive developmental disordersJournal of Autism and Developmental Disorders 24: 659–685

    Article  PubMed  CAS  Google Scholar 

  • Lord, C., Risi S., Lambrecht L., Cook E., Leventhal B., 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(3): 205–223

    Article  PubMed  CAS  Google Scholar 

  • Morgan, C., Grillon, C., Lubin, H., Southwick, S. (1997). Startle abnormalities in women with sexual assault related PTSDAmerican Journal of Psychiatry 154: 1076–1080

    PubMed  Google Scholar 

  • Morris, J., Frith, C., Perrett, D., Rowland, D., Young, A., Calder, A., Dolan, R. (1996). A differential neural response in the human amygdala to fearful and happy facial expressionsNature 383: 812–815

    Article  PubMed  CAS  Google Scholar 

  • Morris, J., Ohman, A., Dolan, R. (1998). Conscious and unconscious emotional learning in the human amygdala. Nature, 393: 467–470

    Article  PubMed  CAS  Google Scholar 

  • Muris, P., Steerneman, P., Merckelbach, H., Holdrinet, I., Meesters, C. (1998). Comorbid anxiety symptoms in children with pervasive developmental disordersJournal of Anxiety Disorders 12: 387–393

    Article  PubMed  CAS  Google Scholar 

  • Murphy, B., Bolton, P., Pickles, A., Fombonne, E., Piven, J., Rutter, M. (2000). Personality traits of the relatives of autistic probandsPsychological Medicine 30(6): 1411–1424

    Article  PubMed  CAS  Google Scholar 

  • Newman, J., J. Bachevalier (1997). Neonatal ablations of the amygdala and inferior temporal cortex alter the vocal response to social separation in rhesus macaquesBrain Research 758(1–2): 180–186

    Article  PubMed  CAS  Google Scholar 

  • Ohman, A. (2002). Automaticity and the amygdala: Nonconscious responses to emotional faces. Current Directions in Psychological Science, 11, 62–66

    Article  Google Scholar 

  • Phelps, E., O’Connor, K.,Cunningham, W., Funayama, E., Gatenby, J., Gore, J., Banaji, M. (2000). Performance on indirect measures of race evaluation predicts amygdala activationJournal of Cognitive Neuroscience 12(5): 729–738

    Article  PubMed  CAS  Google Scholar 

  • Phelps, E., O’Connor, K., Gatenby, J., Gore, J., Grilon, C., davis, M. (2001). Activation of the left amygdala to a cognitive representation of feNatural Neuroscience 4(4): 437–441

    Article  CAS  Google Scholar 

  • Piven, J., (2001). The broad autism phenotype: A complementary strategy for molecular genetic studies of autismAmerican Journal of Medical Genetics 105: 34–35

    Article  PubMed  CAS  Google Scholar 

  • Rosvold, H., Mirsky, A., pribram, K. (1954). Influence of amygdalectomy on social behavior in monkeysJournal of Comparative and Physiological Psychology 47: 173–178

    Article  PubMed  CAS  Google Scholar 

  • Salmond, C., de Haan, M., Friston, K., Gadian, D., Vargha-khadem, F. (2003). Investigating individual differences in brain abnormalities in autismPhilosophical transactions of the Royal Society of London, series B, biological sciences328(405–413

    Article  Google Scholar 

  • Schmolck, H., L. Squire (2001). Impaired perception of facial emotions following bilateral damage to the anterior temporal lobeNeuropsychology 15(1): 30–38

    Article  PubMed  CAS  Google Scholar 

  • Schultz, R., Romanski, L., tsatsanis, K. (2000). Neurofunctional models of autistic disorder and Asperger Syndrome: Clues from neuroimaging In A. Klin, F. Volkmar, S. Sparrow (eds), Asperger syndrome. The Guilford Press, New York, pp. 172–209

    Google Scholar 

  • Sparks, B., Friedman, S., Shaw, D., Aylward, E., Echelard, D., Artru, A., Maravilla, K., Giedd, J., Munson, J., Dawson, G., Dager, S. (2002). Brain structural abnormalities in young children with autism spectrum disorders Neurology 59(2): 184–192

    PubMed  CAS  Google Scholar 

  • Spielberger, C. (2003). Manual for the State-Trait Anxiety Inventory (STAI). Consulting Psychologists Press, PaloAlto, CA

    Google Scholar 

  • Thompson, C., Bergland, R., Towfighi, J. (1977). Social and nonsocial behaviors of adult rhesus monkeys after amygdalectomy in infancy or adulthoodJournal of Comparative and Physiological Psychology 91(533–548)

    Article  PubMed  CAS  Google Scholar 

  • Whalen, P., Rauch, S., Etcoff, N., Mcinerney, S., Lee, M., Jenike, M. (1998). Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledgeThe Journal of Neuroscience 18(1): 411–418

    PubMed  CAS  Google Scholar 

  • Wicker, B., Michel, F., Henaff, M., decety, J. (1998). Brain regions involved in the perception of gaze: A PET studyNeuroimage 8(2): 221–227

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by a program project grant from the National Institute of Child Health and Human Development and the National Institute on Deafness and Communication Disability (PO1HD34565), which is part of the NICHD/NIDCD Collaborative Program of Excellence in Autism, a center grant from the National Institute of Mental Health (U54MH066399), which is part of the NIH STAART Centers Program, and the Cure Autism Now Foundation. We gratefully acknowledge the contributions of individuals who participated in this study and several other people who made significant contributions to this research: James McPartland, Jeff Munson and several undergraduate research assistants.

Author information

Authors and Affiliations

  1. Center on Human Development and Disability, University of Washington, 98195 , Seattle, WA, USA

    Raphael Bernier, Geraldine Dawson, Heracles Panagiotides & Sara Webb

  2. Center on Human Development and Disability, University of Washington, Box 357920, Seattle, WA , 98195, USA

    Raphael Bernier

Authors
  1. Raphael Bernier
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Geraldine Dawson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Heracles Panagiotides
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sara Webb
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raphael Bernier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bernier, R., Dawson, G., Panagiotides, H. et al. Individuals with Autism Spectrum Disorder Show Normal Responses to a Fear Potential Startle Paradigm. J Autism Dev Disord 35, 575–583 (2005). https://doi.org/10.1007/s10803-005-0002-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-005-0002-0

Keywords

Search

Navigation