Abstract
Autism is a pervasive developmental disorder of childhood characterized by deficits in social interaction, language, and stereotyped behaviors along with a restricted range of interests. It is further marked by an inability to perceive and respond to social and emotional signals in a typical manner. This might due to the functional disconnectivity of networks important for specific aspects of social cognition and behavioral control resulting in deficits of sensory information integration. According to several recent theories sensory processing and integration abnormalities may play an important role in impairments of perception, cognition, and behavior in individuals with autism. Among these sensory abnormalities, auditory perception distortion may contribute to many typical symptoms of autism. The present study used Berard’s technique of auditory integration training (AIT) to improve sound integration in children with autism. It also aimed to understand the abnormal neural and functional mechanisms underlying sound processing distortion in autism by incorporating behavioral, psychophysiological and neurophysiological outcomes. It was proposed that exposure to twenty 30-min AIT sessions (total 10 h of training) would result in improved behavioral evaluation scores, improve profile of cardiorespiratory activity, and positively affect both early [N1, mismatch negativity (MMN)] and late (P3) components of evoked potentials in auditory oddball task. Eighteen children with autism spectrum disorder (ASD) participated in the study. A group of 16 typically developing children served as a contrast group in the auditory oddball task. Autonomic outcomes of the study reflected a linear increase of heart rate variability measures and respiration rate. Comparison of evoked potential characteristics of children with ASD versus typically developing children revealed several group difference findings, more specifically, a delayed latency of N1 to rare and frequent stimuli, larger MMN; higher P3a to frequent stimuli, and at the same time delayed latency of P3b to rare stimuli in the autism group. Post-AIT changes in evoked potentials could be summarized as a decreased magnitude of N1 to rare stimuli, marginally lower negativity of MMN, and decrease of the P3a to frequent stimuli along with delayed latency and higher amplitude of the P3b to the rare stimuli. These evoked potential changes following completion of Berard AIT course are in a positive direction, making them less distinct from those recorded in age-matched group of typical children, thus could be considered as changes towards normalization. Parental questionnaires clearly demonstrated improvements in behavioral symptoms such as irritability, hyperactivity, repetitive behaviors and other important behavioral domains. The results of the study propose that more controlled research is necessary to document behavioral and psychophysiological changes resulting from Berard AIT and to provide explanation of the neural mechanisms of how auditory integration training may affect behavior and psychophysiological responses of children with ASD.
Similar content being viewed by others
References
Abdeltawwab, M. M., & Baz, H. (2015). Automatic pre-attentive auditory responses: MMN to tone burst frequency changes in autistic school-age children. Journal of International Advances in Otolaryngology, 11(1), 36–41.
Alho, K. (1995). Cerebral generators of mismatch negativity (MMN) and its magnetic counterpart (MMNm) elicited by sound changes. Ear and Hearing, 16, 38–51.
Aman, M. G. (2004). Management of hyperactivity and other acting out problems in patients with autism spectrum disorder. Seminars in Pediatric Neurology, 11, 225–228.
Aman, M. G. (2012). Aberrant behavior checklist: Current identity and future developments. Clinical and Experimental Pharmacology, 2, e114. doi:10.4172/2161-1459.1000e114.
Aman, M. G., & Singh, N. N. (1986). Aberrant behavior checklist: Manual. East Aurora, NY: Slosson.
Aman, M. G., & Singh, N. N. (1994). Aberrant behavior checklist—Community. Supplementary manual. East Aurora, NY: Slosson Educational Publications.
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (DSM-IV-TR) (text revised) (4th ed.). Washington, DC: American Psychiatric Association.
Ayres, E. G. (2005). Sensory integration and the child. Los Angeles, CA: Western Psychological Services.
Barry, R. J., & James, A. L. (1988). Coding of stimulus parameters in autistic, retarded, and normal children: Evidence for a two-factor theory of autism. International Journal of Psychophysiology, 6, 139–149.
Bartha-Doering, L., Deuster, D., Giordano, V., Zehnhoff-Dinnesen, A., & Dobel, C. (2015). A systematic review of the mismatch negativity as an index for auditory sensory memory: From basic research to clinical and developmental perspectives. Psychophysiology, 52(9), 1115–1130.
Berard, G., & Brockett, S. (2011). Hearing equals behavior: Updated and expanded. Manchester Center, VT: Northshire Press.
Berntson, G., Bigger, J. T., Eckberg, D., Grossman, P., et al. (1997). Heart rate variability: Origins, methods and interpretive caveates. Psychophysiology, 34, 623–648.
Bihm, E. M., & Poindexter, A. R. (1991). Cross-validation of the factor structure of the Aberrant Behavior Checklist for persons with mental retardation. American Journal of Mental Retardation, 96, 209–211.
Bluestone, J. (2004). The fabric of autism: Weaving the threads into a cogent theory. Seattle: The HANDLE Institute.
Bodfish, J. W., Symons, F. J., & Lewis, M. H. (1999). Repetitive behavior scale. Western Carolina Center Research Reports.
Bodfish, J. W., Symons, F. S., Parker, D. E., & Lewis, M. H. (2000). Varieties of repetitive behavior in autism: Comparisons to mental retardation. Journal of Autism and Developmental Disorders, 30, 237–243.
Bomba, M., & Pang, E. W. (2004). Cortical auditory evoked potentials in autism: A review. International Journal of Psychophysiology, 53, 161–168.
Boucsein, W. (2012). Electrodermal activity. New York: Plenum Press.
Brandwein, A. B., Foxe, J. J., Butler, J. S., Frey, H. P., Bates, J. C., Shulman, L. H., et al. (2015). Neurophysiological indices of atypical auditory processing and multisensory integration are associated with symptom severity in autism. Journal of Autism and Developmental Disorders, 45(1), 230–244.
Brock, J., Brown, C. C., Boucher, J., & Rippon, G. (2002). The temporal binding deficit hypothesis of autism. Developmental Psychopathology, 14, 209–224.
Brockett, S. (2012). Comprehensive performance index (CPI). North Haven, CT: IDEA Training Center Publication.
Brockett, S., Lawton-Shirley, N., & Giencke-Kimball, J. (2014). Berard auditory integration training: Behavior changes related to sensory modulation. Autism Insights, 6, 1–10. doi:10.4137/AUI.S13574.
Brown, M. M. (1999). Auditory integration training and autism: Two case studies. British Journal of Occupational Therapy, 62, 13–18.
Brown, E., Aman, M. G., & Havercamp, S. M. (2002). Factor analysis and norms for parent ratings on the Aberrant Behavior Checklist-Community for young people in special education. Research in Developmental Disabilities, 23, 45–60.
Bruneau, N., Roux, S., Adrien, J. L., & Barthelemy, C. (1999). Auditory associative cortex dysfunction in children with autism: Evidence from late auditory evoked potentials (N1 wave–T Complex). Clinical Neurophysiology, 110, 1927–1934.
Bruneau, N., Roux, S., Guerin, P., Barthelemy, C., & Lelord, G. (1997). Temporal prominence of auditory evoked potentials (N1 wave) in 4–8 year old children. Psychophysiology, 34, 32–38.
Buchwald, J. S., Erwin, R., Van Lancker, D., Guthrie, D., Schwafel, J., & Tanguay, P. (1992). Midlatency auditory evoked responses: P1 abnormalities in adult autistic subjects. Electroencephalography and Clinical Neurophysiology, 84, 164–171.
Bundy, A., Lane, S., & Murray, E. (2002). Sensory integration theory and practice (2nd ed.). Philadelphia, PA: F. A. Davis Company.
Ceponiene, R., Lepisto, T., Shestakova, A., Vanhala, R., Alku, P., Naatanen, R., et al. (2003). Speech-sound-selectiveauditory impairment in children with autism: They can perceive but do not attend. Proceedings of the National Academy of Sciences, 100, 5567–5572.
Ciesielski, K. T., Courchesne, E., & Elmasian, R. (1990). Effects of focused selective attention tasks on event-related potentials in autistic and normal individuals. Electroencephalography and Clinical Neurophysiology, 75, 207–220.
Courchesne, E., Lincoln, A. J., Kilman, B. A., & Galambos, R. (1985). Event-related brain potential correlates of the processing of novel visual and auditory information in autism. Journal Autism Developmental Disorders, 15, 55–76.
Dawson, G., Finley, C., Phillips, S., Galpert, L., & Lewy, A. (1988). Reduced P3 amplitude of the event-related brain potential: Its relationship to language ability in autism. Journal Autism Developmental Disorders, 18, 493–504.
Donchin, E. (1981). Surprise!…surprise? Psychophysiology, 18, 493–513.
Dunn, M. A., Gomes, H., & Gravel, J. (2008). Mismatch Negativity in children with autism and typical development. Journal of Autism Developmental Disorders, 38, 52–71.
Edelson, S. M., Arin, D., Bauma, M., Lukas, S. E., Rudy, J. H., Sholar, M., et al. (1999). Auditory integration training: A double-blind study of behavioral and electrophysiological effects in people with autism. Focus on Autism and Other Developmental Disabilities, 14(2), 73–81.
Fan, Y. T., & Cheng, Y. (2014). Atypical mismatch negativity in response to emotional voices in people with autism spectrum conditions. PLoS One, 9(7), e102471.
Ferri, R., Elia, M., Agarwal, N., Lanuzza, B., Musumeci, S. A., & Pennisi, G. (2003). The mismatch negativity and the P3a components of the auditory event-related potentials in autistic low functioning subjects. Clinical Neurophysiology, 114, 1671–1680.
Fishman, Y. (2014). The mechanisms and meaning of the mismatch negativity. Brain Topography, 27(4), 500–526.
Giard, M. H., Perrin, F., Pernier, J., & Bouchet, P. (1990). Brain generators implicated in the processing of auditory stimulus deviance: A topographic event-related potential study. Psychophysiology, 27, 627–640.
Goldstein, G., Johnson, C. R., & Minshew, N. J. (2001). Attentional processes in autism. Journal of Autism and Developmental Disorders, 31, 433–440.
Gomot, M., Giard, M. H., Adrien, J. L., Barthelemy, C., & Bruneau, N. (2002). Hypersensitivity to acoustic change in children with autism: Electrophysiological evidence of left frontal cortex dysfunctioning. Psychophysiology, 39, 577–584.
Hirstein, W., Iversen, P., & Ramachandran, V. S. (2001). Autonomic responses of autistic children to people and objects. Proceedings of Royal Society (London), Biological Sciences, 268(1479), 1883–1888.
Jansson-Verkasalo, E., Cieponiene, R., Kielinen, M., Suominen, K., Jantti, V., Linna, S., et al. (2003). Deficient auditory processing in children with Asperger Syndrome, indexed by event-related potentials. Neuroscience Letters, 338, 197–200.
Jeste, S. S., & Nelson, C. A. (2009). Event related potentials in the understanding of autism spectrum disorders: An analytical review. Journal of Autism and Developmental Disorders, 39(3), 495–510.
Julu, P. O., Kerr, A. M., Apartipoulos, F., Al-Rawas, S., Engerstrom, I. W., et al. (2001). Characterisation of breathing and associated central autonomic dysfunction in the Rett disorder. Archives of Disorders Child, 85, 29–37.
Katayma, J., & Polich, J. (1996). P300 from one-, two-, and three-stimulus auditory paradigms. International Journal of Psychophysiology, 23, 33–40.
Kemner, C., Verbaten, M. N., Cuperus, J. M., Camfferman, G., & van Engeland, H. (1995). Auditory event-related brain potentials in autistic children and three different control groups. Biological Psychiatry, 38, 150–165.
Kraus, N., McGee, T., Carrell, T. D., Zecker, S. G., Nicol, T. G., & Koch, D. B. (1996). Auditory neurophysiologic responses and discrimination deficits in children with learning problems. Science, 273, 971–973.
Kujala, T., Lepistö, T., Nieminen-von Wendt, T., Näätänen, P., & Näätänen, R. (2005). Neurophysiological evidence for cortical discrimination impairment of prosody in Asperger syndrome. Neuroscience Letters, 383(3), 260–265.
Lam, K. S., & Aman, M. G. (2007). The Repetitive Behavior Scale-Revised: Independent validation in individuals with Autism Spectrum Disorders. Journal of Autism and Developmental Disorders, 37, 855–866.
Lam, K. S., Bodfish, J., & Piven, J. (2008). Evidence for three subtypes of repetitive behavior in autism that differ in familiarity and association with other symptoms. Journal of Child Psychology and Psychiatry, 49, 1193–1200.
Le Couteur, A., Lord, C., & Rutter, M. (2003). The autism diagnostic interview—Revised (ADI-R). Los Angeles, CA: Western Psychological Services.
Lepistö, T., Silokallio, S., Nieminen-von Wendt, T., Alku, P., Näätänen, R., & Kujala, T. (2006). Auditory perception and attention as reflected by the brain event-related potentials in children with Asperger syndrome. Clinical Neurophysiology, 117(10), 2161–2171.
Lincoln, A. J., Courchesne, E., Harms, L., & Allen, M. (1993). Contextual probability evaluation in autistic, receptive developmental language disorder and control children: Event-related brain potential evidence. Journal Autism Developmental Disorders, 23, 37–58.
Ludlow, A., Mohr, B., Whitmore, A., Garagnani, M., Pulvermüller, F., & Gutierrez, R. (2014). Auditory processing and sensory behaviours in children with autism spectrum disorders as revealed by mismatch negativity. Brain Cognition, 86, 55–63.
McKean, T. A. (1994). Soon will come the light. Arlington, TX: Future Education, Inc.
Ming, X., Julu, P. O., Brimacombe, M., Connor, S., & Daniels, M. L. (2005). Reduced cardiac parasympathetic activity in children with autism. Brain Development, 27(7), 509–516.
Mirenda, P., Smith, I. M., Vaillancourt, T., Georgiades, S., Duku, E., Szatmari, P., et al. (2010). Validating the Repetitive Behavior Scale-Revised in young children with Autism Spectrum Disorder. Journal of Autism and Developmental Disorders, 40, 1521–1530.
Movius, H., & Allen, J. (2005). Cardiac vagal tone, defensiveness, motivational style. BiolPsychol, 68, 147–162.
Näätänen, R. (1990). The role of attention in auditory information processing as revealed by ERPs and other brain measures of cognitive function. Behavioral Brain Sciences, 13, 201–288.
Näätänen, R., & Alho, K. (1997). Mismatch negativity—The measure for central sound representation accuracy. Audiology & Neuro-Otology, 2, 341–353.
Näätänen, R., Jacobsen, T., & Winkler, I. (2005). Memory-based or afferent processes in mismatch negativity (MMN): A review of the evidence. Psychophysiology, 42, 25–32.
Näätänen, R., Paavilainen, P., Rinne, T., & Alho, K. (2007). The mismatch negativity (MMN) in basic research of central auditory processing: A review. Clinical Neurophysiology, 118(12), 2544–2590.
Näätänen, R., & Picton, T. W. (1987). The N1 wave of the human electric and magnetic response to sound. A review and an analysis of the component structure. Psychophysiology, 24, 375–425.
Novick, B., Vaughan, H. G., Jr., Kurtzberg, D., & Simson, R. (1980). An electrophysiologic indication of auditory processing defects in autism. Psychiatry Research, 3, 107–114.
O’Connor, K. (2012). Auditory processing in autism spectrum disorder: A review. Neuroscience and Biobehavioral Reviews, 36, 836–854.
Oades, R. D., Walker, M. K., Geffen, L. B., & Stern, L. M. (1988). Event related potentials in autistic and healthy children on an auditory choice reaction task. International Journal Psychophysiology, 6, 25–37.
Orekhova, E. V., & Stroganova, T. A. (2014). Arousal and attention re-orienting in autism spectrum disorders: Evidence from auditory event-related potentials. Frontiers in Human Neuroscience, 8, 34.
Orekhova, E. V., Stroganova, T. A., Prokofiev, A. O., Nygren, G., Gillberg, C., & Elam, M. (2009). The right hemisphere fails to respond to temporal novelty in autism: Evidence from an ERP study. Clinical Neurophysiology, 120(3), 520–529.
Ornitz, E. M. (1989). Autism at the interface between sensory and information processing. In G. Dawson (Ed.), Autism: Nature, diagnosis, and treatment (pp. 174–207). New York: Guilford Press.
Palkovitz, R. J., & Wiesenfeld, A. R. (1980). Differential autonomic responses of autistic and normal children. Journal of Autism Developmental Disorders, 10, 347–360.
Picton, T. W. (1992). The P300 wave of the human event-related potential. Journal Clinical Neurophysiology, 9, 456–479.
Picton, T. W., Alain, C., Otten, L., Ritter, W., & Achim, A. (2000). Mismatch negativity: Different water in the same river. Audiology Neuro-otology, 5, 111–139.
Porges, S. (1995). Orienting in defensive world: Mammalian modifications of our evolutionary heritage, a polyvagal theory. Psychophysiology, 32, 301–318.
Porges, S. W. (2003). The polyvagal theory. Physiology Behavior, 79, 503–513.
Powers, M. D. (2000). Children with autism: A parents’ guide. Bethesda: Woodbine House.
Rimland, B., & Edelson, S. (1994). The effects of auditory integration training on autism. Journal of Speech—Language Pathology, 3, 16–24.
Rimland, B., & Edelson, S. (1995). Auditory integration training: A pilot study. Journal Autism Developmental Disorders, 25, 61–70.
Rosentall, U., Nordin, V., Branberg, K., & Gillberg, C. (2003). Autism and auditory brain stem. Ear and Hearing, 24, 206–214.
Sams, M., Paavilainen, P., Alho, K., & Naatanen, R. (1985). Auditory frequency discrimination and event-related potentials. Electroencephalography and Clinical Neurophysiology, 62, 437–448.
Samson, F., Mottron, L., Jemel, B., Belin, P., & Ciocca, V. (2006). Can spectro-temporal complexity explain the autistic pattern of performance on auditory tasks? Journal of Autism and Developmental Disorders, 36(1), 65–76.
Schall, U. (2015). Is it time to move mismatch negativity into the clinic? Biological Psychology. doi:10.1016/j.biopsycho.2015.09.001.
Schoeneck, L. (2012). iLS case study: Autism, ADHD. Accessed June 5, 2012, from http://www.integratedlistening.com/ils-case-autism-adhd.
Seri, S., Cerquiglini, A., Pisani, F., & Curatolo, P. (1999). Autism in tuberous sclerosis: Evoked potential evidence for a deficit in auditory sensory processing. Clinical Neurophysiology, 110, 1825–1830.
Stroganova, T. A., Kozunov, V. V., Posikera, I. N., Galuta, I. A., Gratchev, V. V., & Orekhova, E. V. (2013). Abnormal pre-attentive arousal in young children with autism spectrum disorder contributes to their atypical auditory behavior: An ERP study. PLoS One, 8(7), e69100.
Tecchio, F., Benassi, F., Zappasodi, F., Gialloreti, L. E., Palermo, M., Seri, S., et al. (2003). Auditory sensory processing in autism: A magnetoencephalographic study. Biological Psychiatry, 54(6), 647–654.
Van Engeland, H. (1984). The electrodermal orienting response to auditive stimuli in autistic children, normal children, mentally retarded children, and child psychiatric patients. Journal Autism Developmental Disorders, 14, 261–279.
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence (WASI). San Antonio, TX: Psychological Corporation.
Wechsler, D. (2003). Wechsler Intelligence Scale for Children (4th ed.). San Antonio, TX: Psychological Corporation.
Acknowledgments
This study was funded by the Autism Research Institute (ARI, San Diego, CA) pilot research Grant ARI-03.2012 to Estate M. Sokhadze.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors do not have any potential conflict of interest to disclose. All authors therefore declare that they do not have any conflict of interests.
Ethical Approval
All procedures performed in this study that involved human subjects were in accordance with the ethical standards of the institutional research committee (IRB) and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The protocol of the study was approved by the University of Louisville IRB. Signed informed consent forms (from parents) and informed assent forms (from children) were obtained from all individual participants and parents of children included in the study. The results of the study propose that more controlled research is necessary to document behavioral and psychophysiological changes resulting from Berard AIT and to provide explanation of the neural mechanisms of how auditory integration training may affect behavior and psychophysiological responses of children with ASD.
Rights and permissions
About this article
Cite this article
Sokhadze, E.M., Casanova, M.F., Tasman, A. et al. Electrophysiological and Behavioral Outcomes of Berard Auditory Integration Training (AIT) in Children with Autism Spectrum Disorder. Appl Psychophysiol Biofeedback 41, 405–420 (2016). https://doi.org/10.1007/s10484-016-9343-z
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10484-016-9343-z