Neuromodulation based on rTMS affects behavioral measures and autonomic nervous system activity in children with autism

Authors

  • Guela Sokhadze Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY
  • Manuel F Casanova Smart State Endowed Chair in Childhood Neurotherapeutics, Professor of Biomedical Sciences, University of South Carolina School of Medicine Greenville Campus, Greenville, SC
  • Desmond Kelly Dr Kelly is Vice-Chair for Academic Affairs at Department of Pediatrics at Children's Hospital of Greenville Health System, Greenville, SC
  • Emily Casanova Dr Emily Casanova is post-doctoral fellow at University of South Carolina School of Medicine-Greenville
  • Brook Russell Dr Russell is assistant professor of statistics at Clemson University, Clemson, SC
  • Estate M Sokhadze Department of Biomedical Sciences University of South Carolina School of Medicine-Greenville, Greenvile, SC 29615

DOI:

https://doi.org/10.15540/nr.4.2.65

Keywords:

TMS, HRV, Skin conductance, autism, behavior

Abstract

Many children with autism spectrum disorder (ASD) exhibit symptoms associated with autonomic nervous system (ANS) dysfunction indicative of low psychophysiological flexibility.  It is suggested that ASD symptoms are associated with generalized abnormalities in the central nervous system, including structures and networks involved in the top-down regulation of the ANS. Repetitive transcranial magnetic stimulation (rTMS) has been suggested as a possible therapy to target ANS regulation deficits in ASD. In the current study we used neuromodulation based on rTMS over the dorsolateral prefrontal cortex (DLPFC) to reduce sympathetic arousal and increase parasympathetic activity in children with ASD. In a study on 27 children with autism we administered weekly 0.5 Hz rTMS bilaterally over the DLPFC with concurrent recording of autonomic activity.  Statistical analysis of time and frequency domain heart rate variability (HRV) indices and skin conductance level (SCL) revealed a strong linear regression of most HRV and SCL measures. Several parental behavioral rating scores improved post-TMS and showed a correlation with autonomic outcomes, in particular parasympathetic indices of HRV negatively correlated with repetitive and stereotyped behaviors, while sympathetic arousal indices showed positive correlation with the same behaviors.  The paper discusses potential neurobiological mechanisms involved in post-TMS autonomic balance and aberrant behavior improvements.

Author Biographies

Guela Sokhadze, Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY

Guela is graduate student (PhD candidate) at Department of Anatomical Sciences and Neurobiology, University of Louisville, Louisville, KY. He holds MS from University of Louisville.

Manuel F Casanova, Smart State Endowed Chair in Childhood Neurotherapeutics, Professor of Biomedical Sciences, University of South Carolina School of Medicine Greenville Campus, Greenville, SC

Dr Casanova is Smart State Endowed Chair in Childhood Neurotherapeutics, Professor of Biomedical Sciences, University of South Carolina School of Medicine Greenville Campus, Greenville, SC. He is specialist in neuropathology and psychiatry, author of numerous publications on autism and other psychiatric disorders. 

Desmond Kelly, Dr Kelly is Vice-Chair for Academic Affairs at Department of Pediatrics at Children's Hospital of Greenville Health System, Greenville, SC

Vice-Chair for Academic Affairs at Department of Pediatrics at Children's Hospital of Greenville Health System, Greenville, SC,

Dr Kelly is Clinical Professor of Pediatrics at University of South Carolina School of Medicine, Greenville, SC

Emily Casanova, Dr Emily Casanova is post-doctoral fellow at University of South Carolina School of Medicine-Greenville

Dr Emily Casanova is post-doctoral fellow
at University of South Carolina School of Medicine-Greenville, Department of Biomedical Sciences

Brook Russell, Dr Russell is assistant professor of statistics at Clemson University, Clemson, SC

Dr Russell is assistant professor of statistics at Clemson University, Clemson, SC

Estate M Sokhadze, Department of Biomedical Sciences University of South Carolina School of Medicine-Greenville, Greenvile, SC 29615

Research professor, Department of Biomedical Sciences, University of South Carolina School of Medicine-Greenville, Greenville, SC, 29615

Gratis associate professor, Department of Psychiatry & behavioral Sciences, University of Louisville, Louisville, KY 40202

References

American Psychiatric Association (2013). Diagnostic and statistical manual of mental disorders, fifth edition. Washington, DC. http://dx.doi.org/10.1176/appi.books.9780890425596

Althaus, M., Mulder, L. J., Mulder, G., Aarnoudse, C., & Minderaa, R. (1999). Cardiac adaptivity to attention-demanding tasks in children with a pervasive developmental disorder not otherwise specified (PDD-NOS). Biological Psychiatry, 46(6), 799-809. http://dx.doi.org/10.1016/S0006-3223(98)00374-6

Aman, M. G., & Singh, N. N. (1994). Aberrant Behavior Checklist - Community. Supplementary Manual. East Aurora, NY: Slosson Educational Publications.

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(2), 139-149. http://dx.doi.org/10.1016/0167-8760(88)90045-1

Baruth, J., Casanova, M., El-Baz, A., Horrell, T., Mathai, G., Sears, L., & Sokhadze, E. (2010). Low-frequency repetitive transcranial magnetic stimulation modulates evoked-gamma frequency oscillations in autism spectrum disorders. Journal of Neurotherapy, 14(3), 179-194. http://dx.doi.org/10.1080/10874208.2010.501500

Baruth, J., Williams, E., Sokhadze, E., El-Baz, A., Sears, L., & Casanova, M. F. (2011). Repetitive transcranial stimulation (rTMS) improves electroencephalographic and behavioral outcome measures in autism spectrum disorders (ASD). Autism Science Digest, 1(1), 52-57.

Bachevalier, J., & Loveland, K. A. (2006). The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism. Neuroscience Biobehavioral Reviews, 30(1), 97-117. http://dx.doi.org/10.1016/j.neubiorev.2005.07.002

Benevides, T. W., & Lane, S. J. (2015). A review of cardiac autonomic measures: considerations for examination of physiological response in children with autism spectrum disorder. Journal Autism and Developmental Disorders, 45(2), 560-575. http://dx.doi.org/10.1007/s10803-013-1971-z

Ben-Shachar, D., Belmaker, R. H., Grisaru, N., & Klein, E. (1997). Transcranial magnetic stimulation induces alterations in brain monoamines. Journal of Neural Transmission, 104(2-3), 191-197. http://dx.doi.org/10.1007/BF01273180

Berntson, G., Bigger, J. T., Eckberg, D., Grossman, P., Kaufmann P. G., Malik, M., ... Van der Molen, M. W. (1997). Heart rate variability: origins, methods and interpretive caveates. Psychophysiology, 34(6), 623-648. http://dx.doi.org/10.1111/j.1469-8986.1997.tb02140.x

Bodfish, J. W., Symons, F. J., & Lewis, J. (1999). Repetitive Behavior Scale. Western Carolina Center Research Reports.

Boucsein, W. (2012). Electrodermal activity (2nd ed.) New York: Springer. http://dx.doi.org/10.1007/978-1-4614-1126-0

Casanova, M. F. (2005). Minicolumnar pathology in autism. In M. F. Casanova (ed.), Recent developments in autism research (pp.133-144). New York: Nova Biomedical Books.

Casanova, M. F. (2006). Neuropathological and genetic findings in autism: the significance of a putative minicolumnopathy. Neuroscientist, 12(5), 435-441. http://dx.doi.org/10.1177/1073858406290375

Casanova, M. F., Buxhoeveden, D. P., & Brown, C. (2002). Clinical and macroscopic correlates of minicolumnar pathology in autism. Journal of Child Neurology, 17(9), 692-695. http://dx.doi.org/10.1177/088307380201700908

Casanova, M. F., van Kooten, I. A., Switala, A. E., van England, H., Heinsen, H., Steinbusch, H. W., ... Schmitz, C. (2006). Minicolumnar abnormalities in autism. Acta Neuropathologica, 112(3), 287-303. http://dx.doi.org/10.1007/s00401-006-0085-5

Casanova, M. F., Baruth, J., El-Baz, A., Tasman, A., Sears, L., & Sokhadze, E. (2012). Repetitive transcranial magnetic stimulation (rTMS) modulates event-related potential (ERP) indices of attention in autism. Translational Neuroscience,3(2), 170-180. http://dx.doi.org/10.2478/s13380-012-0022-0

Casanova, M. F., Hensley, M. K., Sokhadze, E. M., El-Baz, A. S., Wang, Y, Li, X., & Sears, L. (2014). Effects of weekly low-frequency rTMS on autonomic measures in children with autism spectrum disorder. Frontiers in Human Neuroscience, 8. http://dx.doi.org/10.3389/fnhum.2014.00851

Casanova, M. F., Sokhadze, E., Opris, I., Wang, Y., & Li, X. (2015). Autism spectrum disorders: linking neuropathological findings to treatment with transcranial magnetic stimulation. Acta Paediatrica, 104(4), 346-355. http://dx.doi.org/10.1111/apa.12943

Chang, M. C., Parham, L. D., Blanche, E. I., Schell, A., Chou, C. P., Dawson, M., & Clark, F. (2012). Autonomic and behavioral responses of children with autism to auditory stimuli. American Journal of Occupational Therapy, 66(5), 567-576. http://dx.doi.org/10.5014/ajot.2012.004242

Cohen, N., Benjamin, J., Geva, A. B., Matar, M. A., Kaplan, Z., & Kotler, M. (2000). Autonomic dysregulation in panic disorder and in post-traumatic stress disorder: application of power spectrum analysis of heart rate variability at rest and in response to recollection of trauma or panic attack. Psychiatry Research, 96(1), 1-13. http://dx.doi.org/10.1016/S0165-1781(00)00195-5

Cohen, S., Masyn, K., Mastergeorge, A., & Hessl, D. (2015). Psychophysiological responses to emotional stimuli in children and adolescents with autism and fragile X syndrome. Journal of Clinical Child and Adolescent Psychology, 44(2), 250-263. http://dx.doi.org/10.1080/15374416.2013.843462

Constantino, J. N., & Gruber, C. P. (2005). The Social Responsiveness Scale (SRS) Manual. Los Angeles, CA: Western Psychological Services.

Coronoa, R., Dissanayake, C., Arbelle, S., Wellington, P., & Sigman, M. (1998). Is affect aversive to young children with autism? Behavioral and cardiac responses to experimenter distress. Child Development, 69(6), 1494-1502. http://dx.doi.org/10.1111/j.1467-8624.1998.tb06172.x

Critchley, H. D. (2005).Neural mechanisms of autonomic, affective, and cognitive integration. Journal of Comparative Neurology, 493(1), 154-166.

http://dx.doi.org/10.1002/cne.20749

Czéh, B., Welt, T., Fischer, A. K., Erhardt, A., Schmitt, W., Müller, M. B., ... Keck, M. E. (2002). Chronic psychosocial stress and concomitant repetitive transcranial magnetic stimulation: effects on stress hormone levels and adult hippocampal neurogenesis. Biological Psychiatry, 52(11), 1057-1065. http://dx.doi.org/10.1016/S0006-3223(02)01457-9

Damasio, A. R. (1996). The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philosophical Transactions of the Royal Society of London, Biological Sciences, 351(1346), 1413-1420. http://dx.doi.org/10.1098/rstb.1996.0125

Dombroski, B., Kaplan, M., Kotsamanidis-Burg, B., Edelson, S. M., Hensley, M. K., Sokhadze, E.M., & Casanova, M. F. (2014). Effects of ambient prism lenses and visual-motor training on heart rate variability and behavioral outcomes in autism. In K. Siri and T. Lyons (eds.), Cutting-edge therapies for autism (4th ed.) (pp.138-150). New York, NY: Skyhorse Publishing.

Friedman, B. H., & Thayer, J. F. (1998). Anxiety and autonomic flexibility: a cardiovascular approach. Biological Psychology, 49(3), 303-323. http://dx.doi.org/10.1016/S0301-0511(98)00051-9

Filippi, M. M., Oliveri, M., Vernieri, F., Pasqualetti, P., & Rossini, P. M. (2000). Are autonomic signals influencing cortico-spinal motor excitability? A study with transcranial magnetic stimulation. Brain Research, 881(2), 159-164. http://dx.doi.org/10.1016/S0006-8993(00)02837-7

Friedman, B. H. (2007). An autonomic flexibility-neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology,74(2),185-199. http://dx.doi.org/10.1016/j.biopsycho.2005.08.009

George, M. S., Lisanby, S. H., & Sackeim, H. A. (1999). Transcranial magnetic stimulation: applications in neuropsychiatry. Archives of General Psychiatry, 56(4), 300-311. http://dx.doi.org/10.1001/archpsyc.56.4.300

Gillott, A., Furniss, F., & Walter, A. (2001). Anxiety in high-functioning children with autism. Autism, 5(3), 277-286. http://dx.doi.org/10.1177/1362361301005003005

Hedges, D. W., Salyer, D. L., Higginbotham, B. J., Lund, T. D., Hellewell, J. L., Ferguson, D., & Lephart, E. D. (2002). Transcranial magnetic stimulation (TMS) effects on testosterone, prolactin, and corticosterone in adult male rats. Biological Psychiatry, 51(5), 417-421. http://dx.doi.org/10.1016/S0006-3223(01)01266-5

Helverschou, S. B., & Martinsen, H. (2011). Anxiety in people diagnosed with autism and intellectual disability: recognition and phenomenology. Research in Autism Spectrum Disorders, 5(1), 377-387. http://dx.doi.org/10.1016/j.rasd.2010.05.003

Hensley, M., El-Baz, A., Sokhadze, G., Sears, L., Casanova, M. F., & Sokhadze, E. M. (2012). TMS effects on cardiac autonomic control in children with autism. Psychophysiology, 49, S40.

Hensley, M., El-Baz, A., Casanova, M. F., & Sokhadze, E. (2013). Heart rate variability and cardiac autonomic measures changes during rTMS in autism. Applied Psychophysiology Biofeedback, 38, 238.

Hirstein, W., Iversen, P., & Ramachandran, V. S. (2001). Autonomic responses of autistic children to people and objects. Proceedings of the Royal Society of London, Biological Sciences, 268 (1479), 1883-1888. http://dx.doi.org/10.1098/rspb.2001.1724

Holsboer, F. (2000). The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology, 23(5), 477-501. http://dx.doi.org/10.1016/S0893-133X(00)00159-7

Hutt, C., Forrest, S. J., & Richer, J. (1975). Cardiac arrhythmia and behavior in autistic children. Acta Psychiatrica Scandinaica, 51(5), 361-372. http://dx.doi.org/10.1111/j.1600-0447.1975.tb00014.x

Jansen, L. M., Gispen-de Wied, C. C., van der Gaag, R. J., ten Hove, F., Willemsen-Swinkels, S. W. M., Harteveld, E., & van Engeland, H. (2000). Unresponsiveness to psychosocial stress in a group of autistic-like children, multiple complex developmental disorder. Psychoneuroendocrinology, 25(8), 753-764. http://dx.doi.org/10.1016/S0306-4530(00)00020-2

Jenkins, J., Shajahan, P. M., Lappin, J. M., & Ebmeier, K. P. (2002). Right and left prefrontal transcranial magnetic stimulation at 1 Hz does not affect mood in healthy volunteers. BMC Psychiatry, 2(1). http://dx.doi.org/10.1186/1471-244X-2-1

Julu, P. O., Kerr, A. M., Apartipoulos, F., Al-Rawas, S., Engerström, I. W., Engerström, L., ... Hansen, S. (2001). Characterization of breathing and associated central autonomic dysfunction in the Rett disorder. Archives of Disease in Childhood, 85(1), 29-37. http://dx.doi.org/10.1136/adc.85.1.29

Keehn, B., Müller, R. A., & Townsend, J. (2013). Atypical attentional networks and the emergence of autism. Neuroscience and Biobehavioral Reviews, 37(2), 164-183. http://dx.doi.org/10.1016/j.neubiorev.2012.11.014

Kleberg, J. L. (2015). Resting state arousal and functional connectivity in autism spectrum disorder. Journal of Neurophysiology, 113(9), 3035-3037. http://dx.doi.org/10.1152/jn.00292.2014

Kleiger, R. E., Stein, P. K., & Bigger, J. T. Jr. (2005). Heart rate variability: measurement and clinical utility. Annals of Noninvasive Electrocardiology, 10(1), 88-101. http://dx.doi.org/10.1111/j.1542-474X.2005.10101.x

Kushki, A., Drumm, E., Mobarak, M. P., Tanel, N., Dupius, A., Chau, T., & Anagnostou, E. (2013). Investigating the autonomic nervous system response to anxiety in children with autism spectrum disorders. PLoS One, 8(4), e59730.

http://dx.doi.org/10.1371/journal.pone.0059730

Kushki, A., Brian, J., Dupius, A., & Anagnostou, E. (2014). Functional autonomic nervous system profile in children with autism spectrum disorder. Molecular Autism, 5(1), 39. http://dx.doi.org/10.1186/2040-2392-5-39

Lacey J. I., & Lacey, B. C. (1970). Some autonomic-central nervous system interrelationships. In P. Black (ed.), Physiological correlates of emotion (pp. 214-236). New York: Academic Press. http://dx.doi.org/10.1016/B978-0-12-102850-3.50016-5

Le Couteur, A., Lord, C., & Rutter, M. (2003). The autism diagnostic interview – revised (ADI-R). Los Angeles, CA: Western Psychological Services.

Liss, M., Saulnier, C., Fein, D., & Kinsbourne, M. (2006). Sensory and attention abnormalities in autistic spectrum disorders. Autism, 10(2), 155-172. http://dx.doi.org/10.1177/1362361306062021

Loveland, K. A., Bachevalier, J., Pearson, D. A., & Lane, D. M. (2008). Fronto-limbic functioning in children and adolescents with and without autism. Neuropsychologia, 46(1), 49-62. http://dx.doi.org/10.1016/j.neuropsychologia.2007.08.017

Malliani, A., Pagani, M., & Lombardi, F. (1994). Physiology and clinical implications of variability of cardiovascular parameters with focus on heart rate and blood pressure. American Journal of Cardiology, 73(10), C3-C9. http://dx.doi.org/10.1016/0002-9149(94)90617-3

Ming, X., Julu, P. O., Wark, J., Apartopoulos, F., & Hansen, S. (2004). Discordant mental and physical efforts in an autistic patient. Brain & Development, 26(8), 519-524. http://dx.doi.org/10.1016/j.braindev.2004.02.005

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. http://dx.doi.org/10.1016/j.braindev.2005.01.003

Ming, X., Bain, J. M., Smith, D., Brimacombe, M., Gold von-Simson, G., & Axelrod, F. B. (2011). Assessing autonomic dysfunction symptoms in children: a pilot study. Journal of Child Neurology, 26(4), 420-427. http://dx.doi.org/10.1177/0883073810381921

Ming, X., Patel, R., Kang, V., Chokroverty, S., & Julu, P. O. (2016). Respiratory an autonomic dysfunction in children with autism spectrum disorders. Brain & Development, 38(2), 225-232. http://dx.doi.org/10.1016/j.braindev.2015.07.003

Mountcastle, V. B. (2003). Introduction. Computation in cortical columns. Cerebral Cortex, 13(1), 2-4. http://dx.doi.org/10.1093/cercor/13.1.2

Movius, H. L., & Allen, J. J. (2005). Cardiac vagal tone, defensiveness, and motivational style. Biological Psychology, 68(2), 147-162. http://dx.doi.org/10.1016/j.biopsycho.2004.03.019

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. http://dx.doi.org/10.3389/fnhum.2014.00034

Pagani, M., Lombardi, F., Guzzetti, S., Rimoldi, O., Furlan, R., Pizzinelli, P., ... Piccaluga, E. (1986). Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog. Circulation Research, 59(2), 178-193. http://dx.doi.org/10.1161/01.RES.59.2.178

Palkovitz, R. J., & Wiesenfeld, A. R. (1980). Differential autonomic responses of autistic and normal children. Journal of Autism and Developmental Disorders, 10(3), 347-360. http://dx.doi.org/10.1007/BF02408294

Pascual-Leone, A., Walsh, V., & Rothwell, J. (2000). Transcranial magnetic stimulation in cognitive neuroscience--virtual lesion, chronometry, and functional connectivity. Current Opinion in Neurobiology, 10(2), 232-237. http://dx.doi.org/10.1016/S0959-4388(00)00081-7

Patriquin, M. A., Lorenzi, J., & Scarpa, A. (2013). Relationship between respiratory sinus arrhythmia, heart period, and caregiver-reported language and cognitive delays in children with autism spectrum disorders. Applied Psychophysiology and Biofeedback, 38(3), 203-207. http://dx.doi.org/10.1007/s10484-013-9225-6

Paus, T., Jech, R., Thompson, C. J., Comeau, R., Peters, T., & Evans, A. C. (1997). Transcranial magnetic stimulation during positron emission tomography: a new method for studying connectivity of the human cerebral cortex. Journal of Neuroscience, 17(9), 3178-3184.

Porges , S. (1995). Orienting in a defensive world: mammalian modifications of our evolutionary heritage. A polyvagal theory. Psychophysiology, 32(4), 301-318.

http://dx.doi.org/10.1111/j.1469-8986.1995.tb01213.x

Porges, S. W. (2003). The polyvagal theory: phylogenetic contributions to social behavior. Physiology & Behavior, 79(3), 503-513. http://dx.doi.org/10.1016/S0031-9384(03)00156-2

Porges, S. W. (2011). The polyvagal theory: neurophysiological foundations of emotions, attachment, communication, and self-regulation. New York: WW Norton & Co.

Porges, S. W., Doussard-Roosevelt, J. A., Portales, A. L., & Greenspan, S. I. (1996). Infant regulation of the vagal "brake" predicts child behavioral problems: a psychobiological model of social behavior. Developmental Psychobiology, 29(8), 697-712.http://dx.doi.org/10.1002/(SICI)1098-2302(199612)29:8%3C697::AID-DEV5%3E3.0.CO;2-O

Rees, C. A. (2014). Lost among trees? The autonomic nervous system and paediatrics. Achives of Disease in Childhood, 99(6), 552-562. http://dx.doi.org/10.1136/archdischild-2012-301863

Rogers, S. J., & Ozonoff, S. (2005). Annotation: what do we know about sensory dysfunction in autism? A critical review of the empirical evidence. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 46(12), 1255-1268. http://dx.doi.org/10.1111/j.1469-7610.2005.01431.x

Rubenstein, J. L., & Merzenich, M. M. (2003). Model of autism: increased ratio of excitation/inhibition in key neural systems. Genes, Brain, and Behavior, 2(5), 255-267. http://dx.doi.org/10.1034/j.1601-183X.2003.00037.x

Seminowicz, D. A., Mayberg, H. S., McIntosh, A. R., Goldapple, K., Kennedy, S., Segal, Z., & Rafi-Tari, S. (2004). Limbic-frontal circuitry in major depression: a path modeling meta-analysis. NeuroImage, 22(1), 409-418.

http://dx.doi.org/10.1016/j.neuroimage.2004.01.015

Schoen, S. A., Miller, L. J., Brett-Green, B. A., & Nielsen, D. M. (2009). Physiological and behavioral differences in sensory processing: a comparison of children with autism spectrum disorder and sensory modulation disorder. Frontiers in Integrative Neuroscience, 3. http://dx.doi.org/10.3389/neuro.07.029.2009

Smeekens, I., Didden, R., & Verhoeven, E. W. (2015). Exploring the relationship of autonomic and endocrine activity with social functioning in adults with autism spectrum disorders. Journal of Autism and Developmental Disorders, 45(2), 495-505. http://dx.doi.org/10.1007/s10803-013-1947-z

Sohn, J. H., Sokhadze, E., & Watanuki, S. (2001). Electrodermal and cardiovascular manifestations of emotions in children. Journal of Physiological Anthropology and Applied Human Science, 20(2), 55-64. http://dx.doi.org/10.2114/jpa.20.55

Sokhadze, E. M., El-Baz, A., Baruth, J., Mathai, G., Sears, L., & Casanova, M. F. (2009a). Effects of low-frequency repetitive transcranial magnetic stimulation (rTMS) on induced gamma frequency oscillations and event-related potentials during processing of illusory figures in autism. Journal of Autism and Developmental Disorders, 39(4), 619-634. http://dx.doi.org/10.1007/s10803-008-0662-7

Sokhadze, E., Baruth, J., Tasman, A., Sears, L., Mathai, G., El-Baz, A., & Casanova, M. F. (2009b). Event-related potential study of novelty processing abnormalities in autism. Applied Psychophysiology and Biofeedback, 34(1), 37-51. http://dx.doi.org/10.1007/s10484-009-9074-5

Sokhadze, G., Kaplan, M., Edelson, S. M., … Casanova, M. F. (2012). Effects of ambient prism lenses on autonomic reactivity to emotional stimuli in autism. Applied Psychophysiology and Biofeedback, 37, 303.

Sokhadze, E. M., Casanova, M. F., El-Baez, A. S., Farag, H. E., Li, X., & Wang, Y. (2016). TMS-based neuromodulation of evoked and induced gamma oscillations and event-related potentials in children with autism. NeuroRegulation, 3(3), 101-126. http://dx.doi.org/10.15540/nr.3.3.101

Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61(3), 201-216. http://dx.doi.org/10.1016/S0165-0327(00)00338-4

Thayer, J. F., Hansen, A. L., Saus-Rose, E., & Johnsen, B. H. (2009). Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Annals of Behavioral Medicine, 37(2), 141-153 http://dx.doi.org/10.1007/s12160-009-9101-z

Thayer, J. F., & Friedman, B. H. (2002). Stop that! Inhibition, sensitization, and their neurovisceral concomitants. Scandinavian Journal of Psychology, 43(2), 123-130. http://dx.doi.org/10.1111/1467-9450.00277

Thayer, J. F., Ahs, F., Fredrikson, M., Sollers, J. J. , & Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neuroscience and Biobehavioral Reviews, 36(2), 747-756. http://dx.doi.org/10.1016/j.neubiorev.2011.11.009

Toichi, M., Kubota, Y., Murai, T., Kamio, Y., Sakihama, M., Toriuchi, T., … Miyoshi, K. (1999). The influence of psychotic states on the autonomic nervous system in schizophrenia. International Journal of Psychophysiology, 31(2), 147-154.

http://dx.doi.org/10.1016/S0167-8760(98)00047-6

Toichi, M., & Kamio, Y. (2003). Paradoxical autonomic response to mental tasks in autism. Journal of Autism and Developmental Disorders, 33(4), 417-426. http://dx.doi.org/10.1023/A:1025062812374

Udupa, K., Sathyaprabha, T. N., Thirthalli, J., Kishore, K. R., Raju, T. R., & Gangadhar, B. N. (2007). Modulation of cardiac autonomic functions in patients with major depression treated with repetitive transcranial magnetic stimulation. Journal of Affect Disorders, 104(1-3), 231-236. http://dx.doi.org/10.1016/j.jad.2007.04.002

van Engeland, H. (1984). The electrodermal orienting response to auditive stimuli in autistic children, normal children, mentally retarded children, and child psychiatric patients. Journal of Autism and Developmental Disorders, 14(3), 261-279. http://dx.doi.org/10.1007/BF02409578

Wagner, T., Rushmore, J., Eden, U., & Valero-Cabre, A. (2009). Biophysical foundations underlying TMS: setting the stage for an effective use of neurostimulation in the cognitive neurosciences. Cortex, 45(9), 1025-1034. http://dx.doi.org/10.1016/j.cortex.2008.10.002

Wang, Y., Hensley, M. K., Tasman, A., Sears, L., Casanova, M. F., & Sokhadze, E. M. (2016). Heart rate variability and skin conductance during repetitive TMS course in children with autism. Applied Psychophysiology and Biofeedback, 41(1), 47-60.

http://dx.doi.org/10.1007/s10484-015-9311-z

Williams, L. M., Brown, K. J., Das, P., Boucsein, W., Sokolov, E. N., Brammer, M. J., … Gordon, E. (2004). The dynamics of cortico-amygdala and autonomic activity over the experimental time course of fear perception. Brain Research. Cognitive Brain Research, 21(1), 114-123. http://dx.doi.org/10.1016/j.cogbrainres.2004.06.005

Yoshida, T., Yoshino, A., Kobayashi, Y., Inoue, M., Kamakura, K., & Nomura, S. (2001). Effects of slow repetitive transcranial magnetic stimulation on heart rate variability according to power spectrum analysis. Journal of the Neurological Sciences, 184(1), 77-80. http://dx.doi.org/10.1016/S0022-510X(00)00505-0

Zahn, T. P., Rumsey, J. M., & Van Kammen, D. P. (1987). Autonomic nervous system activity in autistic, schizophrenic, and normal men: effects of stimulus significance. Journal of Abnormal Psychology, 96(2), 135-144.

http://dx.doi.org/10.1037/0021-843X.96.2.135

Downloads

Published

2017-06-30

Issue

Section

Research Papers