Abstract
Objectives
Mindfulness-based therapies can reduce depression and anxiety in adults with autism spectrum disorder (ASD). However, the underlying neurophysiological mechanisms have yet to be fully characterized. While mindfulness-related improvements are theorized to be derived from alterations to resting-state networks—especially within the default mode network (DMN)—in other clinical populations, it is unclear if changes in DMN neurophysiology relate to symptom reduction in autistic adults.
Method
In this randomized controlled trial, 96 adults with ASD were assigned to either a Mindfulness-Based Stress Reduction (MBSR) or a social support and relaxation education (SE) active control group. Resting-state electroencephalography recordings and self-report questionnaires assessing depression (BDI-2) and trait anxiety (STAI-2) were collected before and after the 8-week intervention to examine neurophysiological correlates of DMN activity—namely, gamma and high beta (beta-2) power across midline electrodes.
Results
Spectral power analysis of neurophysiological signatures of DMN activity from 62 participants (MBSR n=29; SE n=33) identified distinct MBSR-induced reductions in frontal and parietal gamma power and frontal beta-2 power relative to the SE group. Both MBSR and SE groups showed reductions in central beta-2 and gamma-band power, suggestive of an overlapping mechanism. MBSR-specific decreases in parietal gamma power were associated with alleviation of anxiety symptoms.
Conclusions
Findings suggest distinct neurophysiological correlates of mindfulness training implicating the DMN and point to a potential anxiolytic mechanism in adults with ASD.
Preregistration
NCT04017793
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Data Availability
Data can be shared upon reasonable request
References
American Psychiatric Association. (2022). Diagnostic and statistical manual of mental disorders, (5th ed., text rev.). https://doi.org/10.1176/appi.books.9780890425787
Andreescu, C., Sheu, L. K., Tudorascu, D., Walker, S., & Aizenstein, H. (2014). The ages of anxiety - Differences across the lifespan in the default mode network functional connectivity in generalized anxiety disorder. International Journal of Geriatric Psychiatry, 29(7), 704–712. https://doi.org/10.1002/gps.4051
Baio, J. (2012). Prevalence of autism spectrum disorders - Autism and developmental disabilities monitoring network, 14 Sites, United States, 2008. Morbidity and Mortality Weekly Report, 61(SS-3), 1–19.
Beck, K. B., Greco, C. M., Terhorst, L. A., Skidmore, E. R., Kulzer, J. L., & McCue, M. P. (2020). Mindfulness-Based Stress Reduction for adults with autism spectrum disorder: Feasibility and estimated effects. Mindfulness, 11(5), 1286–1297. https://doi.org/10.1007/s12671-020-01345-2
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57(1), 289–300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Berkovich-Ohana, A. (2017). A case study of a meditation-induced altered state: Increased overall gamma synchronization. Phenomenology and the Cognitive Sciences, 16(1), 91–106. https://doi.org/10.1007/s11097-015-9435-x
Berkovich-Ohana, A., Glicksohn, J., & Goldstein, A. (2012). Mindfulness-induced changes in gamma band activity - Implications for the default mode network, self-reference and attention. Clinical Neurophysiology, 123(4), 700–710. https://doi.org/10.1016/j.clinph.2011.07.048
Berkovich-ohana, A., Glicksohn, J., Goldstein, A., & Israel, R. G. (2014). Studying the default mode and its mindfulness-induced changes using EEG functional connectivity. Social Cognitive and Affective Neuroscience, 9(10), 1616–1624. https://doi.org/10.1093/scan/nst153
Braboszcz, C., Rael Cahn, B., Levy, J., Fernandez, M., & Delorme, A. (2017). Increased gamma brainwave amplitude compared to control in three different meditation traditions. PLoS ONE, 12(1)
Braden, B. B., Pagni, B. A., Monahan, L., Walsh, M. J. M., Dixon, M. V., Delaney, S., Ballard, L., & Ware, J. E. (2021). Quality of life in adults with autism spectrum disorder: Influence of age, sex, and a controlled, randomized mindfulness-based stress reduction pilot intervention. Quality of Life Research, 31, 1427–1440. https://doi.org/10.1007/s11136-021-03013-x
Cahn, B. R., Delorme, A., & Polich, J. (2010). Occipital gamma activation during Vipassana meditation. Cognitive Processing, 11(1), 39–56. https://doi.org/10.1007/s10339-009-0352-1
Chiesa, A., Anselmi, R., & Serretti, A. (2014). Psychological mechanisms of mindfulness-based interventions: What do we know? Holistic Nursing Practice, 28(2), 124–148. https://doi.org/10.1097/HNP.0000000000000017
Coleman, D. M., Adams, J. B., Anderson, A. L., & Frye, R. E. (2019). Rating of the effectiveness of 26 psychiatric and seizure medications for autism spectrum disorder: Results of a national survey. Journal of Child and Adolescent Psychopharmacology, 29(2), 107–123. https://doi.org/10.1089/cap.2018.0121
Das, A., de los Angeles, C., & Menon, V. (2022). Electrophysiological foundations of the human default-mode network revealed by intracranial-EEG recordings during resting-state and cognition. NeuroImage, 250, 118927. https://doi.org/10.1016/j.neuroimage.2022.118927
Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods, 134(1), 9–21. https://doi.org/10.1016/j.jneumeth.2003.10.009
Dietz, P. M., Rose, C. E., McArthur, D., & Maenner, M. (2020). National and state estimates of adults with autism spectrum disorder. Journal of Autism and Developmental Disorders, 50(12), 4258–4266. https://doi.org/10.1007/s10803-020-04494-4
Dor-Ziderman, Y., Ataria, Y., Fulder, S., Goldstein, A., & Berkovich-Ohana, A. (2016). Self-specific processing in the meditating brain: A MEG neurophenomenology study. Neuroscience of Consciousness, 2016(1), niw019. https://doi.org/10.1093/nc/niw019
Dor-Ziderman, Y., Berkovich-Ohana, A., Glicksohn, J., & Goldstein, A. (2013). Mindfulness-induced selflessness: A MEG neurophenomenological study. Frontiers in Human Neuroscience, 7, 1–17. https://doi.org/10.3389/fnhum.2013.00582
Engel, A. K., & Fries, P. (2010). Beta-band oscillations—Signalling the status quo? Current Opinion in Neurobiology, 20(2), 156–165. https://doi.org/10.1016/j.conb.2010.02.015
Faria, V., Gingnell, M., Hoppe, J. M., Hjorth, O., Alaie, I., Frick, A., Hultberg, S., Wahlstedt, K., Engman, J., Månsson, K. N. T., Carlbring, P., Andersson, G., Reis, M., Larsson, E. M., Fredrikson, M., & Furmark, T. (2017). Do you believe tt? Verbal suggestions influence the clinical and neural effects of escitalopram in social anxiety disorder: A randomized trial. EBioMedicine, 24, 179–188. https://doi.org/10.1016/j.ebiom.2017.09.031
Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175–191. https://doi.org/10.3758/bf03193146
Ferree, T. C., Luu, P., Russell, G. S., & Tucker, D. M. (2001). Scalp electrode impedance, infection risk, and EEG data quality. Clinical Neurophysiology, 112(3), 536–544. https://doi.org/10.1016/s1388-2457(00)00533-2
Garrison, K. A., Santoyo, J. F., Davis, J. H., Thornhill, T. A., IV, Kerr, C. E., & Brewer, J. A. (2013). Effortless awareness: Using real time neurofeedback to investigate correlates of posterior cingulate cortex activity in meditators’ self-report. Frontiers in Human Neuroscience, 7, 1–9. https://doi.org/10.3389/fnhum.2013.00440
Goldin, P., Ziv, M., Jazaieri, H., & Gross, J. J. (2012). Randomized controlled trial of mindfulness-based stress reduction versus aerobic exercise: Effects on the self-referential brain network in social anxiety disorder. Frontiers in Human Neuroscience, 6, 1–16. https://doi.org/10.3389/fnhum.2012.00295
Goldstein, M. R., Turner, A. D., Dawson, S. C., Segal, Z. V., Shapiro, S. L., Wyatt, J. K., Manber, R., Sholtes, D., & Ong, J. C. (2019). Increased high-frequency NREM EEG power associated with mindfulness-based interventions for chronic insomnia: Preliminary findings from spectral analysis. Journal of Psychosomatic Research, 120, 12–19. https://doi.org/10.1016/j.jpsychores.2019.02.012
Gruber, T., & Müller, M. M. (2002). Effects of picture repetition on induced gamma band responses, evoked potentials, and phase synchrony in the human EEG. Cognitive Brain Research, 13(3), 377–392. https://doi.org/10.1016/S0926-6410(01)00130-6
Hedley, D., Uljarević, M., Wilmot, M., Richdale, A., & Dissanayake, C. (2017). Brief report: Social support, depression and suicidal ideation in adults with autism spectrum disorder. Journal of Autism and Developmental Disorders, 47(11), 3669–3677. https://doi.org/10.1007/s10803-017-3274-2
Hlinka, J., Alexakis, C., Diukova, A., Liddle, P. F., & Auer, D. P. (2010). Slow EEG pattern predicts reduced intrinsic functional connectivity in the default mode network: An inter-subject analysis. NeuroImage, 53(1), 239–246. https://doi.org/10.1016/j.neuroimage.2010.06.002
Hölzel, B. K., Lazar, S. W., Gard, T., Schuman-Olivier, Z., Vago, D. R., & Ott, U. (2011). How does mindfulness meditation work? Proposing mechanisms of action from a conceptual and neural perspective. Perspectives on Psychological Science, 6(6), 537–559. https://doi.org/10.1177/1745691611419671
Howlin, P. (2000). Outcome in adult life for more able individuals with autism or Asperger syndrome. Autism, 4(1), 63–83. https://doi.org/10.1177/1362361300004001005
Imperatori, C., Farina, B., Adenzato, M., Valenti, E. M., Murgia, C., Marca, G. D., Brunetti, R., Fontana, E., & Ardito, R. B. (2019). Default mode network alterations in individuals with high-trait-anxiety: An EEG functional connectivity study. Journal of Affective Disorders, 246, 611–618. https://doi.org/10.1016/j.jad.2018.12.071
Jerbi, K., Vidal, J. R., Ossandon, T., Dalal, S. S., Jung, J., Hoffmann, D., Minotti, L., Bertrand, O., Kahane, P., & Lachaux, J. P. (2010). Exploring the electrophysiological correlates of the default-mode network with intracerebral EEG. Frontiers in Systems Neuroscience, 4, 1–9. https://doi.org/10.3389/fnsys.2010.00027
Jin, M. J., Kim, J. S., Kim, S., Hyun, M. H., & Lee, S. H. (2018). An integrated model of emotional problems, beta power of electroencephalography, and low frequency of heart rate variability after childhood trauma in a non-clinical sample: A path analysis study. Frontiers in Psychiatry, 8, 314. https://doi.org/10.3389/fpsyt.2017.00314
Jokiranta-Olkoniemi, E., Gyllenberg, D., Sucksdorff, D., Suominen, A., Kronström, K., Chudal, R., & Sourander, A. (2021). Risk for premature mortality and intentional self-harm in autism spectrum disorders. Journal of Autism and Developmental Disorders, 51(9), 3098–3108. https://doi.org/10.1007/s10803-020-04768-x
Kabat-Zinn, J. (2003). Mindfulness-based interventions in context: Past, present, and future. Clinical Psychology: Science and Practice, 10(2), 144–156. https://doi.org/10.1093/clipsy/bpg016
Kaufman, A. S. (2004). Kaufman brief intelligence test–second edition (KBIT-2). American Guidance Service.
Kaunhoven, R. J., & Dorjee, D. (2021). Mindfulness versus cognitive reappraisal: The impact of mindfulness-based stress reduction (MBSR) on the early and late brain potential markers of emotion regulation. Mindfulness, 12(9), 2266–2280. https://doi.org/10.1007/s12671-021-01692-8
Kilpatrick, L. A., Suyenobu, B. Y., Smith, S. R., Bueller, J. A., Goodman, T., Creswell, J. D., Tillisch, K., Mayer, E. A., & Naliboff, B. D. (2011). Impact of mindfulness-based stress reduction training on intrinsic brain connectivity. NeuroImage, 56(1), 290–298. https://doi.org/10.1016/j.neuroimage.2011.02.034
Kok, B. E., & Singer, T. (2017). Phenomenological fingerprints of four meditations: Differential state changes in affect, mind-wandering, meta-cognition, and interoception before and after daily practice across 9 months of training. Mindfulness, 8(1), 218–231. https://doi.org/10.1007/s12671-016-0594-9
Kral, T. R. A., Imhoff-Smith, T., Dean, D. C., Grupe, D., Adluru, N., Patsenko, E., Mumford, J. A., Goldman, R., Rosenkranz, M. A., & Davidson, R. J. (2019). Mindfulness-based stress reduction-related changes in posterior cingulate resting brain connectivity. Social Cognitive and Affective Neuroscience, 14(7), 777–787. https://doi.org/10.1093/scan/nsz050
Kropotov, J. D. (2009). Chapter 3 - Beta Rhythms. In J. D. Kropotov (Ed.), Quantitative EEG, Event-Related Potentials and Neurotherapy (pp. 59–76). Academic Press. https://doi.org/10.1016/B978-0-12-374512-5.00003-7
Laufs, H., Holt, J. L., Elfont, R., Krams, M., Paul, J. S., Krakow, K., & Kleinschmidt, A. (2006). Where the BOLD signal goes when alpha EEG leaves. NeuroImage, 31(4), 1408–1418. https://doi.org/10.1016/j.neuroimage.2006.02.002
Lemogne, C., Delaveau, P., Freton, M., Guionnet, S., & Fossati, P. (2012). Medial prefrontal cortex and the self in major depression. Journal of Affective Disorders, 136(1–2), e1–e11. https://doi.org/10.1016/j.jad.2010.11.034
Lin, Y., Callahan, C. P., & Moser, J. S. (2018). A mind full of self: Self-referential processing as a mechanism underlying the therapeutic effects of mindfulness training on internalizing disorders. Neuroscience and Biobehavioral Reviews, 92, 172–186. https://doi.org/10.1016/j.neubiorev.2018.06.007
Lord, C., Rutter, M., DiLavore, P., Risi, S., Gotham, K., & Bishop, S. (2012). Autism diagnostic observation schedule–2nd edition (ADOS-2). Western Psychological Corporation.
Moss, P., Mandy, W., & Howlin, P. (2017). Child and adult factors related to quality of life in adults with autism. Journal of Autism and Developmental Disorders, 47(6), 1830–1837. https://doi.org/10.1007/s10803-017-3105-5
Nejad, A. B., Fossati, P., & Lemogne, C. (2013). Self-referential processing, rumination, and cortical midline structures in major depression. Frontiers in Human Neuroscience, 7, 666. https://doi.org/10.3389/fnhum.2013.00666
Neuner, I., Arrubla, J., Werner, C. J., Hitz, K., Boers, F., Kawohl, W., & Shah, N. J. (2014). The default mode network and EEG regional spectral power: A simultaneous fMRI-EEG study. PLoS ONE, 9(2), e88214. https://doi.org/10.1371/journal.pone.0088214
Ng, H. Y. H., Wu, C. W., Huang, F. Y., Cheng, Y. T., Guu, S. F., Huang, C. M., Hsu, C. F., Chao, Y. P., Jung, T. P., & Chuang, C. H. (2021). Mindfulness training associated with resting-state electroencephalograms dynamics in novice practitioners via mindful breathing and body-scan. Frontiers in Psychology, 12, 4939. https://doi.org/10.3389/fpsyg.2021.748584
Northoff, G., & Bermpohl, F. (2004). Cortical midline structures and the self. Trends in Cognitive Sciences, 8(3), 102–107. https://doi.org/10.1016/j.tics.2004.01.004
Northoff, G., Heinzel, A., de Greck, M., Bermpohl, F., Dobrowolny, H., & Panksepp, J. (2006). Self-referential processing in our brain-A meta-analysis of imaging studies on the self. NeuroImage, 31(1), 440–457. https://doi.org/10.1016/j.neuroimage.2005.12.002
O’Neill, J., Piacentini, J., Chang, S., Ly, R., Lai, T. M., Armstrong, C. C., Bergman, L., Rozenman, M., Peris, T., Vreeland, A., Mudgway, R., Levitt, J. G., Salamon, N., Posse, S., Hellemann, G. S., Alger, J. R., McCracken, J. T., & Nurmi, E. L. (2017). Glutamate in pediatric obsessive-compulsive disorder and response to cognitive-behavioral therapy: Randomized clinical trial. Neuropsychopharmacology, 42(12), 2414–2422. https://doi.org/10.1038/npp.2017.77
Ossandón, T., Jerbi, K., Vidal, J. R., Bayle, D. J., Henaff, M. A., Jung, J., Minotti, L., Bertrand, O., Kahane, P., & Lachaux, J. P. (2011). Transient suppression of broadband gamma power in the default-mode network is correlated with task complexity and subject performance. Journal of Neuroscience, 31(41), 14521–14530. https://doi.org/10.1523/JNEUROSCI.2483-11.2011
Pagni, B. A., & Braden, B. B. (2021). Early reflections on the therapeutic effects of mindfulness-based therapies in adults with autism and suggestions for future research. Journal of Psychiatry and Brain Science, 6, e210013. https://doi.org/10.20900/jpbs20210013
Pagni, B. A., Hill, E., Walsh, M. J. M., Delaney, S., Guerithault, N., Dixon, M. V., Ballard, L., & Braden, B. B. (2023). Distinct and shared therapeutic neural mechanisms of mindfulness-based and social support stress reduction groups in adults with autism spectrum disorder. Journal of Psychiatry & Neuroscience, 48(2), E102–E114. https://doi.org/10.1503/jpn.220159
Pagni, B. A., Walsh, M. J. M., Foldes, E., Sebren, A., Dixon, M. V., Guerithault, N., & Braden, B. B. (2020). The neural correlates of mindfulness-induced depression reduction in adults with autism spectrum disorder: A pilot study. Journal of Neuroscience Research, 98(6), 1150–1161. https://doi.org/10.1002/jnr.24600
Pavlenko, V. B., Chernyi, S. V., & Goubkina, D. G. (2009). Eeg correlates of anxiety and emotional stability in adult healthy subjects. Neurophysiology, 41(5), 337–345. https://doi.org/10.1007/s11062-010-9111-2
Plechawska-Wojcik, M., Kaczorowska, M., & Zapala, D. (2019). The artifact subspace reconstruction (ASR) for EEG signal correction. A comparative study. In Information Systems Architecture and Technology: Proceedings of 39th International Conference on Information Systems Architecture and Technology – ISAT 2018 (pp. 125–135). Springer
Reynolds, C. R., & Kamphaus, R. W. (2013). Autism Spectrum Disorder 299.00 (F84.0). 00, 0–2.
Sheynin, J., Duval, E. R., King, A. P., Angstadt, M., Phan, K. L., Simon, N. M., Rauch, S. A. M., & Liberzon, I. (2020). Associations between resting-state functional connectivity and treatment response in a randomized clinical trial for posttraumatic stress disorder. Depression and Anxiety, 37(10), 1037–1046. https://doi.org/10.1002/da.23075
Sizoo, B. B., & Kuiper, E. (2017). Cognitive behavioural therapy and mindfulness based stress reduction may be equally effective in reducing anxiety and depression in adults with autism spectrum disorders. Research in Developmental Disabilities, 64, 47–55. https://doi.org/10.1016/j.ridd.2017.03.004
Spek, A. A., Van Ham, N. C., & Nyklíček, I. (2013). Research in Developmental Disabilities Mindfulness-based therapy in adults with an autism spectrum disorder: A randomized controlled trial. Research in Developmental Disabilities, 34(1), 246–253. https://doi.org/10.1016/j.ridd.2012.08.009
Takamiya, A., Hirano, J., Yamagata, B., Takei, S., Kishimoto, T., & Mimura, M. (2019). Electroconvulsive therapy modulates resting-state EEG oscillatory pattern and phase synchronization in nodes of the default mode network in patients with depressive disorder. Frontiers in Human Neuroscience, 13, 1–9. https://doi.org/10.3389/fnhum.2019.00001
Wells, R. E., Yeh, G. Y., Kerr, C. E., Wolkin, J., Davis, R. B., Tan, Y., Spaeth, R., Wall, R. B., Walsh, J., Kaptchuk, T. J., Press, D., Phillips, R. S., & Kong, J. (2013). Meditation’s impact on default mode network and hippocampus in mild cognitive impairment: Pilot study. Neuroscience Letters, 556, 15–19. https://doi.org/10.1016/j.neulet.2013.10.001
Williams, D. (2010). Theory of own mind in autism: Evidence of a specific deficit in self-awareness? Autism, 14(5), 474–494. https://doi.org/10.1177/1362361310366314
Acknowledgements
We send gratitude to our participants who made this study possible.
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This work was supported by Arizona State University (Start-up Funding) and the National Center for Complementary and Integrative Health (F31AT01097).
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Broc A. Pagni: conceptualization; data curation; formal analysis; investigation; methodology; project administration; validation; visualization; writing—original draft preparation; writing—review and editing. Cole Williams: formal analysis, methodology, validation, visualization, writing—review and editing. Gabrielle Adams: data curation, software, writing—review and editing. Chris Blais: conceptualization, funding acquisition, methodology, resources, software, supervision, validation, writing—review and editing. Gene Brewer: funding acquisition, investigation, resources, software, supervision, writing—review and editing. B. Blair Braden: conceptualization; formal analysis; funding acquisition; investigation; methodology; project administration; resources; supervision; visualization; writing—original draft; writing—review and editing.
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Pagni, B.A., Williams, C., Abrams, G. et al. Neurophysiological Signatures of Mindfulness-Based Stress Reduction in Adults with Autism: Putative Mechanism of Anxiety Alleviation. Mindfulness 14, 2124–2136 (2023). https://doi.org/10.1007/s12671-023-02195-4
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DOI: https://doi.org/10.1007/s12671-023-02195-4