Functional Brain Network Changes Following Use of an Allostatic, Closed-Loop, Acoustic Stimulation Neurotechnology for Military-Related Traumatic Stress

Sung W Lee, Paul J Laurienti, Jonathan H Burdette, Catherine L Tegeler, Ashley R Morgan, Sean L Simpson, Lee Gerdes, Charles H Tegeler, Sung W Lee, Paul J Laurienti, Jonathan H Burdette, Catherine L Tegeler, Ashley R Morgan, Sean L Simpson, Lee Gerdes, Charles H Tegeler

Abstract

Background and purpose: Post-traumatic stress disorder is associated with connectivity changes in the default mode, central executive, and salience networks, and other brain regions. This study evaluated changes in network connectivity associated with usage of High-resolution, relational, resonance-based electroencephalic mirroring (HIRREM® ; Brain State Technologies, Scottsdale, AZ), a closed-loop, allostatic, acoustic stimulation neurotechnology, for military-related traumatic stress.

Methods: Eighteen participants (17 males, mean age 41 years [SD = 7], 15 active duty) enrolled in an IRB approved pilot trial for symptoms of military-related traumatic stress. Participants received 19.5 (1.1) HIRREM sessions over 12 days. Symptoms, physiological and functional measures, and whole brain resting MRI were collected before and after HIRREM. Six whole brain functional networks were evaluated using summary variables and community structure of predefined networks. Pre to postintervention change was analyzed using paired-sample statistical tests.

Results: Postintervention, there was an overall increase in connectivity of the default mode network (P = .0094). There were decreases of community structure in both the anterior portion of the default mode (medial prefrontal cortex, P = .0097) and in the sensorimotor (P = .005) network. There were no statistically significant changes at the whole brain level, or in the central executive, salience, or other networks analyzed. Participants demonstrated significant improvements in clinical symptoms, as well as autonomic cardiovascular regulation, which have been reported previously.

Conclusions: Use of closed-loop, allostatic, acoustic stimulation neurotechnology (HIRREM) was associated with connectivity changes in the default mode and sensorimotor networks, in directions that may have explained the subjects' clinical improvements.

Keywords: HIRREM; default mode network; fMRI; post-traumatic stress; sensorimotor network.

© 2018 The Authors. Journal of Neuroimaging published by Wiley Periodicals, Inc. on behalf of American Society of Neuroimaging.

Figures

Figure 1
Figure 1
Maps showing location and extent of the ROIs used in this study. Montreal Neurological Institute (MNI) coordinates are listed below each slice.
Figure 2
Figure 2
Effect of threshold on network metrics of whole‐brain analyses including global efficiency, local efficiency, and modularity.
Figure 3
Figure 3
Maps showing spatial location of the top network hubs for (A) degree, (B) global efficiency, and (C) local efficiency pre‐ and post‐HIRREM. P values for the paired comparison between pre and postintervention are presented for each network metric. The calibration bar applies to all images.
Figure 4
Figure 4
Maps showing consistency of community structure across the group for each of the functional brain regions/subnetworks pre‐ and post‐HIRREM intervention. P values for the paired comparison between pre and postintervention are presented for each subnetwork. The images were scaled to visually depict the spatial variance in the community consistency. Thus, the minimum and maximum consistencies are different across subnetworks. The scaling values (min, max) for each subnetwork are: attention (.01, .13), basal ganglia (.01, .1), default‐mode (.01, .18), sensorimotor (.01, .33), salience (.01, .07), and visual (.01, .25).

References

    1. Menon V. Large‐scale brain networks and psychopathology: a unifying triple network model. Trends Cogn Sci 2011;15:483‐506.
    1. Lanius RA, Frewen PA, Tursich M, et al. Restoring large‐scale brain networks in PTSD and related disorders: a proposal for neuroscientifically‐informed treatment interventions. Eur J Psychotraumatol 2015;6:27313.
    1. Koch SB, van Zuiden M, Nawijn L, et al. Aberrant resting‐state brain activity in posttraumatic stress disorder: a meta‐analysis and systematic review. Depress Anxiety 2016;33:592‐605.
    1. Akiki TJ, Averill CL, Abdallah CG. A network‐based neurobiological model of PTSD: evidence from structural and functional neuroimaging studies. Curr Psychiatry Rep 2017;19:81.
    1. American Psychiatric Association . Diagnostic and Statistical Manual of Mental Disorders: DSM‐5. 5th ed. Arlington, VA: American Psychiatric Association; 2013.
    1. Kennis M, van Rooij SJ, van den Heuvel MP, et al. Functional network topology associated with posttraumatic stress disorder in veterans. Neuroimage Clin 2016;10:302‐9.
    1. Kennis M, Rademaker AR, van Rooij SJ, et al. Resting state functional connectivity of the anterior cingulate cortex in veterans with and without post‐traumatic stress disorder. Hum Brain Mapp 2015;36:99‐109.
    1. Daniels JK, McFarlane AC, Bluhm RL, et al. Switching between executive and default mode networks in posttraumatic stress disorder: alterations in functional connectivity. J Psychiatry Neurosci 2010;35:258‐66.
    1. Sripada RK, King AP, Welsh RC, et al. Neural dysregulation in posttraumatic stress disorder: evidence for disrupted equilibrium between salience and default mode brain networks. Psychosom Med 2012;74:904‐11.
    1. Tursich M, Ros T, Frewen PA, et al. Distinct intrinsic network connectivity patterns of post‐traumatic stress disorder symptom clusters. Acta Psychiatr Scand 2015;132:29‐38.
    1. Bluhm RL, Williamson PC, Osuch EA, et al. Alterations in default network connectivity in posttraumatic stress disorder related to early‐life trauma. J Psychiatry Neurosci 2009;34:187‐94.
    1. Lanius RA, Bluhm RL, Coupland NJ, et al. Default mode network connectivity as a predictor of post‐traumatic stress disorder symptom severity in acutely traumatized subjects. Acta Psychiatr Scand 2010;121:33‐40.
    1. Cisler JM, Sigel BA, Kramer TL, et al. Modes of large‐scale brain network organization during threat processing and posttraumatic stress disorder symptom reduction during TF‐CBT among adolescent girls. PLoS One 2016;11:e0159620.
    1. Long Z, Duan X, Xie B, et al. Altered brain structural connectivity in post‐traumatic stress disorder: a diffusion tensor imaging tractography study. J Affect Disord 2013;150:798‐806.
    1. King AP, Block SR, Sripada RK, et al. Altered default mode network (DMN) resting state functional connectivity following a mindfulness‐based exposure therapy for posttraumatic stress disorder (PTSD) in combat veterans of Afghanistan and Iraq. Depress Anxiety 2016;33:289‐99.
    1. Tegeler CL, Gerdes L, Shaltout HA, et al. Successful use of closed‐loop allostatic neurotechnology for post‐traumatic stress symptoms in military personnel: self‐reported and autonomic improvements. Mil Med Res 2017;4:38.
    1. Gerdes L, Gerdes P, Lee SW, et al. HIRREM: a noninvasive, allostatic methodology for relaxation and auto‐calibration of neural oscillations. Brain Behav 2013;3:193‐205.
    1. Tegeler CH, Kumar SR, Conklin D, et al. Open label, randomized, crossover pilot trial of high‐resolution, relational, resonance‐based, electroencephalic mirroring to relieve insomnia. Brain Behav 2012;2:814‐24.
    1. Tegeler CH, Cook JF, Tegeler CL, et al. Clinical, hemispheric, and autonomic changes associated with use of closed‐loop, allostatic neurotechnology by a case series of individuals with self‐reported symptoms of post‐traumatic stress. BMC Psychiatry 2017;17:141.
    1. Sterling P. Allostasis: a model of predictive regulation. Physiol Behav 2012;106:5‐15.
    1. Lei D, Li K, Li L, et al. Disrupted functional brain connectome in patients with posttraumatic sress disorder. Radiology 2015;276:818‐27.
    1. Ogawa S, Lee TM, Kay AR, et al. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci USA 1990;87:9868‐72.
    1. Tzourio‐Mazoyer N, Landeau B, Papathanassiou D, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single‐subject brain. Neuroimage 2002;15:273‐89.
    1. Biswal B, Yetkin FZ, Haughton VM, et al. Functional connectivity in the motor cortex of resting human brain using echo‐planar MRI. Magn Reson Med 1995;34:537‐41.
    1. Hayasaka S. Functional connectivity networks with and without global signal correction. Front Hum Neurosci 2013;7:880.
    1. Power JD, Barnes KA, Snyder AZ, et al. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage 2012;59:2142‐54.
    1. Power JD, Mitra A, Laumann TO, et al. Methods to detect, characterize, and remove motion artifact in resting state fMRI. Neuroimage 2014;84:320‐41.
    1. Hayasaka S, Laurienti PJ. Comparison of characteristics between region‐and voxel‐based network analyses in resting‐state fMRI data. Neuroimage 2010;50:499‐508.
    1. Laurienti PJ, Joyce KE, Telesford QK, et al. Universal fractal scaling of self‐organized networks. Physica A 2011;390:3608‐13.
    1. Latora V, Marchiori M. Efficient behavior of small‐world networks. Phys Rev Lett 2001;87:198701.
    1. Newman ME, Girvan M. Finding and evaluating community structure in networks. Phys Rev E Stat Nonlin Soft Matter Phys 2004;69:026113.
    1. Vincent DB, Jean‐Loup G, Renaud L, et al. Fast unfolding of communities in large networks. J Stat Mech 2008;2008:P10008.
    1. Bullmore E, Sporns O. Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 2009;10:186‐98.
    1. Hagmann P, Cammoun L, Gigandet X, et al. Mapping the structural core of human cerebral cortex. PLoS Biol 2008;6:e159.
    1. van den Heuvel MP, Stam CJ, Boersma M, et al. Small‐world and scale‐free organization of voxel‐based resting‐state functional connectivity in the human brain. Neuroimage 2008;43:528‐39.
    1. Steen M, Hayasaka S, Joyce K, et al. Assessing the consistency of community structure in complex networks. Phys Rev E Stat Nonlin Soft Matter Phys 2011;84:016111.
    1. Moussa MN, Steen MR, Laurienti PJ, et al. Consistency of network modules in resting‐state FMRI connectome data. PLoS One 2012;7:e44428.
    1. Shirer WR, Ryali S, Rykhlevskaia E, et al. Decoding subject‐driven cognitive states with whole‐brain connectivity patterns. Cereb Cortex 2012;22:158‐65.
    1. Hugenschmidt CE, Burdette JH, Morgan AR, et al. Graph theory analysis of functional brain networks and mobility disability in older adults. J Gerontol B Psychol Sci Soc Sci 2014;69:1399‐406.
    1. Simpson SL, Lyday RG, Hayasaka S, et al. A permutation testing framework to compare groups of brain networks. Front Comput Neurosci 2013;7:171.
    1. Uddin LQ, Kelly AM, Biswal BB, et al. Functional connectivity of default mode network components: correlation, anticorrelation, and causality. Hum Brain Mapp 2009;30:625‐37.
    1. Wisco BE, Marx BP, Miller MW, et al. Probable posttraumatic stress disorder in the US veteran population according to DSM‐5: results from the National Health and Resilience in Veterans Study. J Clin Psychiatry 2016;77:1503‐10.
    1. Wu CW, Liu PY, Tsai PJ, et al. Variations in connectivity in the sensorimotor and default‐mode networks during the first nocturnal sleep cycle. Brain Connect 2012;2:177‐90.
    1. Zhu Y, Feng Z, Xu J, et al. Increased interhemispheric resting‐state functional connectivity after sleep deprivation: a resting‐state fMRI study. Brain Imaging Behav 2016;10:911‐9.
    1. Sterling P. Principles of allostasis: optimal design, predictive regulation, pathophysiology, and rational therapeutics In: Schulkin J, ed. Allostasis, Homeostasis, and the Costs of Physiological Adaptation. New York, NY: Cambridge University Press; 2004:17‐64.
    1. Fortunato JE, Tegeler CL, Gerdes L, et al. Use of an allostatic neurotechnology by adolescents with postural orthostatic tachycardia syndrome (POTS) is associated with improvements in heart rate variability and changes in temporal lobe electrical activity. Exp Brain Res 2016;234:791‐8.
    1. Tegeler CH, Tegeler CL, Cook JF, et al. A preliminary study of the effectiveness of an allostatic, closed‐loop, acoustic stimulation neurotechnology in the treatment of athletes with persisting post‐concussion symptoms. Sports Med Open 2016;2:39.
    1. Tegeler CH, Tegeler CL, Cook JF, et al. Reduction in menopause‐related symptoms associated with use of a noninvasive neurotechnology for autocalibration of neural oscillations. Menopause 2015;22:650‐5.
    1. Ramchand R, Rudavsky R, Grant S, et al. Prevalence of, risk factors for, and consequences of posttraumatic stress disorder and other mental health problems in military populations deployed to Iraq and Afghanistan. Curr Psychiatry Rep 2015;17:37.

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