Reduced resting-state brain activity in the default mode network in children with (central) auditory processing disorders

Agnieszka Pluta, Tomasz Wolak, Natalia Czajka, Monika Lewandowska, Katarzyna Cieśla, Mateusz Rusiniak, Diana Grudzień, Henryk Skarżyński, Agnieszka Pluta, Tomasz Wolak, Natalia Czajka, Monika Lewandowska, Katarzyna Cieśla, Mateusz Rusiniak, Diana Grudzień, Henryk Skarżyński

Abstract

Background: In recent years, there has been a growing interest in Central Auditory Processing Disorder (C)APD. However, the neural correlates of (C)APD are poorly understood. Previous neuroimaging experiments have shown changes in the intrinsic activity of the brain in various cognitive deficits and brain disorders. The present study investigated the spontaneous brain activity in (C)APD subjects with resting-state fMRI (rs-fMRI).

Methods: Thirteen children diagnosed with (C)APD and fifteen age and gender-matched controls participated in a rs-fMRI study during which they were asked to relax keeping their eyes open. Two different techniques of the rs-fMRI data analysis were used: Regional Homogeneity (ReHo) and Independent Component Analysis (ICA), which approach is rare.

Results: Both methods of data analysis showed comparable results in the pattern of DMN activity within groups. Additionally, ReHo analysis revealed increased co-activation of the superior frontal gyrus, the posterior cingulate cortex/the precuneus in controls, compared to the (C)APD group. ICA yielded inconsistent results across groups.

Conclusions: Our ReHo results suggest that (C)APD children seem to present reduced regional homogeneity in brain regions considered a part of the default mode network (DMN). These findings might contribute to a better understanding of neural mechanisms of (C)APD.

Figures

Figure 1
Figure 1
Cortical representations of DMN obtained with the ReHo method in (C)APD and the control subjects and a comparison between normal controls and patients with (C)APD (maps thresholded at p < .005, AlphaSim corrected, no of voxels > 66). The color scale represents T values.
Figure 2
Figure 2
Cortical representations of DMN obtained with the ICA method for different model settings in (C)APD, and the control subjects (maps thresholded at p < .005, AlphaSim corrected, no of voxels > 66). The color scale represents T values.

References

    1. Moore DR, Ferguson MA, Edmondson-Jones AM, Ratib S, Riley A. Nature of auditory processing disorder in children. Pediatrics. 2010;126:e382–e390. doi: 10.1542/peds.2009-2826.
    1. Bamiou D-E, Musiek FE, Luxon LM. Aetiology and clinical presentations of auditory processing disorders—a review. Arch Dis Child. 2001;85:361–365. doi: 10.1136/adc.85.5.361.
    1. Bailey T. Auditory pathways and processes: implications for neuropsychological assessment and diagnosis of children and adolescents. Child Neuropsychol. 2010;16:521–548. doi: 10.1080/09297041003783310.
    1. Kim M-J, Jeon H-A, Lee K-M, Son Y-D, Kim Y-B, Cho Z-H. Neuroimaging features in a case of developmental central auditory processing disorder. J Neurol Sci. 2009;277:176–180. doi: 10.1016/j.jns.2008.10.020.
    1. Bartel-Friedrich S, Broecker Y, Knoergen M, Koesling S. Development of fMRI tests for children with central auditory processing disorders. In Vivo. 2010;24:201–209.
    1. Snyder AZ, Raichle ME. A brief history of the resting state: the Washington University perspective. NeuroImage. 2012;62:902–910. doi: 10.1016/j.neuroimage.2012.01.044.
    1. Assaf M, Jagannathan K, Calhoun VD, Miller L, Stevens MC, Sahl R, O’Boyle JG, Schultz RT, Pearlson GD. Abnormal functional connectivity of default mode sub-networks in autism spectrum disorder patients. NeuroImage. 2010;53:247–256. doi: 10.1016/j.neuroimage.2010.05.067.
    1. Camchong J, MacDonald AW, Bell C, Mueller BA, Lim KO. Altered functional and anatomical connectivity in schizophrenia. Schizophr Bull. 2011;37:640–650. doi: 10.1093/schbul/sbp131.
    1. Buckner RL, Andrews-Hanna JR, Schacter DL. The brain’s default network: anatomy, function, and relevance to disease. Ann N Y Acad Sci. 2008;1124:1–38. doi: 10.1196/annals.1440.011.
    1. Leech R, Kamourieh S, Beckmann CF, Sharp DJ. Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. J Neurosci. 2011;31:3217–3224. doi: 10.1523/JNEUROSCI.5626-10.2011.
    1. Hinds O, Thompson TW, Ghosh S, Yoo JJ, Whitfield-Gabrieli S, Triantafyllou C, Gabrieli JDE. Roles of default-mode network and supplementary motor area in human vigilance performance: evidence from real-time fMRI. J Neurophysiol. 2013;109:1250–1258. doi: 10.1152/jn.00533.2011.
    1. Bonnelle V, Leech R, Kinnunen KM, Ham TE, Beckmann CF, Boissezon XD, Greenwood RJ, Sharp DJ. Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. J Neurosci. 2011;31:13442–13451. doi: 10.1523/JNEUROSCI.1163-11.2011.
    1. Broyd SJ, Demanuele C, Debener S, Helps SK, James CJ, Sonuga-Barke EJS. Default-mode brain dysfunction in mental disorders: a systematic review. Neurosci Biobehav Rev. 2009;33:279–296. doi: 10.1016/j.neubiorev.2008.09.002.
    1. Bell SM, McCallum RS, Cox EA. Toward a research-based assessment of dyslexia: using cognitive measures to identify reading disabilities. J Learn Disabil. 2003;36:505–516. doi: 10.1177/00222194030360060201.
    1. Riccio CA, Cohen MJ, Garrison T, Smith B. Auditory processing measures: correlation with neuropsychological measures of attention, memory, and behavior. Child Neuropsychol. 2005;11:363–372. doi: 10.1080/09297040490916956.
    1. Chermak GD, Somers EK, Seikel JA. Behavioral signs of central auditory processing disorder and attention deficit hyperactivity disorder. J Am Acad Audiol. 1998;9:78–84.
    1. Hoeksma MR, Kenemans JL, Kemner C, van Engeland H. Variability in spatial normalization of pediatric and adult brain images. Clin Neurophysiol. 2005;116:1188–1194. doi: 10.1016/j.clinph.2004.12.021.
    1. Castellanos FX, Margulies DS, Kelly AMC, Uddin LQ, Ghaffari M, Kirsch A, Shaw D, Shehzad Z, Di Martino A, Biswal B, Sonuga-Barke EJS, Rotrosen J, Adler LA, Milham MP. Cingulate - precuneus interactions: a new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biol Psychiatry. 2008;63:332–337. doi: 10.1016/j.biopsych.2007.06.025.
    1. Cao Q, Zang Y, Sun L, Sui M, Long X, Zou Q, Wang Y. Abnormal neural activity in children with attention deficit hyperactivity disorder: a resting-state functional magnetic resonance imaging study. Neuroreport. 2006;17:1033–1036. doi: 10.1097/01.wnr.0000224769.92454.5d.
    1. Weissman DH, Roberts KC, Visscher KM, Woldorff MG. The neural bases of momentary lapses in attention. Nat Neurosci. 2006;9:971–978. doi: 10.1038/nn1727.
    1. Sonuga-Barke EJS, Castellanos FX. Spontaneous attentional fluctuations in impaired states and pathological conditions: a neurobiological hypothesis. Neurosci Biobehav Rev. 2007;31:977–986. doi: 10.1016/j.neubiorev.2007.02.005.
    1. Calhoun VD, Adali T, Pearlson GD, Pekar JJ. A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp. 2001;14:140–151. doi: 10.1002/hbm.1048.
    1. Ding X, Lee S-W. Cocaine addiction related reproducible brain regions of abnormal default-mode network functional connectivity: a group ICA study with different model orders. Neurosci Lett. 2013;548:110–114.
    1. Allen EA, Damaraju E, Plis SM, Erhardt EB, Eichele T, Calhoun VD. Tracking whole-brain connectivity dynamics in the resting state. Cereb Cortex. 2014;24:663–676. doi: 10.1093/cercor/bhs352.
    1. Damoiseaux JS, Beckmann CF, Arigita EJ, Barkhof F, Scheltens P, Stam CJ, Smith SM, Rombouts SA. Reduced resting-state brain activity in the “default network” in normal aging. Cereb Cortex. 2008;18:1856–1864. doi: 10.1093/cercor/bhm207.
    1. Raichle ME, Snyder AZ. A default mode of brain function: a brief history of an evolving idea. NeuroImage. 2007;37:1083–1090. doi: 10.1016/j.neuroimage.2007.02.041.
    1. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, Kochunov PV, Nickerson D, Mikiten SA, Fox PT. Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp. 2000;10:120–131. doi: 10.1002/1097-0193(200007)10:3<120::AID-HBM30>;2-8.
    1. Van Dijk KRA, Sabuncu MR, Buckner RL. The influence of head motion on intrinsic functional connectivity MRI. NeuroImage. 2012;59:431–438. doi: 10.1016/j.neuroimage.2011.07.044.
    1. Power JD, Mitra A, Laumann TO, Snyder AZ, Schlaggar BL, Petersen SE. Methods to detect, characterize, and remove motion artifact in resting state fMRI. NeuroImage. 2014;84:320–341.
    1. Rombouts SARB, Damoiseaux JS, Goekoop R, Barkhof F, Scheltens P, Smith SM, Beckmann CF. Model‒free group analysis shows altered BOLD FMRI networks in dementia. Hum Brain Mapp. 2009;30:256–266. doi: 10.1002/hbm.20505.
    1. Leech R, Braga R, Sharp DJ. Echoes of the brain within the posterior cingulate cortex. J Neurosci Off J Soc Neurosci. 2012;32:215–222. doi: 10.1523/JNEUROSCI.3689-11.2012.
    1. Pearson JM, Heilbronner SR, Barack DL, Hayden BY, Platt ML. Posterior cingulate cortex: adapting behavior to a changing world. Trends Cogn Sci. 2011;15:143–151. doi: 10.1016/j.tics.2011.02.002.
    1. Uddin LQ, Kelly AMC, Biswal BB, Margulies DS, Shehzad Z, Shaw D, Ghaffari M, Rotrosen J, Adler LA, Castellanos FX, Milham MP. Network homogeneity reveals decreased integrity of default-mode network in ADHD. J Neurosci Methods. 2008;169:249–254. doi: 10.1016/j.jneumeth.2007.11.031.
    1. Cacace AT, McFarland DJ. The importance of modality specificity in diagnosing central auditory processing disorder. Am J Audiol. 2005;14:112–123. doi: 10.1044/1059-0889(2005/012).
    1. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE. Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. Neuroimage. 2012;59:2142–2154. doi: 10.1016/j.neuroimage.2011.10.018.
    1. De Celis Alonso B, Hidalgo Tobón S, Dies Suarez P, García Flores J, De Celis Carrillo B, Barragán Pérez E. A multi-methodological MR resting state network analysis to assess the changes in brain physiology of children with ADHD. PLoS One. 2014;9:e99119. doi: 10.1371/journal.pone.0099119.
    1. Cole DM, Smith SM, Beckmann CF. Advances and pitfalls in the analysis and interpretation of resting-state FMRI data. Front Syst Neurosci. 2010;4:8.
    1. Beckmann CF, Smith SM. Tensorial extensions of independent component analysis for multisubject FMRI analysis. NeuroImage. 2005;25:294–311. doi: 10.1016/j.neuroimage.2004.10.043.
    1. Liu C-H, Ma X, Li F, Wang Y-J, Tie C-L, Li S-F, Chen T-L, Fan T, Zhang Y, Dong J, Yao L, Wu X, Wang C-Y. Regional homogeneity within the default mode network in bipolar depression: a resting-state functional magnetic resonance imaging study. PLoS One. 2012;7:e48181. doi: 10.1371/journal.pone.0048181.
    1. Von dem Hagen EAH, Stoyanova RS, Baron-Cohen S, Calder AJ. Reduced functional connectivity within and between “social” resting state networks in autism spectrum conditions. Soc Cogn Affect Neurosci. 2013;8(6):694–701. doi: 10.1093/scan/nss053.
    1. Valsasina P, Rocca M, Misci P, Pagani E, Falini A, Filippi M. Proceedings of The International Society for Magnetic Resonance in Medicine. Honolulu, Hawai’i, USA; 2009.

Source: PubMed

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