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Default mode network abnormalities during state switching in attention deficit hyperactivity disorder

Published online by Cambridge University Press:  12 October 2015

J. Sidlauskaite ,
E. Sonuga-Barke ,
H. Roeyers  and
J. R. Wiersema
J. Sidlauskaite*
Affiliation:
Department of Experimental-Clinical and Health Psychology, Ghent University, Ghent, Belgium
E. Sonuga-Barke
Affiliation:
Department of Experimental-Clinical and Health Psychology, Ghent University, Ghent, Belgium Developmental Brain-Behaviour Unit, Psychology, University of Southampton, Shackleton Building (B44), Highfield Campus, Southampton, UK
H. Roeyers
Affiliation:
Department of Experimental-Clinical and Health Psychology, Ghent University, Ghent, Belgium
J. R. Wiersema
Affiliation:
Department of Experimental-Clinical and Health Psychology, Ghent University, Ghent, Belgium
*
*Address for correspondence: J. Sidlauskaite, Department of Experimental-Clinical and Health Psychology, Ghent University, Henri Dunantlaan 2, Ghent B-9000, Belgium. (Email: Justina.Sidlauskaite@UGent.be)
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Abstract

Background

Individuals with attention deficit hyperactivity disorder (ADHD) display excess levels of default mode network (DMN) activity during goal-directed tasks, which are associated with attentional disturbances and performance decrements. One hypothesis is that this is due to attenuated down-regulation of this network during rest-to-task switching. A second related hypothesis is that it may be associated with right anterior insula (rAI) dysfunction – a region thought to control the actual state-switching process.

Method

These hypotheses were tested in the current fMRI study in which 19 adults with ADHD and 21 typically developing controls undertook a novel state-to-state switching paradigm. Advance cues signalled upcoming switches between rest and task periods and switch-related anticipatory modulation of DMN and rAI was measured. To examine whether rest-to-task switching impairments may be a specific example of a more general state regulation deficit, activity upon task-to-rest cues was also analysed.

Results

Against our hypotheses, we found that the process of down-regulating the DMN when preparing to switch from rest to task was unimpaired in ADHD and that there was no switch-specific deficit in rAI modulation. However, individuals with ADHD showed difficulties up-regulating the DMN when switching from task to rest.

Conclusions

Rest-to-task DMN attenuation seems to be intact in adults with ADHD and thus appears unrelated to excess DMN activity observed during tasks. Instead, individuals with ADHD exhibit attenuated up-regulation of the DMN, hence suggesting disturbed re-initiation of a rest state.

Keywords

Attention deficit hyperactivity disorderdefault mode networkinsulastate switching
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 3 , February 2016 , pp. 519 - 528
Copyright
Copyright © Cambridge University Press 2015 

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References

Aron, AR, Poldrack, RA (2005). The cognitive neuroscience of response inhibition: relevance for genetic research in attention-deficit/hyperactivity disorder. Biological Psychiatry 57, 1285–1292.CrossRefGoogle ScholarPubMed
Bonnelle, V, Leech, R, Kinnunen, KM, Ham, TE, Beckmann, CF, De Boissezon, X, Greenwood, RJ, Sharp, DJ (2011). Default mode network connectivity predicts sustained attention deficits after traumatic brain injury. Journal of Neuroscience 31, 13442–13451.CrossRefGoogle ScholarPubMed
Brass, M, Von Cramon, DY (2002). The role of the Frontal Cortex in task preparation. Cerebral Cortex 12, 908–914.CrossRefGoogle ScholarPubMed
Brunia, CH, van Boxtel, GJ (2001). Wait and see. International Journal of Psychophysiology 43, 59–75.CrossRefGoogle ScholarPubMed
Buckner, RL, Andrews-Hanna, JR, Schacter, DL (2008). The brain's default network: anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences 1124, 1–38.CrossRefGoogle ScholarPubMed
Bush, G, Frazier, JA, Rauch, SL, Seidman, LJ, Whalen, PJ, Jenike, MA, Rosen, BR, Biederman, J (1999). Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the counting stroop. Biological Psychiatry 45, 1542–1552.CrossRefGoogle ScholarPubMed
Clerkin, SM, Schulz, KP, Berwid, OG, Fan, J, Newcorn, JH, Tang, CY, Halperin, JM (2013). Thalamo-cortical activation and connectivity during response preparation in adults with persistent and remitted ADHD. American Journal of Psychiatry 170, 1011–1019.CrossRefGoogle ScholarPubMed
Coghill, DR, Seth, S, Matthews, K (2014). A comprehensive assessment of memory, delay aversion, timing, inhibition, decision making and variability in attention deficit hyperactivity disorder: advancing beyond the three-pathway models. Psychological Medicine 44, 1989–2001.CrossRefGoogle ScholarPubMed
Cortese, S, Kelly, C, Chabernaud, C, Proal, E, Di Martino, A, Milham, MP, Castellanos, FX (2012). Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies. American Journal of Psychiatry 169, 1038–1055.CrossRefGoogle ScholarPubMed
Cubillo, A, Halari, R, Smith, A, Taylor, E, Rubia, K (2012). A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with Attention Deficit Hyperactivity Disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention. Cortex 48, 194–215.CrossRefGoogle ScholarPubMed
Dove, A, Pollmann, S, Schubert, T, Wiggins, CJ, von Cramon, DY (2000). Prefrontal cortex activation in task switching: an event-related fMRI study. Brain Research. Cognitive Brain Research 9, 103–109.CrossRefGoogle ScholarPubMed
Downar, J, Crawley, AP, Mikulis, DJ, Davis, KD (2000). A multimodal cortical network for the detection of changes in the sensory environment. Nature Neuroscience 3, 277–283.CrossRefGoogle Scholar
Downar, J, Crawley, AP, Mikulis, DJ, Davis, KD (2001). The effect of task relevance on the cortical response to changes in visual and auditory stimuli: an event-related fMRI study. NeuroImage 14, 1256–1267.CrossRefGoogle ScholarPubMed
Downar, J, Crawley, AP, Mikulis, DJ, Davis, KD (2013). A Cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. Journal of Neurophysiology 87, 615–620.CrossRefGoogle Scholar
Ernst, M (2003). Neural substrates of decision making in adults with attention deficit hyperactivity disorder. American Journal of Psychiatry 160, 1061–1070.CrossRefGoogle ScholarPubMed
Fassbender, C, Zhang, H, Buzy, WM, Cortes, CR, Mizuiri, D, Beckett, L, Schweitzer, JB (2009). A lack of default network suppression is linked to increased distractibility in ADHD. Brain Research 1273, 114–128.CrossRefGoogle ScholarPubMed
Franco, AR, Pritchard, A, Calhoun, VD, Mayer, AR (2009). Interrater and intermethod reliability of default mode network selection. Human Brain Mapping 30, 2293–2303.CrossRefGoogle ScholarPubMed
Fransson, P (2006). How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations. Neuropsychologia 44, 2836–2845.CrossRefGoogle ScholarPubMed
Gerlach, KD, Spreng, RN, Gilmore, AW, Schacter, DL (2011). Solving future problems: default network and executive activity associated with goal-directed mental simulations. NeuroImage 55, 1816–1824.CrossRefGoogle ScholarPubMed
Greicius, MD, Krasnow, B, Reiss, AL, Menon, V (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proceedings of the National Academy of Sciences USA 100, 253–258.CrossRefGoogle Scholar
Greicius, MD, Menon, V (2004). Default-mode activity during a passive sensory task: uncoupled from deactivation but impacting activation. Journal of Cognitive Neuroscience 16, 1484–1492.CrossRefGoogle ScholarPubMed
Gusnard, DA, Raichle, ME (2001). Searching for a baseline: functional imaging of the resting human brain. Nature Reviews Neuroscience 2, 685–694.CrossRefGoogle ScholarPubMed
Hahn, B, Ross, TJ, Stein, EA (2007). Cingulate activation increases dynamically with response speed under stimulus unpredictability. Cerebral Cortex 17, 1664–1671.CrossRefGoogle ScholarPubMed
Helps, SK, Broyd, SJ, James, CJ, Karl, A, Chen, W, Sonuga-Barke, EJS (2010). Altered spontaneous low frequency brain activity in attention deficit/hyperactivity disorder. Brain Research 1322, 134–143.CrossRefGoogle ScholarPubMed
Karalunas, SL, Geurts, HM, Konrad, K, Bender, S, Nigg, JT (2014). Annual research review: reaction time variability in ADHD and autism spectrum disorders: measurement and mechanisms of a proposed trans-diagnostic phenotype. Journal of Child Psychology and Psychiatry, and Allied Disciplines 55, 685–710.CrossRefGoogle ScholarPubMed
Kenemans, JL, Bekker, EM, Lijffijt, M, Overtoom, CCE, Jonkman, LM, Verbaten, MN (2005). Attention deficit and impulsivity: selecting, shifting, and stopping. International Journal of Psychophysiology 58, 59–70.CrossRefGoogle ScholarPubMed
Konrad, K, Eickhoff, SB (2010). Is the ADHD brain wired differently? A review on structural and functional connectivity in attention deficit hyperactivity disorder. Human Brain Mapping 31, 904–916.CrossRefGoogle ScholarPubMed
Kooij, JJS, Francken, MH (2010). Diagnostisch Interview Voor ADHD bij volwassenen. DIVA Foundation, Den Haag.Google Scholar
Kooij, S, Buitelaar, K (1997). Zelf-rapportage vragenlijst over aandachtsproblemen en hyperactiviteit voor volwassenheid en kindertijd.Google Scholar
Kriegeskorte, N, Simmons, WK, Bellgowan, PSF, Baker, CI (2009). Circular analysis in systems neuroscience: the dangers of double dipping. Nature Neuroscience 12, 535–540.CrossRefGoogle ScholarPubMed
Kullmann, S, Pape, AA, Heni, M, Ketterer, C, Schick, F, Häring, HU, Fritsche, A, Preissl, H, Veit, R (2013). Functional network connectivity underlying food processing: disturbed salience and visual processing in overweight and obese adults. Cerebral Cortex 23, 1247–1256.CrossRefGoogle ScholarPubMed
Kurth, F, Zilles, K, Fox, PT, Laird, AR, Eickhoff, SB (2010). A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Structure & Function 214, 519–534.CrossRefGoogle ScholarPubMed
Lemiere, J, Danckaerts, M, Van Hecke, W, Mehta, MA, Peeters, R, Sunaert, S, Sonuga-Barke, E (2012). Brain activation to cues predicting inescapable delay in adolescent Attention Deficit/Hyperactivity Disorder: an fMRI pilot study. Brain Research 1450, 57–66.CrossRefGoogle ScholarPubMed
Li, CSR, Yan, P, Bergquist, KL, Sinha, R (2007). Greater activation of the ‘default’ brain regions predicts stop signal errors. NeuroImage 38, 640–648.CrossRefGoogle ScholarPubMed
Liddle, EB, Hollis, C, Batty, MJ, Groom, MJ, Totman, JJ, Liotti, M, Scerif, G, Liddle, PF (2011). Task-related default mode network modulation and inhibitory control in ADHD: effects of motivation and methylphenidate. Journal of Child Psychology and Psychiatry, and Allied Disciplines 52, 761–771.CrossRefGoogle ScholarPubMed
Linssen, AMW, Sambeth, A, Riedel, WJ, Vuurman, EFPM (2013). Higher, faster, stronger: the effect of dynamic stimuli on response preparation and CNV amplitude. Behavioural Brain Research 237, 308–312.CrossRefGoogle ScholarPubMed
Lopez-Larson, MP, King, JB, Terry, J, McGlade, EC, Yurgelun-Todd, D (2012). Reduced insular volume in attention deficit hyperactivity disorder. Psychiatry Research 204, 32–39.CrossRefGoogle ScholarPubMed
McKiernan, KA, Kaufman, JN, Kucera-Thompson, J, Binder, JR (2003). A parametric manipulation of factors affecting task-induced deactivation in functional neuroimaging. Journal of Cognitive Neuroscience 15, 394–408.CrossRefGoogle ScholarPubMed
Medford, N, Critchley, HD (2010). Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Structure & Function 214, 535–549.CrossRefGoogle ScholarPubMed
Meiran, N, Hsieh, S, Dimov, E (2010). Resolving task rule incongruence during task switching by competitor rule suppression. Journal of Experimental Psychology 36, 992–1002.Google ScholarPubMed
Menon, V, Uddin, LQ (2010). Saliency, switching, attention and control: a network model of insula function. Brain Structure & Function 214, 655–667.CrossRefGoogle ScholarPubMed
Metin, B, Roeyers, H, Wiersema, JR, van der Meere, J, Sonuga-Barke, E (2012). A meta-analytic study of event rate effects on Go/No-Go performance in attention-deficit/hyperactivity disorder. Biological Psychiatry 72, 990–996.CrossRefGoogle ScholarPubMed
Nagai, Y, Critchley, HD, Featherstone, E, Fenwick, PBC, Trimble, MR, Dolan, RJ (2004). Brain activity relating to the contingent negative variation: an fMRI investigation. NeuroImage 21, 1232–1241.CrossRefGoogle Scholar
Owens, JA (2006). The ADHD and sleep conundrum redux: moving forward. Sleep Medicine Reviews 10, 377–379.CrossRefGoogle ScholarPubMed
Owens, JA (2009). A clinical overview of sleep and attention-deficit/hyperactivity disorder in children and adolescents. Journal of the Canadian Academy of Child and Adolescent Psychiatry 18, 92–102.Google ScholarPubMed
Paloyelis, Y, Mehta, Ma, Kuntsi, J, Asherson, P (2007). Functional MRI in ADHD: a systematic literature review. Expert Review of Neurotherapeutics 7, 1337–1356.CrossRefGoogle ScholarPubMed
Peterson, BS, Potenza, MN, Wang, Z, Zhu, H, Martin, A, Marsh, R, Plessen, KJ, Yu, S (2009). An FMRI study of the effects of psychostimulants on default-mode processing during Stroop task performance in youths with ADHD. American Journal of Psychiatry 166, 1286–1294.CrossRefGoogle ScholarPubMed
Plichta, MM, Wolf, I, Hohmann, S, Baumeister, S, Boecker, R, Schwarz, AJ, Zangl, M, Mier, D, Diener, C, Meyer, P, Holz, N, Ruf, M, Gerchen, MF, Bernal-Casas, D, Kolev, V, Yordanova, J, Flor, H, Laucht, M, Banaschewski, T, Kirsch, P, Meyer-Lindenberg, A, Brandeis, D (2013). Simultaneous EEG and fMRI reveals a causally connected subcortical-cortical network during reward anticipation. Journal of Neuroscience 33, 14526–14533.CrossRefGoogle ScholarPubMed
Poljac, E, Yeung, N (2014). Dissociable neural correlates of intention and action preparation in voluntary task switching. Cerebral Cortex 24, 465–478.CrossRefGoogle ScholarPubMed
Pyka, M, Beckmann, CF, Schöning, S, Hauke, S, Heider, D, Kugel, H, Arolt, V, Konrad, C (2009). Impact of working memory load on FMRI resting state pattern in subsequent resting phases. PLoS ONE 4, e7198.CrossRefGoogle ScholarPubMed
Raichle, ME, MacLeod, AM, Snyder, AZ, Powers, WJ, Gusnard, DA, Shulman, GL (2001). A default mode of brain function. Proceedings of the National Academy of Sciences USA 98, 676–682.CrossRefGoogle ScholarPubMed
Ryan, JJ, Ward, LC (1999). Validity, reliability, and standard errors of measurement for two seven-subtest short forms of the Wechsler Adult Intelligence Scale—III. Psychological Assessment 11, 207–211.CrossRefGoogle Scholar
Seeley, WW, Menon, V, Schatzberg, AF, Keller, J, Glover, GH, Kenna, H, Reiss, AL, Greicius, MD (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience 27, 2349–2356.CrossRefGoogle ScholarPubMed
Sidlauskaite, J, Wiersema, JR, Roeyers, H, Krebs, RM, Vassena, E, Fias, W, Brass, M, Achten, E, Sonuga-Barke, E (2014). Anticipatory processes in brain state switching - Evidence from a novel cued-switching task implicating default mode and salience networks. NeuroImage 98, 359–365.CrossRefGoogle ScholarPubMed
Singh, KD, Fawcett, IP (2008). Transient and linearly graded deactivation of the human default-mode network by a visual detection task. NeuroImage 41, 100–112.CrossRefGoogle ScholarPubMed
Sonuga-Barke, E, Bitsakou, P, Thompson, M (2010 a). Beyond the dual pathway model: evidence for the dissociation of timing, inhibitory, and delay-related impairments in attention-deficit/hyperactivity disorder. Journal of the American Academy of Child & Adolescent Psychiatry 49, 345–355.Google ScholarPubMed
Sonuga-Barke, EJS, Castellanos, FX (2007). Spontaneous attentional fluctuations in impaired states and pathological conditions: a neurobiological hypothesis. Neuroscience and Biobehavioral Reviews 31, 977–986.CrossRefGoogle ScholarPubMed
Sonuga-Barke, EJS, Wiersema, JR, van der Meere, JJ, Roeyers, H (2010 b). Context-dependent dynamic processes in attention deficit/hyperactivity disorder: differentiating common and unique effects of state regulation deficits and delay aversion. Neuropsychology Review 20, 86–102.CrossRefGoogle ScholarPubMed
Spinelli, S, Joel, S, Nelson, TE, Vasa, RA, Pekar, JJ, Mostofsky, SH (2011). Different neural patterns are associated with trials preceding inhibitory errors in children with and without attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry 50, 705–715.CrossRefGoogle ScholarPubMed
Spreng, RN, Grady, CL (2010). Patterns of brain activity supporting autobiographical memory, prospection, and theory of mind, and their relationship to the default mode network. Journal of Cognitive Neuroscience 22, 1112–1123.CrossRefGoogle ScholarPubMed
Sridharan, D, Levitin, DJ, Menon, V (2008). A critical role for the right fronto-insular cortex in switching between central-executive and default-mode networks. Proceedings of the National Academy of Sciences USA 105, 12569–12574.CrossRefGoogle ScholarPubMed
Sripada, C, Kessler, D, Fang, Y, Welsh, RC, Prem Kumar, K, Angstadt, M (2014). Disrupted network architecture of the resting brain in attention-deficit/hyperactivity disorder. Human Brain Mapping 35, 4693–4705.CrossRefGoogle ScholarPubMed
Tian, L, Jiang, T, Wang, Y, Zang, Y, He, Y, Liang, M, Sui, M, Cao, Q, Hu, S, Peng, M, Zhuo, Y (2006). Altered resting-state functional connectivity patterns of anterior cingulate cortex in adolescents with attention deficit hyperactivity disorder. Neuroscience Letters 400, 39–43.CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N, Landeau, B, Papathanassiou, D, Crivello, F, Etard, O, Delcroix, N, Mazoyer, B, Joliot, M (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15, 273–289.CrossRefGoogle ScholarPubMed
Valera, EM, Spencer, RMC, Zeffiro, TA, Makris, N, Spencer, TJ, Faraone, SV, Biederman, J, Seidman, LJ (2010). Neural substrates of impaired sensorimotor timing in adult attention-deficit/hyperactivity disorder. Biological Psychiatry 68, 359–367.CrossRefGoogle ScholarPubMed
Ward, MF, Wender, PH, Reimherr, FH (1993). The Wender Utah rating scale: an aid in the retrospective diagnosis of childhood attention deficit hyperactivity disorder. American Journal of Psychiatry 150, 885–890.Google ScholarPubMed
Weissman, DH, Roberts, KC, Visscher, KM, Woldorff, MG (2006). The neural bases of momentary lapses in attention. Nature Neuroscience 9, 971–978.CrossRefGoogle ScholarPubMed
Wiersema, R, van der Meere, J, Antrop, I, Roeyers, H (2006). State regulation in adult ADHD: an event-related potential study. Journal of Clinical and Experimental Neuropsychology 28, 1113–1126.CrossRefGoogle ScholarPubMed
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