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Failed cooperative, but not competitive, interaction between large-scale brain networks impairs working memory in schizophrenia

Published online by Cambridge University Press:  08 January 2016

W. Pu ,
Q. Luo ,
L. Palaniyappan ,
Z. Xue ,
S. Yao ,
J. Feng  and
Z. Liu
W. Pu
Affiliation:
Medical Psychological Institute, Second Xiangya Hospital, Central South University, Changsha, People's Republic of China Institute of Mental Health, Second Xiangya Hospital, Central South University, Changsha, People's Republic of China
Q. Luo
Affiliation:
School of Life Sciences, Fudan University, Shanghai, People's Republic of China Centre for Computational Systems Biology, School of Mathematical Sciences, Fudan University, Shanghai, People's Republic of China
L. Palaniyappan
Affiliation:
Department of Psychiatry, Schulich School of Medicine and Dentistry, University of Western Ontario, London, Ontario, Canada Robarts Research Institute, University of Western Ontario, London, Ontario, Canada
Z. Xue
Affiliation:
Institute of Mental Health, Second Xiangya Hospital, Central South University, Changsha, People's Republic of China
S. Yao
Affiliation:
Medical Psychological Institute, Second Xiangya Hospital, Central South University, Changsha, People's Republic of China
J. Feng*
Affiliation:
School of Life Sciences, Fudan University, Shanghai, People's Republic of China Centre for Computational Systems Biology, School of Mathematical Sciences, Fudan University, Shanghai, People's Republic of China Shanghai Center for Mathematical Sciences, Shanghai, People's Republic of China Department of Computer Science, University of Warwick, Coventry, UK Collaborative Innovation Center for Brain Science, Fudan University, Shanghai, People's Republic of China
Z. Liu*
Affiliation:
Institute of Mental Health, Second Xiangya Hospital, Central South University, Changsha, People's Republic of China The State Key Laboratory of Medical Genetics, Central South University, People's Republic of China
*
*Addresses for correspondence: Z. Liu, M.D., Ph.D., Institute of Mental Health, Second Xiangya Hospital, Central South University, Changsha 410011, People's Republic of China; J. Feng, Ph.D., School of Life Sciences, Fudan University, Shanghai 200433, People's Republic of China. (Email: zningl@163.com) [Z.L.] (Email: jianfeng64@gmail.com) [J.F.]
*Addresses for correspondence: Z. Liu, M.D., Ph.D., Institute of Mental Health, Second Xiangya Hospital, Central South University, Changsha 410011, People's Republic of China; J. Feng, Ph.D., School of Life Sciences, Fudan University, Shanghai 200433, People's Republic of China. (Email: zningl@163.com) [Z.L.] (Email: jianfeng64@gmail.com) [J.F.]
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Abstract

Background

A large-scale network named the default mode network (DMN) dynamically cooperates and competes with an external attention system (EAS) to facilitate various cognitive functioning that is prominently impaired in schizophrenia. However, it is unclear whether the cognitive deficit in schizophrenia is related to the disrupted competition and/or cooperation between these two networks.

Method

A total of 35 schizophrenia patients and 30 healthy controls were scanned using gradient-echo echo-planar imaging during n-back working memory (WM) processing. Brain activities of the DMN and EAS were measured using general linear modelling of the functional magnetic resonance imaging data. Dynamic interaction between the DMN and EAS was decomposed into two directions using Granger causality analysis.

Results

We observed a significant failure of DMN suppression in patients with schizophrenia, which was significantly related to WM/attentional deficit. Granger causality modelling showed that in healthy controls, while the EAS inhibitorily influenced the DMN, the DMN exerted an ‘excitatory’ or cooperative influence back on the EAS, especially in those with lower WM accuracy. In schizophrenia, this ‘excitatory’ DMN→EAS influence within the reciprocal EAS–DMN loop was significantly reduced, especially in patients with WM/attentional deficit.

Conclusions

The dynamic interaction between the DMN and EAS is likely to be comprised of both competitive and cooperative influences. In healthy controls, both the ‘inhibitory’ EAS→DMN interaction and ‘excitatory’ DMN→EAS interaction are correlated with WM performance. In schizophrenia, reduced ‘cooperative’ influence from the DMN to dorsal nodes of the EAS occurs in the context of non-suppression of the DMN and may form a possible pathophysiological substrate of WM deficit and attention disorder.

Keywords

Default mode networkdynamic interactionexternal attention systemschizophreniaworking memory
Type
Original Articles
Information
Psychological Medicine , Volume 46 , Issue 6 , April 2016 , pp. 1211 - 1224
Copyright
Copyright © Cambridge University Press 2016 

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References

Andreasen, NC (1983). Scale for the Assessment of Negative Symptoms. University of Iowa: Iowa City, IA.Google Scholar
Andreasen, NC (1984). Scale for the Assessment of Positive Symptoms. University of Iowa: Iowa City, IA.Google Scholar
Anticevic, A, Repovs, G, Barch, DM (2013). Working memory encoding and maintenance deficits in schizophrenia: neural evidence for activation and deactivation abnormalities. Schizophrenia Bulletin 39, 168–178.Google Scholar
Barch, DM, Carter, CS, Braver, TS, Sabb, FW, MacDonald, A 3rd Noll, DC, Cohen, JD (2001). Selective deficits in prefrontal cortex function in medication-naive patients with schizophrenia. Archives of General Psychiatry 58, 280–288.Google Scholar
Barch, DM, Ceaser, A (2012). Cognition in schizophrenia: core psychological and neural mechanisms. Trends in Cognitive Sciences 16, 27–34.CrossRefGoogle ScholarPubMed
Bluhm, RL, Clark, CR, McFarlane, AC, Moores, KA, Shaw, ME, Lanius, RA (2011). Default network connectivity during a working memory task. Human Brain Mapping 32, 1029–1035.Google Scholar
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.Google Scholar
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 Science 1124, 1–38.CrossRefGoogle ScholarPubMed
Buschman, TJ, Miller, EK (2007). Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315, 1860–1862.CrossRefGoogle ScholarPubMed
Chen, G, Hamilton, JP, Thomason, ME, Gotlib, IH, Saad, ZS, Cox, RW (2009). Granger causality via vector auto-regression tuned for fMRI data analysis. Proceedings of the International Society for Magnetic Resonance in Medicine 17, 1718.Google Scholar
Cocchi, L, Zalesky, A, Fornito, A, Mattingley, JB (2013). Dynamic cooperation and competition between brain systems during cognitive control. Trends in Cognitive Science 17, 493–501.CrossRefGoogle ScholarPubMed
Corbetta, M, Patel, G, Shulman, GL (2008). The reorienting system of the human brain: from environment to theory of mind. Neuron 58, 306–324.Google Scholar
Coyle, JT (2006). Glutamate and schizophrenia: beyond the dopamine hypothesis. Cell and Molecular Neurobiology 26, 365–384.Google Scholar
de Leeuw, M, Kahn, RS, Zandbelt, BB, Widschwendter, CG, Vink, M (2013). Working memory and default mode network abnormalities in unaffected siblings of schizophrenia patients. Schizophrenia Research 150, 555–562.Google Scholar
Demirci, O, Stevens, MC, Andreasen, NC, Michael, A, Liu, J, White, T, Pearlson, GD, Clark, VP, Calhoun, VD (2009). Investigation of relationships between fMRI brain networks in the spectral domain using ICA and Granger causality reveals distinct differences between schizophrenia patients and healthy controls. NeuroImage 46, 419–431.CrossRefGoogle ScholarPubMed
De Pisapia, N, Turatto, M, Lin, P, Jovicich, J, Caramazza, A (2012). Unconscious priming instructions modulate activity in default and executive networks of the human brain. Cerebral Cortex 22, 639–649.Google Scholar
Ding, M, Chen, Y, Bressler, SL (2006). Granger causality: basic theory and application to neuroscience. In Handbook of Time Series Analysis: Recent Theoretical Developments and Applications (ed. Schelter, B., Winterhalder, M. and Timmer, J.), chapter 17. Wiley-VCH Verlag GmbH & Co. KGaA: Weinheim, Germany.Google Scholar
Dosenbach, NU, Visscher, KM, Palmer, ED, Miezin, FM, Wenger, KK, Kang, HC, Burgund, ED, Grimes, AL, Schlaggar, BL, Petersen, SE (2006). A core system for the implementation of task sets. Neuron 50, 799–812.Google Scholar
Eichele, T, Debener, S, Calhoun, VD, Specht, K, Engel, AK, Hugdahl, K, von Cramon, DY, Ullsperger, M (2008). Prediction of human errors by maladaptive changes in event-related brain networks. Proceedings of the National Academy of Sciences USA 105, 6173–6178.Google Scholar
First, MB, Spitzer, RL, Gibbon, M (editors) (1996). Structured Clinical Interview for DSM-IV Axis I Disorder-Patient Edition (SCID-I/P). Biometrics Research Department, New York State Psychiatric Institute: New York.Google Scholar
Fornito, A, Harrison, BJ, Zalesky, A, Simons, JS (2012). Competitive and cooperative dynamics of large-scale brain functional networks supporting recollection. Proceedings of the National Academy of Sciences USA 109, 12788–12793.CrossRefGoogle ScholarPubMed
Fox, MD, Snyder, AZ, Vincent, JL, Corbetta, M, Van Essen, DC, Raichle, ME (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences USA 102, 9673–9678.Google Scholar
Fox, MD, Zhang, D, Snyder, AZ, Raichle, ME (2009). The global signal and observed anticorrelated resting state brain networks. Journal of Neurophysiology 101, 3270–3283.Google Scholar
Friston, K, Moran, R, Seth, AK (2013). Analysing connectivity with Granger causality and dynamic causal modelling. Current Opinion in Neurobiology 23, 172–178.CrossRefGoogle ScholarPubMed
Fryer, SL, Woods, SW, Kiehl, KA, Calhoun, VD, Pearlson, GD, Roach, BJ, Ford, JM, Srihari, VH, McGlashan, TH, Mathalon, DH (2013). Deficient suppression of default mode regions during working memory in individuals with early psychosis and at clinical high-risk for psychosis. Frontiers in Psychiatry 4, 92.Google Scholar
Garrity, A, Pearlson, G, McKiernan, K, Lloyd, D, Kiehl, K, Calhoun, V (2007). Aberrant “default mode” functional connectivity in schizophrenia. American Journal of Psychiatry 164, 450–457.Google Scholar
Geng, JJ, Mangun, GR (2009). Anterior intraparietal sulcus is sensitive to bottom-up attention driven by stimulus salience. Journal of Cognitive Neuroscience 21, 1584–1601.Google Scholar
Hagmann, P, Cammoun, L, Gigandet, X, Meuli, R, Honey, CJ, Wedeen, VJ, Sporns, O (2008). Mapping the structural core of human cerebral cortex. PLoS Biology 6, e159.CrossRefGoogle ScholarPubMed
Hamilton, JP, Chen, G, Thomason, ME, Schwartz, ME, Gotlib, IH (2011). Investigating neural primacy in major depressive disorder: multivariate Granger causality analysis of resting-state fMRI time-series data. Molecular Psychiatry 16, 763–772.CrossRefGoogle ScholarPubMed
Kelly, AM, Uddin, LQ, Biswal, BB, Castellanos, FX, Milham, MP (2008). Competition between functional brain networks mediates behavioral variability. NeuroImage 39, 527–537.Google Scholar
Kim, MA, Tura, E, Potkin, SG, Fallon, JH, Manoach, DS, Calhoun, VD; FBIRN, , Turner, JA (2010). Working memory circuitry in schizophrenia shows widespread cortical inefficiency and compensation. Schizophrenia Research 117, 42–51.Google Scholar
Kyriakopoulos, M, Dima, D, Roiser, JP, Corrigall, R, Barker, GJ, Frangou, S (2012). Abnormal functional activation and connectivity in the working memory network in early-onset schizophrenia. Journal of the American Academy of Child and Adolescent Psychiatry 51, 911–920.e2.CrossRefGoogle ScholarPubMed
Leech, R, Braga, R, Sharp, DJ (2012). Echoes of the brain within the posterior cingulate cortex. Journal of Neuroscience 32, 215–222.Google Scholar
Leech, R, Kamourieh, S, Beckmann, CF, Sharp, DJ (2011). Fractionating the default mode network: distinct contributions of the ventral and dorsal posterior cingulate cortex to cognitive control. Journal of Neuroscience 31, 3217–3224.CrossRefGoogle ScholarPubMed
Leech, R, Sharp, DJ (2013). The role of the posterior cingulate cortex in cognition and disease. Brain 137, 12–32.CrossRefGoogle ScholarPubMed
Lett, TA, Voineskos, AN, Kennedy, JL, Levine, B, Daskalakis, ZJ (2014). Treating working memory deficits in schizophrenia: a review of the neurobiology. Biological Psychiatry 75, 361–370.CrossRefGoogle ScholarPubMed
Li, L, Gratton, C, Yao, D, Knight, RT (2010). Role of frontal and parietal cortices in the control of bottom-up and top-down attention in humans. Brain Research 1344, 173–184.Google Scholar
Liang, X, Zou, Q, He, Y, Yang, Y (2015). Topologically reorganized connectivity architecture of default-mode, executive-control, and salience networks across working memory task loads. Cerebral Cortex. Published online 16 January 2015. doi:10.1093/cercor/bhu316.Google Scholar
Liu, H, Kaneko, Y, Ouyang, X, Li, L, Hao, Y, Chen, EY, Jiang, T, Zhou, Y, Liu, Z (2012). Schizophrenic patients and their unaffected siblings share increased resting-state connectivity in the task-negative network but not its anticorrelated task-positive network. Schizophrenia Bulletin 38, 285–294.CrossRefGoogle Scholar
Lui, S, Li, T, Deng, W, Jiang, L, Wu, Q, Tang, H, Yue, Q, Huang, X, Chan, RC, Collier, DA (2010). Short-term effects of antipsychotic treatment on cerebral function in drug-naive first-episode schizophrenia revealed by “resting state” functional magnetic resonance imaging. Archives of General Psychiatry 67, 783–792.Google Scholar
Luo, Q, Ge, T, Grabenhorst, F, Feng, J, Rolls, ET (2013). Attention-dependent modulation of cortical taste circuits revealed by Granger causality with signal-dependent noise. PLoS Computational Biology 9, e1003265.CrossRefGoogle ScholarPubMed
MacDonald, AW, Schulz, SC (2009). What we know: findings that every theory of schizophrenia should explain. Schizophrenia Bulletin 3, 493–508.CrossRefGoogle Scholar
Mannell, MV, Franco, AR, Calhoun, VD, Canive, JM, Thoma, RJ, Mayer, AR (2010). Resting state and task-induced deactivation: a methodological comparison in patients with schizophrenia and healthy controls. Human Brain Mapping 31, 424–437.CrossRefGoogle ScholarPubMed
Manoach, DS, Gollub, RL, Benson, ES, Searl, MM, Goff, DC, Halpern, E, Saper, CB, Rauch, SL (2000). Schizophrenic subjects show aberrant fMRI activation of dorsolateral prefrontal cortex and basal ganglia during working memory performance. Biological Psychiatry 48, 99–109.CrossRefGoogle ScholarPubMed
Margulies, DS, Vincent, JL, Kelly, C, Lohmann, G, Uddin, LQ, Biswal, BB, Villringer, A, Castellanos, FX, Milham, MP, Petrides, M (2009). Precuneus shares intrinsic functional architecture in humans and monkeys. Proceedings of the National Academy of Sciences USA 106, 20069–20074.Google Scholar
Mason, MF, Norton, MI, Van Horn, JD, Wegner, DM, Grafton, ST, Macrae, CN (2007). Wandering minds: the default network and stimulus-independent thought. Science 315, 393–395.Google Scholar
Metzak, PD, Riley, JD, Wang, L, Whitman, JC, Ngan, ET, Woodward, TS (2012). Decreased efficiency of task-positive and task-negative networks during working memory in schizophrenia. Schizophrenia Bulletin 38, 803–813.CrossRefGoogle ScholarPubMed
Minzenberg, MJ, Carter, CS (2012). Developing treatments for impaired cognition in schizophrenia. Trends in Cognitive Sciences 16, 35–42.Google Scholar
Palaniyappan, L, Simmonite, M, White, TP, Liddle, EB, Liddle, PF (2013). Neural primacy of the salience processing system in schizophrenia. Neuron 79, 814–828.CrossRefGoogle ScholarPubMed
Pomarol-Clotet, E, Salvador, R, Sarro, S, Gomar, J, Vila, F, Martinez, A, Guerrero, A, Ortiz-Gil, J, Sans-Sansa, B, Capdevila, A, Cebamanos, JM, McKenna, PJ (2008). Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network? Psychological Medicine 38, 1185–1193.CrossRefGoogle ScholarPubMed
Power, JD, Barnes, KA, Snyder, AZ, Schlaggar, BL, Petersen, SE (2012). Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59, 2142–2154.CrossRefGoogle ScholarPubMed
Prado, J, Weissman, DH (2011). Heightened interactions between a key default-mode region and a key task-positive region are linked to suboptimal current performance but to enhanced future performance. NeuroImage 56, 2276–2282.CrossRefGoogle Scholar
Premereur, E, Vanduffel, W, Janssen, P (2011). Functional heterogeneity of macaque lateral intraparietal neurons. Journal of Neuroscience 31, 12307–12317.Google Scholar
Raichle, ME (2010). The brain's dark energy. Scientific American 302, 44–49.Google Scholar
Sala-Llonch, R, Pena-Gomez, C, Arenaza-Urquijo, EM, Vidal-Pineiro, D, Bargallo, N, Junque, C, Bartres-Faz, D (2012). Brain connectivity during resting state and subsequent working memory task predicts behavioural performance. Cortex 48, 1187–1196.CrossRefGoogle ScholarPubMed
Schippers, MB, Renken, R, Keysers, C (2011). The effect of intra- and inter-subject variability of hemodynamic responses on group level Granger causality analyses. NeuroImage 57, 22–36.Google 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.Google Scholar
Simons, JS, Henson, RN, Gilbert, SJ, Fletcher, PC (2008). Separable forms of reality monitoring supported by anterior prefrontal cortex. Journal of Cognitive Neuroscience 20, 447–457.Google Scholar
Spreng, RN, Stevens, WD, Chamberlain, JP, Gilmore, AW, Schacter, DL (2010). Default network activity, coupled with the frontoparietal control network, supports goal-directed cognition. NeuroImage 53, 303–317.Google Scholar
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.Google Scholar
Suzuki, M, Gottlieb, J (2013). Distinct neural mechanisms of distractor suppression in the frontal and parietal lobe. Nature Neuroscience 16, 98–104.CrossRefGoogle ScholarPubMed
Uddin, LQ, Kelly, AM, Biswal, BB, Castellanos, FX, Milham, MP (2009). Functional connectivity of default mode network components: correlation, anticorrelation, and causality. Human Brain Mapping 30, 625–637.Google Scholar
Van Dijk, KR, Sabuncu, MR, Buckner, RL (2012). The influence of head motion on intrinsic functional connectivity MRI. NeuroImage 59, 431–438.Google Scholar
Vincent, JL, Kahn, I, Snyder, AZ, Raichle, ME, Buckner, RL (2008). Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. Journal of Neurophysiology 100, 3328–3342.Google Scholar
Voon, V, Brezing, C, Gallea, C, Ameli, R, Roelofs, K, LaFrance, WC Jr., Hallett, M (2010). Emotional stimuli and motor conversion disorder. Brain 133, 1526–1536.Google Scholar
Weissman, D, Roberts, K, Visscher, K, Woldorff, M (2006). The neural bases of momentary lapses in attention. Nature Neuroscience 9, 971–978.CrossRefGoogle ScholarPubMed
Wen, X, Liu, Y, Yao, L, Ding, M (2013). Top-down regulation of default mode activity in spatial visual attention. Journal of Neuroscience 33, 6444–6453.Google Scholar
Whitfield-Gabrieli, S, Thermenos, HW, Milanovic, S, Tsuang, MT, Faraone, SV, McCarley, RW, Shenton, ME, Green, AI, Nieto-Castanon, A, LaViolette, P (2009). Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proceedings of the National Academy of Sciences USA 106, 1279.Google Scholar
Wu, G, Wang, Y, Mwansisya, TE, Pu, W, Zhang, H, Liu, C, Yang, Q, Chen, EY, Xue, Z, Liu, Z, Shan, B (2014). Effective connectivity of the posterior cingulate and medial prefrontal cortices relates to working memory impairment in schizophrenic and bipolar patients. Schizophrenia Research 158, 85–90.CrossRefGoogle ScholarPubMed
Wu, T, Wang, J, Wang, C, Hallett, M, Zang, Y, Wu, X, Chan, P (2012). Basal ganglia circuits changes in Parkinson's disease patients. Neuroscience Letters 524, 55–59.CrossRefGoogle ScholarPubMed
Yaakub, SN, Dorairaj, K, Poh, JS, Asplund, CL, Krishnan, R, Lee, J, Keefe, RS, Adcock, RA, Wood, SJ, Chee, MW (2013). Preserved working memory and altered brain activation in persons at risk for psychosis. American Journal of Psychiatry 170, 1297–1307.Google Scholar
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