The when and where of working memory dysfunction in early-onset schizophrenia - A functional magnetic resonance imaging study

Cerebral Cortex

Volumn 25, Issue 9, 2015, Pages 2494-2506

  Bittner, Robert A ^a,b,c   Linden, David E J ^d,e   Roebroeck, Alard ^f   Härtling, Fabian ^a   Rotarska Jagiela, Anna ^a,b   Maurer, Konrad ^a   Goebel, Rainer ^f   Singer, Wolf ^b,c   Haenschel, Corinna ^a,g  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^b MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^c ERNST STRÜNGMANN INSTITUTE ESI FOR NEUROSCIENCE IN COOPERATION WITH MAX PLANCK SOCIETY   (Germany)

^d CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^e CARDIFF UNIVERSITY   (United Kingdom)

^f MAASTRICHT UNIVERSITY   (Netherlands)

^g CITY UNIVERSITY   (United Kingdom)

Author keywords

fMRI; Functional Connectivity; Prefrontal cortex; Schizophrenia; Working memory

Indexed keywords

ARIPIPRAZOLE; CHLORPROMAZINE; CLOZAPINE; OLANZAPINE; PERPHENAZINE; QUETIAPINE; RISPERIDONE; OXYGEN;

ADOLESCENT; ADULT; ARTICLE; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; EPISODIC MEMORY; EXTRASTRIATE BODY AREA; FEMALE; FUNCTIONAL CONNECTIVITY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFORMATION RETRIEVAL; MALE; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SCHIZOPHRENIA; VENTROLATERAL PREFRONTAL CORTEX; VISUAL CORTEX; VISUAL EVOKED POTENTIAL; WORKING MEMORY; ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; BLOOD; BRAIN CORTEX; COMPLICATION; IMAGE PROCESSING; MEMORY DISORDERS; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; REACTION TIME; SHORT TERM MEMORY; VASCULARIZATION; YOUNG ADULT;

ADOLESCENT; ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; CEREBRAL CORTEX; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; NEUROPSYCHOLOGICAL TESTS; OXYGEN; REACTION TIME; YOUNG ADULT;

EID: 84973424423     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu050     Document Type: Article

References (96)

1. Andreasen NC 1999. A unitary model of schizophrenia: Bleuler's "fragmented phrene" as schizencephaly. Arch Gen Psychiatry. 56:781-787.
2. Anticevic A, Repovs G, Barch DM. 2013. Working memory encoding and maintenance deficits in schizophrenia: neural evidence for activation and deactivation abnormalities. Schizophr Bull. 39:168-178.
3. Asarnow RF, Nuechterlein KH, Fogelson D, Subotnik KL, Payne DA, Russell AT, Asamen J, Kuppinger H, Kendler KS. 2001. Schizophrenia and schizophrenia-spectrum personality disorders in the first-degree relatives of children with schizophrenia: the UCLA family study. Arch Gen Psychiatry. 58:581-588.
4. Awh E, Vogel EK, Oh SH. 2006. Interactions between attention and working memory. Neuroscience. 139:201-208.
5. Badcock JC, Badcock DR, Read C, Jablensky A. 2008. Examining encoding imprecision in spatial working memory in schizophrenia. Schizophr Res. 100:144-152.
6. Baddeley A, Emslie H, Nimmo-Smith I. 1993. The Spot-the-Word test: a robust estimate of verbal intelligence based on lexical decision. Br J Clin Psychol. 32(Pt 1):55-65.
7. Barch DM 2004. Pharmacological manipulation of human working memory. Psychopharmacology (Berl). 174:126-135.
8. Barch DM, Berman MG, Engle R, Jones JH, Jonides J, Macdonald A 3rd, Nee DE, Redick TS, Sponheim SR. 2009. CNTRICS final task selection: working memory. Schizophr Bull. 35:136-152.
9. 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. Arch Gen Psychiatry. 58:280-288.
10. Barch DM, Csernansky JG. 2007. Abnormal parietal cortex activation during working memory in schizophrenia: verbal phonological coding disturbances versus domain-general executive dysfunction. Am J Psychiatry. 164:1090-1098.
11. Barch DM, Moore H, Nee DE, Manoach DS, Luck SJ. 2012. CNTRICS imaging biomarkers selection: working memory. Schizophr Bull. 38:43-52.
12. Barch DM, Smith E. 2008. The cognitive neuroscience of working memory: relevance to CNTRICS and schizophrenia. Biol Psychiatry. 64:11-17.
13. Bledowski C, Cohen Kadosh K, Wibral M, Rahm B, Bittner RA, Hoechstetter K, Scherg M, Maurer K, Goebel R, Linden DE. 2006. Mental chronometry of working memory retrieval: a combined functional magnetic resonance imaging and event-related potentials approach. J Neurosci. 26:821-829.
14. Bor D, Duncan J, Wiseman RJ, Owen AM. 2003. Encoding strategies dissociate prefrontal activity from working memory demand. Neuron. 37:361-367.
15. Callicott JH, Bertolino A, Mattay VS, Langheim FJ, Duyn J, Coppola R, Goldberg TE, Weinberger DR. 2000. Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cereb Cortex. 10:1078-1092.
16. Callicott JH, Mattay VS, Verchinski BA, Marenco S, Egan MF, Weinberger DR. 2003. Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. Am J Psychiatry. 160:2209-2215.
17. Choi JS, Park JY, Jung MH, Jang JH, Kang DH, Jung WH, Han JY, Choi CH, Hong KS, Kwon JS. 2012. Phase-specific brain change of spatial working memory processing in genetic and ultra-high risk groups of schizophrenia. Schizophr Bull. 38:1189-1199.
18. Cowan N. 2001. The magical number 4 in short-term memory: a reconsideration of mental storage capacity. Behav Brain Sci. 24:87-114; discussion 114.-185.
19. Curtis CE, D'Esposito M. 2003. Persistent activity in the prefrontal cortex during working memory. Trends Cogn Sci. 7:415-423.
20. Deserno L, Sterzer P, Wustenberg T, Heinz A, Schlagenhauf F. 2012. Reduced prefrontal-parietal effective connectivity and working memory deficits in schizophrenia. J Neurosci. 32:12-20.
21. Dias EC, Butler PD, Hoptman MJ, Javitt DC. 2011. Early sensory contributions to contextual encoding deficits in schizophrenia. Arch Gen Psychiatry. 68:654-664.
22. Driesen NR, Leung HC, Calhoun VD, Constable RT, Gueorguieva R, Hoffman R, Skudlarski P, Goldman-Rakic PS, Krystal JH. 2008. Impairment of working memory maintenance and response in schizophrenia: functional magnetic resonance imaging evidence. Biol Psychiatry. 64:1026-1034.
23. Druzgal TJ, D'Esposito M. 2001. A neural network reflecting decisions about human faces. Neuron. 32:947-955.
24. Edin F, Klingberg T, Johansson P, McNab F, Tegner J, Compte A. 2009. Mechanism for top-down control of working memory capacity. Proc Natl Acad Sci USA. 106:6802-6807.
25. Fischl B, Sereno MI, Dale AM. 1999. Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage. 9:195-207.
26. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. 1995. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med. 33:636-647.
27. Friston KJ 1998. The disconnection hypothesis. Schizophr Res. 30:115-125.
28. Fuller RL, Luck SJ, Braun EL, Robinson BM, McMahon RP, Gold JM. 2009. Impaired visual working memory consolidation in schizophrenia. Neuropsychology. 23:71-80.
29. Glahn DC, Ragland JD, Abramoff A, Barrett J, Laird AR, Bearden CE, Velligan DI. 2005. Beyond hypofrontality: a quantitative metaanalysis of functional neuroimaging studies of working memory in schizophrenia. Hum Brain Mapp. 25:60-69.
30. Goebel R, Esposito F, Formisano E. 2006. Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: from singlesubject to cortically aligned group general linear model analysis and self-organizing group independent component analysis. Hum Brain Mapp. 27:392-401.
31. Gold JM, Hahn B, Zhang WW, Robinson BM, Kappenman ES, Beck VM, Luck SJ. 2010. Reduced capacity but spared precision and maintenance of working memory representations in schizophrenia. Arch Gen Psychiatry. 67:570-577.
32. Goldman-Rakic PS. 1995. Architecture of the prefrontal cortex and the central executive. Ann N Y Acad Sci. 769:71-83.
33. Goldman-Rakic PS. 1999. The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia. Biol Psychiatry. 46:650-661.
34. Green MF, Nuechterlein KH, Gold JM, Barch DM, Cohen J, Essock S, Fenton WS, Frese F, Goldberg TE, Heaton RK et al. 2004. Approaching a consensus cognitive battery for clinical trials in schizophrenia: the NIMH-MATRICS conference to select cognitive domains and test criteria. Biol Psychiatry. 56:301-307.
35. Greenwood KE, Landau S, Wykes T. 2005. Negative symptoms and specific cognitive impairments as combined targets for improved functional outcome within cognitive remediation therapy. Schizophr Bull. 31:910-921.
36. Grill-Spector K, Kushnir T, Edelman S, Itzchak Y, Malach R. 1998. Cue-invariant activation in object-related areas of the human occipital lobe. Neuron. 21:191-202.
37. Gur RE, Calkins ME, Gur RC, Horan WP, Nuechterlein KH, Seidman LJ, Stone WS. 2007. The Consortium on the Genetics of Schizophrenia: neurocognitive endophenotypes. Schizophr Bull. 33:49-68.
38. Haenschel C, Bittner RA, Haertling F, Rotarska-Jagiela A, Maurer K, Singer W, Linden DE. 2007. Contribution of impaired early-stage visual processing to working memory dysfunction in adolescents with schizophrenia: a study with event-related potentials and functional magnetic resonance imaging. Arch Gen Psychiatry. 64:1229-1240.
39. Haenschel C, Bittner RA, Waltz J, Haertling F, Wibral M, Singer W, Linden DE, Rodriguez E. 2009. Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia. J Neurosci. 29:9481-9489.
40. Haenschel C, Linden DE, Bittner RA, Singer W, Hanslmayr S. 2010. Alpha phase locking predicts residual working memory performance in schizophrenia. Biol Psychiatry. 68:595-598.
41. Hahn B, Robinson BM, Kaiser ST, Harvey AN, Beck VM, Leonard CJ, Kappenman ES, Luck SJ, Gold JM. 2010. Failure of schizophrenia patients to overcome salient distractors during working memory encoding. Biol Psychiatry. 68:603-609.
42. Hartman M, Steketee MC, Silva S, Lanning K, McCann H. 2003. Working memory and schizophrenia: evidence for slowed encoding. Schizophr Res. 59:99-113.
43. Hollis C. 2000. Adult outcomes of child- and adolescent-onset schizophrenia: diagnostic stability and predictive validity. Am J Psychiatry. 157:1652-1659.
44. Javitt DC, Rabinowicz E, Silipo G, Dias EC. 2007. Encoding vs. retention: differential effects of cue manipulation on working memory performance in schizophrenia. Schizophr Res. 91:159-168.
45. Johnson MR, Morris NA, Astur RS, Calhoun VD, Mathalon DH, Kiehl KA, Pearlson GD. 2006. A functional magnetic resonance imaging study of working memory abnormalities in schizophrenia. Biol Psychiatry. 60:11-21.
46. Jolicoeur P, Dell'Acqua R. 1998. The demonstration of short-term consolidation. Cogn Psychol. 36:138-202.
47. Kay SR, Fiszbein A, Opler LA. 1987. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull. 13: 261-276.
48. Kim DI, Manoach DS, Mathalon DH, Turner JA, Mannell M, Brown GG, Ford JM, Gollub RL, White T, Wible C et al. 2009. Dysregulation of working memory and default-mode networks in schizophrenia using independent component analysis, an fBIRN and MCIC study. Hum Brain Mapp. 30:3795-3811.
49. Kim J, Park S, Shin YW, Jin Lee K, Kwon JS. 2006. Self-initiated encoding facilitates object working memory in schizophrenia: implications for the etiology of working memory deficit. Schizophr Res. 82:65-74.
50. Koychev I, El-Deredy W, Haenschel C, Deakin JF. 2010. Visual information processing deficits as biomarkers of vulnerability to schizophrenia: an event-related potential study in schizotypy. Neuropsychologia. 48:2205-2214.
51. 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. J Am Acad Child Adolesc Psychiatry. 51:911-920.e2.
52. Lee J, Park S. 2006. The role of stimulus salience in CPT-AX performance of schizophrenia patients. Schizophr Res. 81:191-197.
53. Lehrl S. 1995. Mehrfachwahl-Wortschatz-Intelligenztest. MWT-B. Erlangen: Straube.
54. Lencz T, Bilder RM, Turkel E, Goldman RS, Robinson D, Kane JM, Lieberman JA. 2003. Impairments in perceptual competency and maintenance on a visual delayed match-to-sample test in firstepisode schizophrenia. Arch Gen Psychiatry. 60:238-243.
55. Linden DE 2012. The challenges and promise of neuroimaging in psychiatry. Neuron. 73:8-22.
56. Linden DE, Bittner RA, Muckli L, Waltz JA, Kriegeskorte N, Goebel R, Singer W, Munk MH. 2003. Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a frontoparietal network. Neuroimage. 20:1518-1530.
57. Luck SJ, Gold JM. 2008. The construct of attention in schizophrenia. Biol Psychiatry. 64:34-39.
58. Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB. 1995. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA. 92:8135-8139.
59. Manoach DS 2003. Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophr Res. 60:285-298.
60. 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. Biol Psychiatry. 48:99-109.
61. Manoach DS, Press DZ, Thangaraj V, Searl MM, Goff DC, Halpern E, Saper CB, Warach S. 1999. Schizophrenic subjects activate dorsolateral prefrontal cortex during a working memory task, as measured by fMRI. Biol Psychiatry. 45:1128-1137.
62. Mayer JS, Bittner RA, Nikolic D, Bledowski C, Goebel R, Linden DE. 2007. Common neural substrates for visual working memory and attention. Neuroimage. 36:441-453.
63. Mayer JS, Park S. 2012. Working memory encoding and false memory in schizophrenia and bipolar disorder in a spatial delayed response task. J Abnorm Psychol. 121:784-94.
64. Mayer JS, Roebroeck A, Maurer K, Linden DE. 2010. Specialization in the default mode: task-induced brain deactivations dissociate between visual working memory and attention. Hum Brain Mapp. 31:126-139.
65. Meda SA, Stevens MC, Folley BS, Calhoun VD, Pearlson GD. 2009. Evidence for anomalous network connectivity during working memory encoding in schizophrenia: an ICA based analysis. PloS One. 4:e7911.
66. 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. Schizophr Bull. 38:803-813.
67. Meyer-Lindenberg A. 2010. From maps to mechanisms through neuroimaging of schizophrenia. Nature. 468:194-202.
68. Meyer-Lindenberg A, Weinberger DR. 2006. Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat Rev. 7:818-827.
69. Meyer-Lindenberg AS, Olsen RK, Kohn PD, Brown T, Egan MF, Weinberger DR, Berman KF. 2005. Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Arch Gen Psychiatry. 62:379-386.
70. Munk MH, Linden DE, Muckli L, Lanfermann H, Zanella FE, Singer W, Goebel R. 2002. Distributed cortical systems in visual short-term memory revealed by event-related functional magnetic resonance imaging. Cereb Cortex. 12:866-876.
71. Nee DE, Jonides J. 2008. Neural correlates of access to short-term memory. Proc Natl Acad Sci USA. 105:14228-14233.
72. Noesselt T, Hillyard SA, Woldorff MG, Schoenfeld A, Hagner T, Jancke L, Tempelmann C, Hinrichs H, Heinze HJ. 2002. Delayed striate cortical activation during spatial attention. Neuron. 35:575-587.
73. Oertel-Knoechel V, Bittner RA, Knochel C, Prvulovic D, Hampel H. 2011. Discovery and development of integrative biological markers for schizophrenia. Prog Neurobiol. 95:686-702.
74. Oldfield RC 1971. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 9:97-113.
75. Park HJ, Levitt J, Shenton ME, Salisbury DF, Kubicki M, Kikinis R, Jolesz FA, McCarley RW. 2004. An MRI study of spatial probability brain map differences between first-episode schizophrenia and normal controls. Neuroimage. 22:1231-1246.
76. Perlstein WM, Carter CS, Noll DC, Cohen JD. 2001. Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenia. Am J Psychiatry. 158:1105-1113.
77. Perlstein WM, Dixit NK, Carter CS, Noll DC, Cohen JD. 2003. Prefrontal cortex dysfunction mediates deficits in working memory and prepotent responding in schizophrenia. Biol Psychiatry. 53:25-38.
78. Potkin SG, Turner JA, Brown GG, McCarthy G, Greve DN, Glover GH, Manoach DS, Belger A, Diaz M, Wible CG et al. 2009. Working memory and DLPFC inefficiency in schizophrenia: the FBIRN study. Schizophr Bull. 35:19-31.
79. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. 2001. A default mode of brain function. Proc Natl Acad Sci USA. 98:676-682.
80. Reilly JL, Harris MS, Keshavan MS, Sweeney JA. 2006. Adverse effects of risperidone on spatial working memory in first-episode schizophrenia. Arch Gen Psychiatry. 63:1189-1197.
81. Roebroeck A, Formisano E, Goebel R. 2005. Mapping directed influence over the brain using Granger causality and fMRI. Neuroimage. 25:230-242.
82. Sakai K, Rowe JB, Passingham RE. 2002. Active maintenance in prefrontal area 46 creates distractor-resistant memory. Nat Neurosci. 5:479-484.
83. Sass H, Wittchen H. 2003. Diagnostisches und Statistisches Manual Psychischer Störungen. Hogrefe, Bern, Switzerland.
84. Schlosser RG, Koch K, Wagner G, Nenadic I, Roebel M, Schachtzabel C, Axer M, Schultz C, Reichenbach JR, Sauer H. 2008. Inefficient executive cognitive control in schizophrenia is preceded by altered functional activation during information encoding: an fMRI study. Neuropsychologia. 46:336-347.
85. Sehatpour P, Molholm S, Schwartz TH, Mahoney JR, Mehta AD, Javitt DC, Stanton PK, Foxe JJ. 2008. A human intracranial study of longrange oscillatory coherence across a frontal-occipital-hippocampal brain network during visual object processing. Proc Natl Acad Sci USA. 105:4399-4404.
86. Silver H, Feldman P, Bilker W, Gur RC. 2003. Working memory deficit as a core neuropsychological dysfunction in schizophrenia. Am J Psychiatry. 160:1809-1816.
87. Stephane M, Pellizzer G. 2007. The dynamic architecture of working memory in schizophrenia. Schizophr Res. 92:160-167.
88. Tan HY, Callicott JH, Weinberger DR. 2007. Dysfunctional and compensatory prefrontal cortical systems, genes and the pathogenesis of schizophrenia. Cereb Cortex. 17(SUPPL. 1):i171-i181.
89. Tan HY, Sust S, Buckholtz JW, Mattay VS, Meyer-Lindenberg A, Egan MF, Weinberger DR, Callicott JH. 2006. Dysfunctional prefrontal regional specialization and compensation in schizophrenia. Am J Psychiatry. 163:1969-1977.
90. Tek C, Gold J, Blaxton T, Wilk C, McMahon RP, Buchanan RW. 2002. Visual perceptual and working memory impairments in schizophrenia. Arch Gen Psychiatry. 59:146-153.
91. Thormodsen R, Jensen J, Holmen A, Juuhl-Langseth M, Emblem KE, Andreassen OA, Rund BR. 2011. Prefrontal hyperactivation during a working memory task in early-onset schizophrenia spectrum disorders: an fMRI study. Psychiatry Res. 194:257-262.
92. Ungerleider LG, Courtney SM, Haxby JV. 1998. A neural system for human visual working memory. Proc Natl Acad Sci USA. 95:883-890.
93. White T, Hongwanishkul D, Schmidt M. 2011a. Increased anterior cingulate and temporal lobe activity during visuospatial working memory in children and adolescents with schizophrenia. Schizophr Res. 125:118-128.
94. White T, Schmidt M, Kim DI, Calhoun VD. 2011b. Disrupted functional brain connectivity during verbal working memory in children and adolescents with schizophrenia. Cereb Cortex. 21:510-518.
95. Whitfield-Gabrieli S, Thermenos HW, Milanovic S, Tsuang MT, Faraone SV, McCarley RW, Shenton ME, Green AI, Nieto-Castanon A, LaViolette P et al. 2009. Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc Natl Acad Sci USA. 106:1279-1284.
96. Winterer G, Weinberger DR. 2004. Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends Neurosci. 27:683-690.