Working memory in unaffected relatives of patients with schizophrenia: A meta-analysis of functional magnetic resonance imaging studies

Schizophrenia Bulletin

Volumn 42, Issue 4, 2016, Pages 1068-1077

  Zhang, Ruibin ^a   Picchioni, Marco ^b,c   Allen, Paul ^c,d   Toulopoulou, Timothea ^a,c,e  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b St Andrew s Academic Department   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d UNIVERSITY OF ROEHAMPTON   (United Kingdom)

^e BILKENT UNIVERSITY   (Turkey)

Author keywords

Dorsolateral prefrontal cortex; Endophenotype; Functional magnetic resonance imaging (fMRI); Intermediate phenotype; Meta analyses

Indexed keywords

ACTIVATION LIKELIHOOD ESTIMATION; ARTICLE; FAMILIAL DISEASE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFERIOR FRONTAL GYRUS; MEASUREMENT; META ANALYSIS; MIDDLE FRONTAL GYRUS; PRIORITY JOURNAL; SCHIZOPHRENIA; SENSITIVITY ANALYSIS; THALAMUS; WORKING MEMORY; ADOLESCENT; ADULT; ENDOPHENOTYPE; FAMILY; FEMALE; FUNCTIONAL NEUROIMAGING; MALE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX; SHORT TERM MEMORY; STATISTICS AND NUMERICAL DATA; YOUNG ADULT;

ADOLESCENT; ADULT; ENDOPHENOTYPES; FAMILY; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MEMORY, SHORT-TERM; MIDDLE AGED; PREFRONTAL CORTEX; SCHIZOPHRENIA; YOUNG ADULT;

EID: 84979224608     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbv221     Document Type: Article

References (73)

1. Tandon R, Bruijnzeel D, Rankupalli B. Does change in definition of psychotic symptoms in diagnosis of schizophrenia in DSM-5 affect caseness? Asian J Psychiatr. 2013;6:330-332.
2. Consortium SWGotPG. Biological insights from 108 schizophrenia-associated genetic loci. Nature. 2014;511:421-427.
3. Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003;160:636-645.
4. Braff DL, Freedman R, Schork NJ, Gottesman II. Deconstructing schizophrenia: an overview of the use of endophenotypes in order to understand a complex disorder. Schizophr Bull. 2007;33:21-32.
5. Baddeley A. Working memory: looking back and looking forward. Nat Rev Neurosci. 2003;4:829-839.
6. Lee J, Park S. Working memory impairments in schizophrenia: a meta-analysis. J Abnorm Psychol. 2005;114:599-611.
7. Daban C, Amado I, Baylé F, et al. Disorganization syndrome is correlated to working memory deficits in unmedicated schizophrenic patients with recent onset schizophrenia. Schizophr Res. 2003;61:323-324.
8. Haenschel C, Bittner RA, Waltz J, et al. Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia. J Neurosci. 2009;29:9481-9489.
9. Tyson PJ, Laws KR, Roberts KH, Mortimer AM. A longitudinal analysis of memory in patients with schizophrenia. J Clin Exp Neuropsychol. 2005;27:718-734.
10. Carrión RE, McLaughlin D, Auther AM, Olsen R, Correll CU, Cornblatt BA. The impact of psychosis on the course of cognition: a prospective, nested case-control study in individuals at clinical high-risk for psychosis. Psychol Med. 2015;45:3341-3354.
11. Hill SK, Reilly JL, Keefe RS, et al. Neuropsychological impairments in schizophrenia and psychotic bipolar disorder: findings from the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP) study. Am J Psychiatry. 2014;170:1275-1284.
12. Lett TA, Voineskos AN, Kennedy JL, Levine B, Daskalakis ZJ. Treating working memory deficits in schizophrenia: a review of the neurobiology. Biol Psychiatry. 2014;75:361-370.
13. Park S, Holzman PS, Goldman-Rakic PS. Spatial working memory deficits in the relatives of schizophrenic patients. Arch Gen Psychiatry. 1995;52:821-828.
14. Pirkola T, Tuulio-Henriksson A, Glahn D, et al. Spatial working memory function in twins with schizophrenia and bipolar disorder. Biol Psychiatry. 2005;58:930-936.
15. Toulopoulou T, Picchioni M, Rijsdijk F, et al. Substantial genetic overlap between neurocognition and schizophrenia: genetic modeling in twin samples. Arch Gen Psychiatry. 2007;64:1348-1355.
16. Seidman LJ, Meyer EC, Giuliano AJ, et al. Auditory working memory impairments in individuals at familial high risk for schizophrenia. Neuropsychology. 2012;26:288-303.
17. Horan WP, Braff DL, Nuechterlein KH, et al. Verbal working memory impairments in individuals with schizophrenia and their first-degree relatives: findings from the Consortium on the Genetics of Schizophrenia. Schizophr Res. 2008;103:218-228.
18. Mark W, Toulopoulou T. Cognitive intermediate phenotype and genetic risk for psychosis. Curr Opin Neurobiol. 2015;36:23-30.
19. Bora E, Lin A, Wood SJ, Yung AR, McGorry PD, Pantelis C. Cognitive deficits in youth with familial and clinical high risk to psychosis: a systematic review and meta-analysis. Acta Psychiatr Scand. 2014;130:1-15.
20. Sui J, Pearlson GD, Du Y, et al. In search of multimodal neuroimaging biomarkers of cognitive deficits in schizophrenia. Biol Psychiatry. 2015;78:794-804.
21. Voineskos AN, Foussias G, Lerch J, et al. Neuroimaging evidence for the deficit subtype of schizophrenia. JAMA Psychiatry. 2013;70:472-480.
22. Thermenos HW, Keshavan MS, Juelich RJ, et al. A review of neuroimaging studies of young relatives of individuals with schizophrenia: a developmental perspective from schizotaxia to schizophrenia. Am J Med Genet B Neuropsychiatr Genet. 2013;162B:604-635.
23. Wheeler AL, Chakravarty MM, Lerch JP, et al. Disrupted prefrontal interhemispheric structural coupling in schizophrenia related to working memory performance. Schizophr Bull. 2014;40:914-924.
24. Potkin SG, Turner JA, Brown GG, et al.; FBIRN. Working memory and DLPFC inefficiency in schizophrenia: the FBIRN study. Schizophr Bull. 2009;35:19-31.
25. Brahmbhatt SB, Haut K, Csernansky JG, Barch DM. Neural correlates of verbal and nonverbal working memory deficits in individuals with schizophrenia and their high-risk siblings. Schizophr Res. 2006;87:191-204.
26. Karlsgodt KH, Glahn DC, van Erp TG, et al. The relationship between performance and fMRI signal during working memory in patients with schizophrenia, unaffected co-twins, and control subjects. Schizophr Res. 2007;89:191-197.
27. Callicott JH, Egan MF, Mattay VS, et al. Abnormal fMRI response of the dorsolateral prefrontal cortex in cognitively intact siblings of patients with schizophrenia. Am J Psychiatry. 2003;160:709-719.
28. MacDonald AW III, Thermenos HW, Barch DM, Seidman LJ. Imaging genetic liability to schizophrenia: systematic review of FMRI studies of patients' nonpsychotic relatives. Schizophr Bull. 2009;35:1142-1162.
29. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. Coordinate-based activation likelihood estimation metaanalysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp. 2009;30:2907-2926.
30. Caspers S, Zilles K, Laird AR, Eickhoff SB. ALE meta-analysis of action observation and imitation in the human brain. Neuroimage. 2010;50:1148-1167.
31. Minzenberg MJ, Laird AR, Thelen S, Carter CS, Glahn DC. Meta-analysis of 41 functional neuroimaging studies of executive function in schizophrenia. Arch Gen Psychiatry. 2009;66:811-822.
32. Owen AM, McMillan KM, Laird AR, Bullmore E. N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum Brain Mapp. 2005;25:46-59.
33. Thermenos HW, Seidman LJ, Breiter H, et al. Functional magnetic resonance imaging during auditory verbal working memory in nonpsychotic relatives of persons with schizophrenia: a pilot study. Biol Psychiatry. 2004;55:490-500.
34. Seidman LJ, Thermenos HW, Koch JK, et al. Auditory verbal working memory load and thalamic activation in nonpsychotic relatives of persons with schizophrenia: an fMRI replication. Neuropsychology. 2007;21:599-610.
35. Meda SA, Bhattarai M, Morris NA, et al. An fMRI study of working memory in first-degree unaffected relatives of schizophrenia patients. Schizophr Res. 2008;104:85-95.
36. Bakshi N, Pruitt P, Radwan J, et al. Inefficiently increased anterior cingulate modulation of cortical systems during working memory in young offspring of schizophrenia patients. J Psychiatr Res. 2011;45:1067-1076.
37. Diwadkar VA, Pruitt P, Goradia D, et al. Fronto-parietal hypo-activation during working memory independent of structural abnormalities: conjoint fMRI and sMRI analyses in adolescent offspring of schizophrenia patients. Neuroimage. 2011;58:234-241.
38. de Leeuw M, Kahn RS, Zandbelt BB, Widschwendter CG, Vink M. Working memory and default mode network abnormalities in unaffected siblings of schizophrenia patients. Schizophr Res. 2013;150:555-562.
39. Seidman LJ, Thermenos HW, Poldrack RA, et al. Altered brain activation in dorsolateral prefrontal cortex in adolescents and young adults at genetic risk for schizophrenia: an fMRI study of working memory. Schizophr Res. 2006;85:58-72.
40. Karch S, Leicht G, Giegling I, et al. Inefficient neural activity in patients with schizophrenia and nonpsychotic relatives of schizophrenic patients: evidence from a working memory task. J Psychiatr Res. 2009;43:1185-1194.
41. Whitfield-Gabrieli S, Thermenos HW, Milanovic S, et al. Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc Natl Acad Sci U S A. 2009;106:1279-1284.
42. Keshavan MS, Diwadkar VA, Spencer SM, Harenski KA, Luna B, Sweeney JA. A preliminary functional magnetic resonance imaging study in offspring of schizophrenic parents. Prog Neuropsychopharmacol Biol Psychiatry. 2002;26:1143-1149.
43. Rasetti R, Mattay VS, Wiedholz LM, et al. Evidence that altered amygdala activity in schizophrenia is related to clinical state and not genetic risk. Am J Psychiatry. 2009;166:216-225.
44. Choi JS, Park JY, Jung MH, et al. Phase-specific brain change of spatial working memory processing in genetic and ultra-high risk groups of schizophrenia. Schizophr Bull. 2012;38:1189-1199.
45. Diwadkar VA, Pruitt P, Zhang A, et al. The neural correlates of performance in adolescents at risk for schizophrenia: inefficiently increased cortico-striatal responses measured with fMRI. J Psychiatr Res. 2012;46:12-21.
46. Hedges LV, Olkin L. Statistical Methods for Meta-Analysis. Orlando: Academic; 1985.
47. Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA 2000;283:2008-2012.
48. Lancaster JL, Tordesillas-Gutiérrez D, Martinez M, et al. Bias between MNI and Talairach coordinates analyzed using the ICBM-152 brain template. Hum Brain Mapp. 2007;28:1194-1205.
49. Glahn DC, Thompson PM, Blangero J. Neuroimaging endophenotypes: strategies for finding genes influencing brain structure and function. Hum Brain Mapp. 2007;28:488-501.
50. Glahn DC, Ragland JD, Abramoff A, et al. Beyond hypofrontality: a quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Hum Brain Mapp. 2005;25:60-69.
51. Radua J, Mataix-Cols D. Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. Br J Psychiatry. 2009;195:393-402.
52. Aoki Y, Cortese S, Tansella M. Neural bases of atypical emotional face processing in autism: a meta-analysis of fMRI studies. World J Biol Psychiatry. 2015;16:291-300.
53. Goghari VM. Executive functioning-related brain abnormalities associated with the genetic liability for schizophrenia: an activation likelihood estimation meta-analysis. Psychol Med. 2011;41:1239-1252.
54. Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM. The role of the right inferior frontal gyrus: inhibition and attentional control. Neuroimage. 2010;50:1313-1319.
55. Barch DM, Ceaser A. Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci. 2012;16:27-34.
56. Ragland JD, Blumenfeld RS, Ramsay IS, et al. Neural correlates of relational and item-specific encoding during working and long-term memory in schizophrenia. Neuroimage. 2012;59:1719-1726.
57. Bonner-Jackson A, Csernansky JG, Barch DM. Levels-ofprocessing effects in first-degree relatives of individuals with schizophrenia. Biol Psychiatry. 2007;61:1141-1147.
58. Cirillo MA, Seidman LJ. Verbal declarative memory dysfunction in schizophrenia: from clinical assessment to genetics and brain mechanisms. Neuropsychol Rev. 2003;13:43-77.
59. Rasetti R, Mattay VS, White MG, et al. Altered hippocampal-parahippocampal function during stimulus encoding: a potential indicator of genetic liability for schizophrenia. JAMA Psychiatry. 2014;71:236-247.
60. Brébion G, Stephan-Otto C, Huerta-Ramos E, et al. Visual encoding impairment in patients with schizophrenia: contribution of reduced working memory span, decreased processing speed, and affective symptoms. Neuropsychology. 2015;29:17-24.
61. Tan HY, Sust S, Buckholtz JW, et al. Dysfunctional prefrontal regional specialization and compensation in schizophrenia. Am J Psychiatry. 2006;163:1969-1977.
62. Tan HY, Callicott JH, Weinberger DR. Dysfunctional and compensatory prefrontal cortical systems, genes and the pathogenesis of schizophrenia. Cereb Cortex. 2007;17(suppl 1):i171-i181.
63. Bludau S, Eickhoff SB, Mohlberg H, et al. Cytoarchitecture, probability maps and functions of the human frontal pole. Neuroimage. 2014;93(Pt 2):260-275.
64. Ravizza SM, Delgado MR, Chein JM, Becker JT, Fiez JA. Functional dissociations within the inferior parietal cortex in verbal working memory. Neuroimage. 2004;22:562-573.
65. Huang S, Seidman LJ, Rossi S, Ahveninen J. Distinct cortical networks activated by auditory attention and working memory load. Neuroimage. 2013;83:1098-1108.
66. Gisselgård J, Anda LG, Brønnick K, et al. Verbal working memory deficits predict levels of auditory hallucination in first-episode psychosis. Schizophr Res. 2014;153:38-41.
67. Blackwood DH, Glabus MF, Dunan J, O'Carroll RE, Muir WJ, Ebmeier KP. Altered cerebral perfusion measured by SPECT in relatives of patients with schizophrenia. Correlations with memory and P300. Br J Psychiatry. 1999;175:357-366.
68. Seidman LJ, Faraone SV, Goldstein JM, et al. Thalamic and amygdala-hippocampal volume reductions in first-degree relatives of patients with schizophrenia: an MRI-based morphometric analysis. Biol Psychiatry. 1999;46:941-954.
69. Cooper D, Barker V, Radua J, Fusar-Poli P, Lawrie SM. Multimodal voxel-based meta-analysis of structural and functional magnetic resonance imaging studies in those at elevated genetic risk of developing schizophrenia. Psychiatry Res. 2014;221:69-77.
70. Ettinger U, Picchioni M, Landau S, et al. Magnetic resonance imaging of the thalamus and adhesio interthalamica in twins with schizophrenia. Arch Gen Psychiatry. 2007;64:401-409.
71. Haijma SV, Van Haren N, Cahn W, Koolschijn PC, Hulshoff Pol HE, Kahn RS. Brain volumes in schizophrenia: a meta-analysis in over 18 000 subjects. Schizophr Bull. 2013;39:1129-1138.
72. Anticevic A, Cole MW, Repovs G, et al. Characterizing thalamo-cortical disturbances in schizophrenia and bipolar illness. Cereb Cortex. 2014;24:3116-3130.
73. Jardri R, Pouchet A, Pins D, Thomas P. Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. Am J Psychiatry. 2011;168:73-81.