Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-22T05:16:12.288Z Has data issue: false hasContentIssue false

Visual working memory encoding in schizophrenia and first-degree relatives: neurofunctional abnormalities and impaired consolidation

Published online by Cambridge University Press:  09 March 2018

Michael Stäblein*
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
Helena Storchak
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
Denisa Ghinea
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
Dominik Kraft
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
Christian Knöchel
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
David Prvulovic
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
Robert A. Bittner
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
Andreas Reif
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
Viola Oertel-Knöchel
Affiliation:
Department of Psychiatry, Psychosomatic Medicine and Psychotherapy, University Hospital Frankfurt, Frankfurt am Main, Germany
*
Author for correspondence: Michael Stäblein, E-mail: [email protected]

Abstract

Background

Working memory (WM) deficits in schizophrenia (SCZ) have been linked to impairments in the encoding phase that are associated with aberrant neuronal functioning. Similar abnormalities have been observed in unaffected first-degree relatives (REL) and are thus discussed as candidate endophenotypes. The process of WM consolidation – i.e. the formation of durable WM representations – is assumed to be impaired in SCZ, but no study has investigated WM consolidation and neuronal correlates of visual WM encoding in REL before.

Method

We examined whole-brain activation during the encoding phase with an event-related functional magnetic resonance imaging study design in 25 SCZ subjects, 22 REL subjects, and 25 healthy controls. Subjects performed a visual masked change detection task that assessed WM performance and consolidation.

Results

SCZ showed deficient WM performance indicating an impairment consolidation process, accompanied by broad neuronal hypoactivation, most prominently in frontal brain regions, as well as increased activity of the anterior cingulate during the encoding phase. REL showed decreased neuronal activity in the middle and medial frontal gyrus and increased activity in the precentral gyrus and insula during encoding, but no significant behavioral deficits were observed. In respect of given consolidation times, REL showed a shift from decreased frontal activity at short time intervals to increased frontal activity at longer time intervals.

Conclusions

Findings suggest WM consolidation may be slowed in REL so that the deployment of compensatory neuronal resources during encoding is needed to assure proper WM performance. This supports the view of WM-related neuronal dysfunctions as a potential endophenotypic marker.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

American Psychiatric Association (2000) Diagnostic and Statistical Manual of Mental Disorders, 4th edn., Washington DC: American Psychiatric Association.Google Scholar
Anticevic, A, Repovs, G and Barch, DM (2013). Working memory encoding and maintenance deficits in schizophrenia: neural evidence for activation and deactivation abnormalities. Schizophrenia Bulletin 39, 168178.Google Scholar
Baddeley, A (2012) Working memory: theories, models, and controversies. Annual Review of Psychology 63, 129.Google Scholar
Bittner, RA, Linden, DEJ, Roebroeck, A, Härtling, F, Rotarska-Jagiela, A, Maurer, K et al. (2015) The when and where of working memory dysfunction in early-onset schizophrenia-a functional magnetic resonance imaging study. Cerebral Cortex 25, 24942506.Google Scholar
Choi, JS, Park, JY, Jung, MH, Jang, JH, Kang, DH, Jung, WH et al. (2012) Phase-specific brain change of spatial working memory processing in genetic and ultra-high risk groups of schizophrenia. Schizophrenia Bulletin 38, 11891199.Google Scholar
Forbes, NF, Carrick, LA, McIntosh, AM and Lawrie, SM (2009) Working memory in schizophrenia: a meta-analysis. Psychological Medicine 39, 889.Google Scholar
Fuller, RL, Luck, SJ, Braun, EL, Robinson, BM, McMahon, RP and Gold, JM (2009) Impaired visual working memory consolidation in schizophrenia. Neuropsychology 23, 7180.Google Scholar
Fuller, RL, Luck, SJ, McMahon, RP and Gold, JM (2005) Working memory consolidation is abnormally slow in schizophrenia. Journal of Abnormal Psychology 114, 279290.Google Scholar
Glahn, DC, Ragland, JD, Abramoff, A, Barrett, J, Laird, AR, Bearden, CE et al. (2005) Beyond hypofrontality: a quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Human Brain Mapping 25, 6069.Google Scholar
Goghari, VM (2011) Executive functioning-related brain abnormalities associated with the genetic liability for schizophrenia: an activation likelihood estimation meta-analysis. Psychological Medicine 41, 12391252.Google Scholar
Hahn, B, Robinson, BM, Kaiser, ST, Harvey, AN, Beck, VM, Leonard, CJ et al. (2010) Failure of schizophrenia patients to overcome salient distractors during working memory encoding. Biological Psychiatry 68, 603609.Google Scholar
Hui, CLM, Li, YK, Li, AWY, Lee, EHM, Chang, WC, Chan, SKW et al. (2016). Visual working memory deterioration preceding relapse in psychosis. Psychological Medicine 46, 24352444.Google Scholar
Johnson, MR, Morris, NA, Astur, RS, Calhoun, VD, Mathalon, DH, Kiehl, KA et al. (2006) A functional magnetic resonance imaging study of working memory abnormalities in schizophrenia. Biological Psychiatry 60, 1121.Google Scholar
Jolicoeur, P and Dell'Acqua, R (1998) The demonstration of short-term consolidation. Cognitive Psychology 36, 138202.Google Scholar
Kauppi, K, Westlye, LT, Tesli, M, Bettella, F, Brandt, CL, Mattingsdal, M et al. (2015) Polygenic risk for schizophrenia associated with working memory-related prefrontal brain activation in patients with schizophrenia and healthy controls. Schizophrenia Bulletin 41, 736743.Google Scholar
Kay, SR, Fiszbein, A and Opler, LA (1987) The positive and negative syndrome scale for schizophrenia. Schizophrenia Bulletin 13, 261276.Google Scholar
Keshavan, MS, Diwadkar, VA, Spencer, SM, Harenski, KA, Luna, B and Sweeney, JA (2002) A preliminary functional magnetic resonance imaging study in offspring of schizophrenic parents. Progress in Neuro-Psychopharmacology and Biological Psychiatry 26, 11431149.Google Scholar
Lee, J and Park, S (2005) Working memory impairments in schizophrenia: a meta-analysis. Journal of Abnormal Psychology 114, 599611.Google Scholar
Lencz, T, Knowles, E, Davies, G, Guha, S, Liewald, DC, Starr, JM et al. (2014) Molecular genetic evidence for overlap between general cognitive ability and risk for schizophrenia: a report from the Cognitive Genomics consorTium (COGENT). Molecular Psychiatry 19, 168174.Google Scholar
Liu, M, Malone, SM, Vaidyanathan, U, Keller, MC, Abecasis, G, McGue, M, Iacono, WG and Vrieze, SI (2017). Psychophysiological endophenotypes to characterize mechanisms of known schizophrenia genetic loci. Psychological Medicine 47, 11161125.Google Scholar
Mainy, N, Kahane, P, Minotti, L, Hoffmann, D, Bertrand, O and Lachaux, JP (2007) Neural correlates of consolidation in working memory. Human Brain Mapping 28, 183193.Google Scholar
Mayer, JS, Kim, J and Park, S (2014) Failure to benefit from target novelty during encoding contributes to working memory deficits in schizophrenia. Cognitive Neuropsychiatry 19, 268279.Google Scholar
Mayer, JS and Park, S (2012) Working memory encoding and false memory in schizophrenia and bipolar disorder in a spatial delayed response task. Journal of Abnormal Psychology 121, 784794.Google Scholar
McCabe, DP, Roediger, HL, McDaniel, MA, Balota, DA and Hambrick, DZ (2010) The relationship between working memory capacity and executive functioning: evidence for a common executive attention construct. Neuropsychology 24, 222243.Google Scholar
Park, S and Gooding, DC (2014) Working memory impairment as an endophenotypic marker of a schizophrenia diathesis. The Authors Schizophrenia Research: Cognition 1, 127136.Google Scholar
Pessoa, L, Gutierrez, E, Bandettini, P and Ungerleider, L (2002) Neural correlates of visual working memory: fMRI amplitude predicts task performance. Neuron 35, 975987.Google Scholar
Postle, BR, Druzgal, TJ and D'Esposito, M (2003) Seeking the neural substrates of visual working memory storage. Cortex 39, 927946.Google Scholar
Repovš, G and Barch, DM (2012) Working memory related brain network connectivity in individuals with schizophrenia and their siblings. Frontiers in Human Neuroscience 6, 137.Google Scholar
Ricker, TJ and Cowan, N (2014) Differences between presentation methods in working memory procedures: a matter of working memory consolidation. Journal of Experimental Psychology. Learning, Memory, and Cognition 40, 417428.Google Scholar
Schlösser, RGM, Koch, K, Wagner, G, Nenadic, I, Roebel, M, Schachtzabel, C et al. (2008) Inefficient executive cognitive control in schizophrenia is preceded by altered functional activation during information encoding: an fMRI study. Neuropsychologia 46, 336347.Google Scholar
Silver, H, Feldman, P, Bilker, W and Gur, RC (2003) Working memory deficit as a core neuropsychological dysfunction in schizophrenia. American Journal of Psychiatry 160, 18091816.Google Scholar
Snitz, BE, MacDonald, AW and Carter, CS (2006) Cognitive deficits in unaffected first-degree relatives of schizophrenia patients: a meta-analytic review of putative endophenotypes. Schizophrenia Bulletin 32, 179194.Google Scholar
Stäblein, M, Sieprath, L, Knöchel, C, Landertinger, A, Schmied, C, Ghinea, D et al. (2016) Impaired working memory for visual motion direction in schizophrenia: absence of recency effects and association with psychopathology. Neuropsychology 30, 653663.Google Scholar
Tan, H-Y, Callicott, JH and Weinberger, DR (2009) Prefrontal cognitive systems in schizophrenia: towards human genetic brain mechanisms. Cognitive Neuropsychiatry 14, 277298.Google Scholar
Vogel, EK, Woodman, G and Luck, SJ (2006) The time course of consolidation in visual working memory. Journal of Experimental Psychology: Human Perception & Performance 32, 14361451.Google Scholar
Wittchen, H-U, Zaudig, M and Fydrich, T (1997) Strukturiertes klinisches Interview für DSM–IV: Achse I und II. Göttingen: Hogrefe.Google Scholar
Woodman, GF and Vogel, EK (2005) Fractionating working memory: consolidation and maintenance are independent processes. Psychological Science 16, 106113.Google Scholar
Zarahn, E, Aguirre, G and D'Esposito, M (1997) A trial-based experimental design for fMRI. NeuroImage 6, 122138.Google Scholar
Zhang, R, Picchioni, M, Allen, P and Toulopoulou, T (2016) Working memory in unaffected relatives of patients with schizophrenia: a meta-analysis of functional magnetic resonance imaging studies. Schizophrenia Bulletin 42, 10681077.Google Scholar
Supplementary material: PDF

Stäblein et al. supplementary material

Stäblein et al. supplementary material 1

Download Stäblein et al. supplementary material(PDF)
PDF 184.7 KB