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European Archives of Psychiatry and Clinical Neuroscience

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01-09-2014 | Original Paper

Common and disease-specific dysfunctions of brain systems underlying attentional and executive control in schizophrenia and bipolar disorder

Authors: Tobias Melcher, Sarah Wolter, Stefanie Falck, Eva Wild, Florian Wild, Eva Gruber, Peter Falkai, Oliver Gruber

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 6/2014

Abstract

Schizophrenia and bipolar disorder broadly overlap in multiple areas involving clinical phenomenology, genetics, and neurobiology. Still, the investigation into specific elementary (sub-)processes of executive functioning may help to define clear points of distinction between these categorical diagnoses to validate the nosological dichotomy and, indirectly, to further elucidate their pathophysiological underpinnings. In the present behavioral study, we sought to separate common from diagnosis-specific deficits in a series of specific elementary sub-functions of executive processing in patients with schizophrenia and bipolar disorder. For our purpose, we administered a modern and multi-purpose neuropsychological task paradigm to equal-sized and matched groups of schizophrenia patients, patients with bipolar disorder, and healthy control subjects. First, schizophrenia patients compared to the bipolar group exhibited a more pronounced deficit in general measures of task performance comprising both response speed and accuracy. Additionally, bipolar patients showed increased advance task preparation, i.e., were better able to compensate for response speed deficits when longer preparation intervals were provided. Set-shifting, on the other hand, was impaired to a similar degree in both patient groups. Finally, schizophrenia patients exhibited a specific deficit in conflict processing (inhibitory control) and the shielding of task-relevant processing from distraction (i.e., attentional maintenance). The present investigation suggests that specific neuropsychological measures of elementary executive functions may represent important points of dissociation between schizophrenia and bipolar disorder, which may help to differentiate the pathophysiological underpinnings of these major psychiatric disorders. In this context, the present findings highlight the measures of inhibitory control and attentional maintenance as promising candidates.

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Allport DA, Styles EA, Hsieh S (1994) Shifting intentional set: exploring the dynamic control of tasks. In: Umilta C, Moscovitch M (eds) Attention and performance, vol XV. MIT, Cambridge MA, pp 421–452

Altshuler LL, Ventura J, van Gorp WG et al (2004) Neurocognitive function in clinically stable men with bipolar I disorder or schizophrenia and normal control subjects. Biol Psychiatry 56:560–569. doi:10.1016/j.biopsych.2004.08.002 PubMedCrossRef

Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci (Regul Ed) 8:170–177. doi:10.1016/j.tics.2004.02.010 CrossRef

Balanzá-Martínez V, Tabarés-Seisdedos R, Selva-Vera G et al (2005) Persistent cognitive dysfunctions in bipolar I disorder and schizophrenic patients: a 3-year follow-up study. Psychother Psychosom 74:113–119. doi:10.1159/000083170 PubMedCrossRef

Barbone F, McMahon AD, Davey PG, Morris AD, Reid IC, McDevitt DC et al (1998) Association of road-traffic accidents with benzodiazepine use. Lancet 352:1331–1336PubMedCrossRef

Barch DM, Ceaser A (2012) Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci (Regul Ed) 16:27–34. doi:10.1016/j.tics.2011.11.015 CrossRef

Berti S, Schröger E (2001) A comparison of auditory and visual distraction effects: behavioral and event-related indices. Brain Res Cogn Brain Res 10:265–273. doi:10.1016/S0926-6410(00)00044-6 PubMedCrossRef

Bora E, Vahip S, Akdeniz F (2008) The role and importance of cognitive symptoms in bipolar disorder. Turk Psikiyatri Derg 19:81–93PubMed

Bora E, Yucel M, Pantelis C (2009) Cognitive functioning in schizophrenia, schizoaffective disorder and affective psychoses: meta-analytic study. Br J Psychiatry 195:475–482. doi:10.1192/bjp.bp.108.055731 PubMedCrossRef

10.

Ceaser AE, Goldberg TE, Egan MF et al (2008) Set-shifting ability and schizophrenia: a marker of clinical illness or an intermediate phenotype? Biol Psychiatry 64:782–788. doi:10.1016/j.biopsych.2008.05.009 PubMedCentralPubMedCrossRef

11.

Christodoulou T, Messinis L, Papathanasopoulos P, Frangou S (2012) Dissociable and common deficits in inhibitory control in schizophrenia and bipolar disorder. Eur Arch Psychiatry Clin Neurosci 262:125–130. doi:10.1007/s00406-011-0213-7 PubMedCrossRef

12.

Clark L, Goodwin GM (2004) State- and trait-related deficits in sustained attention in bipolar disorder. Eur Arch Psychiatry Clin Neurosci 254:61–68. doi:10.1007/s00406-004-0460-y PubMedCrossRef

13.

Cole MW, Anticevic A, Repovs G, Barch D (2011) Variable global dysconnectivity and individual differences in schizophrenia. Biol Psychiatry 70:43–50. doi:10.1016/j.biopsych.2011.02.010 PubMedCentralPubMedCrossRef

14.

Cornblatt BA, Malhotra AK (2001) Impaired attention as an endophenotype for molecular genetic studies of schizophrenia. Am J Med Genet 105:11–15PubMedCrossRef

15.

Craddock N, Owen MJ (2010) The Kraepelinian dichotomy–going, going…but still not gone. BJP 196:92–95. doi:10.1192/bjp.bp.109.073429 CrossRef

16.

Derrfuss J, Brass M, Neumann J, von Cramon DY (2005) Involvement of the inferior frontal junction in cognitive control: meta-analyses of switching and Stroop studies. Hum Brain Mapp 25:22–34. doi:10.1002/hbm.20127 PubMedCrossRef

17.

Diekhof EK, Gruber O (2010) When desire collides with reason: functional interactions between anteroventral prefrontal cortex and nucleus accumbens underlie the human ability to resist impulsive desires. J Neurosci 30:1488–1493. doi:10.1523/JNEUROSCI.4690-09.2010 PubMedCrossRef

18.

Dreisbach G, Haider H (2008) That’s what task sets are for: shielding against irrelevant information. Psychol Res 72:355–361. doi:10.1007/s00426-007-0131-5 PubMedCrossRef

19.

Frangou S, Dakhil N, Landau S, Kumari V (2006) Fronto-temporal function may distinguish bipolar disorder from schizophrenia. Bipolar Disord 8:47–55. doi:10.1111/j.1399-5618.2006.00274.x PubMedCrossRef

20.

Garavan H, Ross TJ, Stein EA (1999) Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proc Natl Acad Sci USA 96:8301–8306PubMedCentralPubMedCrossRef

21.

Goschke T (2003) Voluntary action and cognitive control from a cognitive neuroscience perspective. In: Maasen S, Prinz W, Roth G (eds) Voluntary action: brains, minds and sociality. Oxford University Press, New York, NY, pp 49–85

22.

Gottesman II, Gould TD (2003) The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160:636–645PubMedCrossRef

23.

Greenzang C, Manoach DS, Goff DC, Barton JJS (2007) Task-switching in schizophrenia: active switching costs and passive carry-over effects in an antisaccade paradigm. Exp Brain Res 181:493–502. doi:10.1007/s00221-007-0946-8 PubMedCrossRef

24.

Gruber O (2011) Neuroimaging markers: their role for differential diagnosis and therapeutic decisions in personalized psychiatry. Nervenarzt 82:1404, 1406, 1408, passim. doi:10.1007/s00115-011-3347-y

25.

Gruber O, Goschke T (2004) Executive control emerging from dynamic interactions between brain systems mediating language, working memory and attentional processes. Acta Psychol (Amst) 115:105–121. doi:10.1016/j.actpsy.2003.12.003 CrossRef

26.

Gruber O, Gruber E, Falkai P (2005) Neural correlates of working memory deficits in schizophrenic patients. Ways to establish neurocognitive endophenotypes of psychiatric disorders. Radiologe 45:153–160. doi:10.1007/s00117-004-1155-0 PubMedCrossRef

27.

Gruber O, Karch S, Schlueter EK et al (2006) Neural mechanisms of advance preparation in task switching. Neuroimage 31:887–895. doi:10.1016/j.neuroimage.2005.12.043 PubMedCrossRef

28.

Gruber O, Melcher T, Diekhof EK et al (2009) Brain mechanisms associated with background monitoring of the environment for potentially significant sensory events. Brain Cogn 69:559–564. doi:10.1016/j.bandc.2008.11.008 PubMedCrossRef

29.

Gruber O, Tost H, Henseler I et al (2010) Pathological amygdala activation during working memory performance: evidence for a pathophysiological trait marker in bipolar affective disorder. Hum Brain Mapp 31:115–125. doi:10.1002/hbm.20849 PubMed

30.

Gur RE, Calkins ME, Gur RC et al (2007) The consortium on the genetics of schizophrenia: neurocognitive endophenotypes. Schizophr Bull 33:49–68. doi:10.1093/schbul/sbl055 PubMedCentralPubMedCrossRef

31.

Henseler I, Falkai P, Gruber O (2009) A systematic fMRI investigation of the brain systems subserving different working memory components in schizophrenia. Eur J Neurosci 30:693–702. doi:10.1111/j.1460-9568.2009.06850.x PubMedCrossRef

32.

Henseler I, Falkai P, Gruber O (2010) Disturbed functional connectivity within brain networks subserving domain-specific subcomponents of working memory in schizophrenia: relation to performance and clinical symptoms. J Psychiatr Res 44:364–372. doi:10.1016/j.jpsychires.2009.09.003 PubMedCrossRef

33.

Jonides J, Smith EE, Marshuetz C et al (1998) Inhibition in verbal working memory revealed by brain activation. Proc Natl Acad Sci USA 95:8410–8413PubMedCentralPubMedCrossRef

34.

Kaladjian A, Jeanningros R, Azorin J-M et al (2007) Blunted activation in right ventrolateral prefrontal cortex during motor response inhibition in schizophrenia. Schizophr Res 97:184–193. doi:10.1016/j.schres.2007.07.033 PubMedCrossRef

35.

Kaladjian A, Jeanningros R, Azorin J-M et al (2011) Impulsivity and neural correlates of response inhibition in schizophrenia. Psychol Med 41:291–299. doi:10.1017/S0033291710000796 PubMedCrossRef

36.

Kendell RE, Brockington IF (1980) The identification of disease entities and the relationship between schizophrenic and affective psychoses. Br J Psychiatry 137:324–331PubMedCrossRef

37.

Kendell R, Jablensky A (2003) Distinguishing between the validity and utility of psychiatric diagnoses. Am J Psychiatry 160:4–12. doi:10.1176/appi.ajp.160.1.4 PubMedCrossRef

38.

Kieffaber PD, Kappenman ES, Bodkins M et al (2006) Switch and maintenance of task set in schizophrenia. Schizophr Res 84:345–358. doi:10.1016/j.schres.2006.01.022 PubMedCrossRef

39.

Kleinknecht R (1975) Review of effects of diazepam on cognitive and psychomotor performance. J Nerv Ment Dis 161:399–411PubMedCrossRef

40.

Krabbendam L, Arts B, van Os J, Aleman A (2005) Cognitive functioning in patients with schizophrenia and bipolar disorder: a quantitative review. Schizophr Res 80:137–149. doi:10.1016/j.schres.2005.08.004 PubMedCrossRef

41.

Krabbendam L, O’Daly O, Morley LA et al (2009) Using the Stroop task to investigate the neural correlates of symptom change in schizophrenia. Br J Psychiatry 194:373–374. doi:10.1192/bjp.bp.108.055459 PubMedCrossRef

42.

Kurtz MM, Gerraty RT (2009) A meta-analytic investigation of neurocognitive deficits in bipolar illness: profile and effects of clinical state. Neuropsychology 23:551–562. doi:10.1037/a0016277 PubMedCentralPubMedCrossRef

43.

Langenecker SA, Saunders EFH, Kade AM et al (2010) Intermediate: cognitive phenotypes in bipolar disorder. J Affect Disord 122:285–293. doi:10.1016/j.jad.2009.08.018 PubMedCentralPubMedCrossRef

44.

Leitman DI, Wolf DH, Loughead J et al (2011) Ventrolateral prefrontal cortex and the effects of task demand context on facial affect appraisal in schizophrenia. Soc Cogn Affect Neurosci 6:66–73. doi:10.1093/scan/nsq018 PubMedCentralPubMedCrossRef

45.

Lévesque J, Eugène F, Joanette Y et al (2003) Neural circuitry underlying voluntary suppression of sadness. Biol Psychiatry 53:502–510PubMedCrossRef

46.

Lichtenstein P, Yip BH, Björk C et al (2009) Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet 373:234–239. doi:10.1016/S0140-6736(09)60072-6 PubMedCrossRef

47.

Lucki I et al (1980) Chronic use of benzodiazepines and psychomotor and cognitive test performance. Psychopharmacology 88:426–433

48.

MacDonald AW 3rd, Carter CS, Kerns JG et al (2005) Specificity of prefrontal dysfunction and context processing deficits to schizophrenia in never-medicated patients with first-episode psychosis. Am J Psychiatry 162:475–484. doi:10.1176/appi.ajp.162.3.475 PubMedCrossRef

49.

McIntosh AM, Job DE, Moorhead WJ et al (2006) Genetic liability to schizophrenia or bipolar disorder and its relationship to brain structure. Am J Med Genet B Neuropsychiatr Genet 141B:76–83. doi:10.1002/ajmg.b.30254 PubMedCrossRef

50.

Meiran N (1996) Is reading ability related to activation dumping speed? Evidence from immediate repetition priming. Mem Cognit 24:41–59PubMedCrossRef

51.

Meiran N, Chorev Z, Sapir A (2000) Component processes in task switching. Cogn Psychol 41:211–253. doi:10.1006/cogp.2000.0736 PubMedCrossRef

52.

Melcher T, Gruber O (2006) Oddball and incongruity effects during Stroop task performance: a comparative fMRI study on selective attention. Brain Res 1121:136–149. doi:10.1016/j.brainres.2006.08.120 PubMedCrossRef

53.

Melcher T, Gruber O (2009) Decomposing interference during Stroop performance into different conflict factors: an event-related fMRI study. Cortex 45:189–200. doi:10.1016/j.cortex.2007.06.004 PubMedCrossRef

54.

Melcher T, Falkai P, Gruber O (2008) Functional brain abnormalities in psychiatric disorders: neural mechanisms to detect and resolve cognitive conflict and interference. Brain Res Rev 59:96–124. doi:10.1016/j.brainresrev.2008.06.003 PubMedCrossRef

55.

Milham MP, Banich MT, Barad V (2003) Competition for priority in processing increases prefrontal cortex’s involvement in top-down control: an event-related fMRI study of the Stroop task. Brain Res Cogn Brain Res 17:212–222PubMedCrossRef

56.

Mojtabai R, Bromet EJ, Harvey PD et al (2000) Neuropsychological differences between first-admission schizophrenia and psychotic affective disorders. Am J Psychiatry 157:1453–1460PubMedCrossRef

57.

Moskvina V, Craddock N, Holmans P et al (2009) Gene-wide analyses of genome-wide association data sets: evidence for multiple common risk alleles for schizophrenia and bipolar disorder and for overlap in genetic risk. Mol Psychiatry 14:252–260. doi:10.1038/mp.2008.133 PubMedCentralPubMedCrossRef

58.

Pattanayak RD, Sagar R, Mehta M (2011) Cognitive dysfunction as a trait marker for Bipolar disorder: a critical review. J Ment Health Hum Behav 16:18–28

59.

Peralta V, Cuesta MJ (2008) Exploring the borders of the schizoaffective spectrum: a categorical and dimensional approach. J Affect Disord 108:71–86. doi:10.1016/j.jad.2007.09.009 PubMedCrossRef

60.

Ragland JD, Laird AR, Ranganath C et al (2009) Prefrontal activation deficits during episodic memory in schizophrenia. Am J Psychiatry 166:863–874. doi:10.1176/appi.ajp.2009.08091307 PubMedCentralPubMedCrossRef

61.

Rogers RD, Monsell S (1995) Costs of a predictable switch between simple cognitive tasks. J Exp Psychol Gen 124:207–231. doi:10.1037/0096-3445.124.2.207 CrossRef

62.

Snitz BE, MacDonald A 3rd, Cohen JD et al (2005) Lateral and medial hypofrontality in first-episode schizophrenia: functional activity in a medication-naive state and effects of short-term atypical antipsychotic treatment. Am J Psychiatry 162:2322–2329. doi:10.1176/appi.ajp.162.12.2322 PubMedCrossRef

63.

Snitz BE, Macdonald AW 3rd, Carter CS (2006) Cognitive deficits in unaffected first-degree relatives of schizophrenia patients: a meta-analytic review of putative endophenotypes. Schizophr Bull 32:179–194. doi:10.1093/schbul/sbi048 PubMedCentralPubMedCrossRef

64.

Stefanopoulou E, Manoharan A, Landau S et al (2009) Cognitive functioning in patients with affective disorders and schizophrenia: a meta-analysis. Int Rev Psychiatry 21:336–356. doi:10.1080/09540260902962149 PubMedCrossRef

65.

Swann AC (2009) Impulsivity in mania. Curr Psychiatry Rep 11:481–487PubMedCrossRef

66.

Swann AC, Steinberg JL, Lijffijt M, Moeller FG (2008) Impulsivity: differential relationship to depression and mania in bipolar disorder. J Affect Disord 106:241–248. doi:10.1016/j.jad.2007.07.011 PubMedCentralPubMedCrossRef

67.

Turetsky BI, Calkins ME, Light GA et al (2007) Neurophysiological endophenotypes of schizophrenia: the viability of selected candidate measures. Schizophr Bull 33:69–94. doi:10.1093/schbul/sbl060 PubMedCentralPubMedCrossRef

68.

Wylie GR, Clark EA, Butler PD, Javitt DC (2010) Schizophrenia patients show task switching deficits consistent with N-methyl-d-aspartate system dysfunction but not global executive deficits: implications for pathophysiology of executive dysfunction in schizophrenia. Schizophr Bull 36:585–594. doi:10.1093/schbul/sbn119 PubMedCentralPubMedCrossRef

69.

Zilles D, Meyer J, Schneider-Axmann T et al (2012) Genetic polymorphisms of 5-HTT and DAT but not COMT differentially affect verbal and visuospatial working memory functioning. Eur Arch Psychiatry Clin Neurosci 262:667–676. doi:10.1007/s00406-012-0312-0 PubMedCentralPubMedCrossRef

Title: Common and disease-specific dysfunctions of brain systems underlying attentional and executive control in schizophrenia and bipolar disorder
Authors: Tobias Melcher
Sarah Wolter
Stefanie Falck
Eva Wild
Florian Wild
Eva Gruber
Peter Falkai
Oliver Gruber
Publication date: 01-09-2014
Publisher: Springer Berlin Heidelberg
Published in: European Archives of Psychiatry and Clinical Neuroscience / Issue 6/2014
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI: https://doi.org/10.1007/s00406-013-0445-9

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Springer Medicine

Common and disease-specific dysfunctions of brain systems underlying attentional and executive control in schizophrenia and bipolar disorder

Abstract

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Abstract

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