Impaired activation in cognitive control regions predicts reversal learning in schizophrenia

Schizophrenia Bulletin

Volumn 42, Issue 2, 2016, Pages 484-493

  Culbreth, Adam J ^a   Gold, James M ^b   Cools, Roshan ^c,d   Barch, Deanna M ^a,e  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cognitive control; FMRI; Negative symptoms; Reinforcement learning; Reversal learning; Reward processing; Schizophrenia

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BOLD SIGNAL; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DECISION MAKING; DISEASE SEVERITY; EXECUTIVE FUNCTION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LEARNING; MAJOR CLINICAL STUDY; MALE; NEGATIVE SYNDROME; PRIORITY JOURNAL; REINFORCEMENT; REWARD; SCHIZOPHRENIA; STIMULUS RESPONSE; TASK PERFORMANCE; BRAIN CORTEX; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADULT; CEREBRAL CORTEX; CORPUS STRIATUM; EXECUTIVE FUNCTION; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; REVERSAL LEARNING; SCHIZOPHRENIA;

EID: 84964849051     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbv075     Document Type: Article

References (59)

1. Kéri S, Kelemen O, Szekeres G, et al. Schizophrenics know more than they can tell: probabilistic classification learning in schizophrenia. Psychol Med. 2000;30:149-155.
2. Bleuler E. Dementia Praecox or the Group of Schizophrenias. Zinkin J, Trans. New York, NY: International UniversitiesPress; 1950.
3. Kraepelin E. Dementia Praecox and Paraphrenia. Huntington, NY: Krieger Publishing Company; 1971.
4. Gold JM, Waltz JA, Prentice KJ, Morris SE, Heerey EA. Reward processing in schizophrenia: A deficit in the representation of value. Schizophr Bull. 2008;34:835-847.
5. Cools R, Clark L, Owen AM, Robbins TW. Defining the neural mechanisms of probabilistic reversal learning using eventrelated functional magnetic resonance imaging. J Neurosci. 2002;22:4563-4567.
6. Waltz JA, Gold JM. Probabilistic reversal learning impairments in schizophrenia: further evidence of orbitofrontal dysfunction. Schizophr Res. 2007;93:296-303.
7. Schlagenhauf F, Huys QJ, Deserno L, et al. Striatal dysfunction during reversal learning in unmedicated schizophrenia patients. Neuroimage. 2014;89:171-180.
8. Juckel G, Schlagenhauf F, Koslowski M, et al. Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology (Berl). 2006;187:222-228.
9. Juckel G, Schlagenhauf F, Koslowski M, et al. Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage. 2006;29:409-416.
10. Gradin VB, Kumar P, Waiter G, et al. Expected value and prediction error abnormalities in depression and schizophrenia. Brain. 2011:059.
11. Koch K, Schachtzabel C, Wagner G, et al. Altered activation in association with reward-related trial- And-error learning in patients with schizophrenia. Neuroimage. 2010;50:223-232.
12. Murray G, Corlett P, Clark L, et al. Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry. 2007;13:267-276.
13. Schlagenhauf F, Sterzer P, Schmack K, et al. Reward feedback alterations in unmedicated schizophrenia patients: relevance for delusions. Biol Psychiatry. 2009;65:1032-1039.
14. Dowd EC, Barch DM. Pavlovian reward prediction and receipt in schizophrenia: relationship to anhedonia. PLoS One. 2012;7:e35622.
15. Simon JJ, Biller A, Walther S, et al. Neural correlates of reward processing in schizophrenia-relationship to apathy and depression. Schizophr Res. 2010;118:154-161.
16. Waltz JA, Schweitzer JB, Ross TJ, et al. Abnormal responses to monetary outcomes in cortex, but not in the basal ganglia, in schizophrenia. Neuropsychopharmacology. 2010;35:2427-2439.
17. Waltz JA, Kasanova Z, Ross TJ, et al. The roles of reward, default, and executive control networks in set-shifting impairments in schizophrenia. PloS One. 2013;8:e57257.
18. Linke J, Kirsch P, King AV, et al. Motivational orientation modulates the neural response to reward. Neuroimage. 2010;49:2618-2625.
19. Cole MW, Schneider W. The cognitive control network: Integrated cortical regions with dissociable functions. Neuroimage. 2007;37:343-360.
20. Kringelbach ML, Rolls ET. Neural correlates of rapid reversal learning in a simple model of human social interaction. Neuroimage. 2003;20:1371-1383.
21. Crone EA, Wendelken C, Donohue SE, Bunge SA. Neural evidence for dissociable components of task-switching. Cereb Cortex. 2006;16:475-486.
22. Rüsch N, Spoletini I, Wilke M, et al. Prefrontal- Thalamic- cerebellar gray matter networks and executive functioning in schizophrenia. Schizophr Res. 2007;93:79-89.
23. Selemon L, Rajkowska G. Cellular pathology in the dorsolateral prefrontal cortex distinguishes schizophrenia from bipolar disorder. Curr Mol Med. 2003;3:427-436.
24. Benes FM. Emerging principles of altered neural circuitry in schizophrenia. Brain Res Brain Res Rev. 2000;31:251-269.
25. Yildiz M, Borgwardt SJ, Berger GE. Parietal lobes in schizophrenia: do they matter? Schizophr Res Treatment. 2011;2011:581686.
26. Barch DM, Csernansky JG, Conturo T, Snyder AZ. Working and long- Term memory deficits in schizophrenia: is there a common prefrontal mechanism? J Abnorm Psychol. 2002;111:478.
27. 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.
28. Semkovska M, Bédard M-A, Godbout L, Limoge F, Stip E. Assessment of executive dysfunction during activities of daily living in schizophrenia. Schizophr Res. 2004;69:289-300.
29. Kerns JG, Nuechterlein KH, Braver TS, Barch DM. Executive functioning component mechanisms and schizophrenia. Biol Psychiatry. 2008;64:26-33.
30. Morris SE, Heerey EA, Gold JM, Holroyd CB. Learningrelated changes in brain activity following errors and performance feedback in schizophrenia. Schizophr Res. 2008;99:274-285.
31. Paulus MP, Frank L, Brown GG, Braff DL. Schizophrenia subjects show intact success-related neural activation but impaired uncertainty processing during decision-making. Neuropsychopharmacology. 2003;28:795-806.
32. Paulus MP, Hozack NE, Zauscher BE, et al. Parietal dysfunction is associated with increased outcome-related decision-making in schizophrenia patients. Biol Psychiatry. 2002;51:995-1004.
33. Strauss GP, Waltz JA, Gold JM. A review of reward processing and motivational impairment in schizophrenia. Schizophr Bull. 2014;40:S107-S116.
34. First MB, Spitzer RL, Gibbon M, Williams JB. Structured Clinical Interview for DSM-IV-TR Axis I Disorders-Patient Edition (SCID-I/p. 2/2001 Revision). New York: Biometrics Research Department, New York State Psychiatric Institute; 2001.
35. Andreasen NC. Scale for the Assessment of Positive Symptoms:(SAPS). Iowa City: University of Iowa; 1984.
36. Andreasen NC. Scale for the Assessment of Negative Symptoms. Iowa City: University of Iowa; 1983.
37. Kirkpatrick B, Strauss GP, Nguyen L, et al. The brief negative symptom scale: psychometric properties. Schizophr Bull. 2011;37:300-305.
38. Chapman LJ, Chapman JP, Raulin ML. Scales for physical and social anhedonia. J Abnorm Psychol. 1976;85:374.
39. Chapman LJ, Chapman JP, Raulin ML. Body-image aberration in schizophrenia. J Abnorm Psychol 1978;87:399.
40. Gard DE, Kring AM, Gard MG, Horan WP, Green MF. Anhedonia in schizophrenia: distinctions between anticipatory and consummatory pleasure. Schizophr Res. 2007;93:253-260.
41. Snaith R, Hamilton M, Morley S, Humayan A, Hargreaves D, Trigwell P. A scale for the assessment of hedonic tone the Snaith-Hamilton Pleasure Scale. Br J Psychiatry. 1995;167:99-103.
42. Starkstein SE, Mayberg HS, Preziosi TJ, Andrezejewski P, Leiguarda R, Robinson RG. Reliability, validity, and clinical correlates of apathy in Parkinson's disease. J Neuropsychiatry Clin Neurosci. 1992;4:134-139.
43. Schneider LC, Struening EL. SLOF: A behavioral rating scale for assessing the mentally ill. Soc Work Res Abstr. 1983;19:9-21.
44. Friston K, Jezzard P, Turner R. Analysis of functional MRI time-series. Hum Brain Mapp. 1994;1:153-171.
45. Snyder A. Difference image versus ratio image error function forms in PET-PET realignment. In: Myers R, Cunningham V, Bailey D, Jones T, eds. Quantification of Brain Function Using PET. San Diego, CA: Academic Press; 1996:131-137.
46. Woods RP, Cherry SR, Mazziotta JC. Rapid automated algorithm for aligning and reslicing PET images. J Comput Assist Tomogr 1992;16:620-633.
47. Talairach J, Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain. 3-Dimensional Proportional System: An Approach to Cerebral Imaging. New York: Thieme Medical Publishers; 1988.
48. Ollinger J, Shulman GL, Corbetta M. Separating processes within a trial in event-related functional MRI: I. The method. Neuroimage. 2001;13:210-217.
49. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med. 1995;33:636-647.
50. McAvoy M, Ollinger J, Buckner R. Cluster size thresholds for assessment of significant activation in fMRI. Neuroimage. 2001;13:198.
51. Hayes AF. PROCESS: A Versatile Computational Tool for Observed Variable Mediation, Moderation, and Conditional Process Modeling [White paper]. 2012. http://www.afhayes.com/public/process2012.pdf.
52. Gardner DM, Murphy AL, O'Donnell H, Centorrino F, Baldessarini RJ. International consensus study of antipsychotic dosing. Psychopharmacology. 2014;12:235-243.
53. Egner T, Hirsch J. The neural correlates and functional integration of cognitive control in a Stroop task. Neuroimage. 2005;24:539-547.
54. O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science. 2004;304:452-454.
55. Collins AGE, Brown JK, Gold JM, Waltz JA, Frank MJ. Working memory contributions to reinforcement learning impairments in schizophrenia. J Neurosci. 2014;34:13747-13756.
56. Braver TS, Krug MK, Chiew KS, et al. Mechanisms of motivation- cognition interaction: challenges and opportunities. Cogn Affect Behav Neurosci. 2014;14:443-472.
57. Kinnison J, Padmala S, Choi J-M, Pessoa L. Network analysis reveals increased integration during emotional and motivational processing. J Neurosci. 2012;32.:8361-8372.
58. Barch DM, Ceaser A. Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci. 2012;16:27-34.
59. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol. 1995:289-300.