Evidence for corticostriatal dysfunction during cognitive skill learning in adolescent siblings of patients with childhood-onset schizophrenia

Schizophrenia Bulletin

Volumn 40, Issue 5, 2014, Pages 1030-1039

  Wagshal, Dana ^a   Knowlton, Barbara Jean ^b   Suthana, Nanthia Ananda ^b   Cohen, Jessica Rachel ^c   Poldrack, Russel Alan ^d   Bookheimer, Susan Yost ^b   Bilder, Robert Martin ^b   Asarnow, Robert Franklin ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Cognitive skill learning; FMRI; Genetic risk; Striatal dysfunction

Indexed keywords

ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; CEREBELLUM; CHILD; CHILDHOOD ONSET SCHIZOPHRENIA; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORPUS STRIATUM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENETIC RISK; HUMAN; INFERIOR FRONTAL GYRUS; INSULA; LEARNING; NEUROIMAGING; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA; SIBLING; SUPERIOR FRONTAL GYRUS; SUPPLEMENTARY MOTOR AREA; ADOLESCENT; BRAIN MAPPING; COGNITION DISORDERS; COMPLICATION; FRONTAL LOBE; GENETICS; NEOSTRIATUM; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ADOLESCENT; AGE OF ONSET; BRAIN MAPPING; CHILD; COGNITION DISORDERS; FRONTAL LOBE; HUMANS; LEARNING; MAGNETIC RESONANCE IMAGING; NEOSTRIATUM; SCHIZOPHRENIA; SIBLINGS;

EID: 84907367872     PISSN: 05867614     EISSN: 17451701     Source Type: Journal    
DOI: 10.1093/schbul/sbt147     Document Type: Article

References (60)

1. Giménez M, Junqué C, Pérez M, et al. Basal ganglia N-acetylaspartate correlates with the performance in the procedural task 'Tower of Hanoi' of neuroleptic-naive schizophrenic patients. Neurosci Lett. 2003;347: 97-100.
2. Schröder J, Tittel A, Stockert A, Karr M. Memory deficits in subsyndromes of chronic schizophrenia. Schizophr Res. 1996;21: 19-26.
3. Purdon SE, Woodward N, Lindborg SR, Stip E. Procedural learning in schizophrenia after 6 months of double-blind treatment with olanzapine, risperidone, and haloperidol. Psychopharmacology (Berl). 2003;169: 390-397.
4. Foerde K, Poldrack RA, Khan BJ, et al. Selective corticostriatal dysfunction in schizophrenia: examination of motor and cognitive skill learning. Neuropsychology. 2008;22: 100-109.
5. Weickert TW, Goldberg TE, Egan MF, et al. Relative risk of probabilistic category learning deficits in patients with schizophrenia and their siblings. Biol Psychiatry. 2010;67: 948-955.
6. Buchanan RW, Breier A, Kirkpatrick B, et al. Structural abnormalities in deficit and nondeficit schizophrenia. Am J Psychiatry. 1993;150: 59-65.
7. Buchsbaum MS. Frontal lobes, basal ganglia, temporal lobes-three sites for schizophrenia? Schizophr Bull. 1990;16: 377-378.
8. Kleist K. Schizophrenic symptoms and cerebral pathology. J Ment Sci. 1960;106: 246-255.
9. Heindel WC, Salmon DP, Shults CW, Walicke PA, Butters N. Neuropsychological evidence for multiple implicit memory systems: a comparison of Alzheimer's, Huntington's, and Parkinson's disease patients. J Neurosci. 1989;9: 582-587.
10. Knowlton BJ, Mangels JA, Squire LR. A neostriatal habit learning system in humans. Science. 1996;273: 1399-1402.
11. Doyon J, Bellec P, Amsel R, et al. Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res. 2009;199: 61-75.
12. Peigneux P, Maquet P, Meulemans T, et al. Striatum forever, despite sequence learning variability: a random effect analysis of PET data. Hum Brain Mapp. 2000;10: 179-194.
13. Grafton ST, Hazeltine E, Ivry R. Functional mapping of sequence learning in normal humans. J Cogn Neurosci. 1995;7: 497-510.
14. Rauch SL, Whalen PJ, Savage CR, et al. Striatal recruitment during an implicit sequence learning task as measured by functional magnetic resonance imaging. Hum Brain Mapp. 1997;5: 124-132.
15. Poldrack RA, Gabrieli JD. Characterizing the neural mechanisms of skill learning and repetition priming: evidence from mirror reading. Brain. 2001;124: 67-82.
16. Schiltz C, Bodart JM, Michel C, Crommelinck M. A pet study of human skill learning: changes in brain activity related to learning an orientation discrimination task. Cortex. 2001;37: 243-265.
17. Aron AR, Shohamy D, Clark J, Myers C, Gluck MA, Poldrack RA. Human midbrain sensitivity to cognitive feedback and uncertainty during classification learning. J Neurophysiol. 2004;92: 1144-1152.
18. Moody TD, Bookheimer SY, Vanek Z, Knowlton BJ. An implicit learning task activates medial temporal lobe in patients with Parkinson's disease. Behav Neurosci. 2004;118: 438-442.
19. Knowlton BJ, Squire LR, Gluck MA. Probabilistic classification learning in amnesia. Learn Mem. 1994;1: 106-120.
20. Marsh R, Alexander GM, Packard MG, et al. Habit learning in Tourette syndrome: a translational neuroscience approach to a developmental psychopathology. Arch Gen Psychiatry. 2004;61: 1259-1268.
21. Kéri S, Juhász A, Rimanóczy A, et al. Habit learning and the genetics of the dopamine D3 receptor: evidence from patients with schizophrenia and healthy controls. Behav Neurosci. 2005;119: 687-693.
22. Horan WP, Green MF, Knowlton BJ, Wynn JK, Mintz J, Nuechterlein KH. Impaired implicit learning in schizophrenia. Neuropsychology. 2008;22: 606-617.
23. Weickert TW, Terrazas A, Bigelow LB, et al. Habit and skill learning in schizophrenia: evidence of normal striatal processing with abnormal cortical input. Learn Mem. 2002;9: 430-442.
24. Paquet F, Soucy JP, Stip E, Lévesque M, Elie A, Bédard MA. Comparison between olanzapine and haloperidol on procedural learning and the relationship with striatal D2 receptor occupancy in schizophrenia. J Neuropsychiatry Clin Neurosci. 2004;16: 47-56.
25. Kumari V, Gray JA, Honey GD, et al. Procedural learning in schizophrenia: a functional magnetic resonance imaging investigation. Schizophr Res. 2002;57: 97-107.
26. Wagshal D, Knowlton BJ, Cohen JR, et al. Deficits in probabilistic classification learning and liability for schizophrenia. Psychiatry Res. 2012;200: 167-172.
27. Asarnow RF. Childhood schizophrenia. In: Beauchaine TP, Hinshaw SP, eds. Child and Adolescent Psychopathology. 2nd ed. Hoboken, NJ: John Wiley and Sons; 2013: 685-714.
28. Asarnow RF, Nuechterlein KH, Fogelson D, et al. Schizophrenia and schizophrenia-spectrum personality disorders in the first-degree relatives of children with schizophrenia: the UCLA family study. Arch Gen Psychiatry. 2001;58: 581-588.
29. Asarnow RF. Neurocognitive impairments in schizophrenia: a piece of the epigenetic puzzle. Eur Child Adolesc Psychiatry. 1999;8(suppl 1): I5-I8.
30. Gold JM, Harvey PD. Cognitive deficits in schizophrenia. Psychiatr Clin North Am. 1993;16: 295-312.
31. Kuperberg G, Heckers S. Schizophrenia and cognitive function. Curr Opin Neurobiol. 2000;10: 205-210.
32. Riley EM, McGovern D, Mockler D, et al. Neuropsychological functioning in first-episode psychosis-evidence of specific deficits. Schizophr Res. 2000;43: 47-55.
33. Brainard DH. The Psychophysics Toolbox. Spat Vis. 1997;10: 433-436.
34. Jenkinson M, Bannister P, Brady M, Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17: 825-841.
35. Smith SM. Fast robust automated brain extraction. Hum Brain Mapp. 2002;17: 143-155.
36. Woolrich MW, Ripley BD, Brady M, Smith SM. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage. 2001;14: 1370-1386.
37. Friston KJ, Worsley KJ, Frackowiak RSJ, Mazziotta JC, Evans AC. Assessing the significance of focal activations using their spatial extent. Hum Brain Mapp. 1994;1: 214-220.
38. Shohamy D, Myers CE, Kalanithi J, Gluck MA. Basal ganglia and dopamine contributions to probabilistic category learning. Neurosci Biobehav Rev. 2008;32: 219-236.
39. Foerde K, Knowlton BJ, Poldrack RA. Modulation of competing memory systems by distraction. Proc Natl Acad Sci U S A. 2006;103: 11778-11783.
40. Poldrack RA, Clark J, Paré-Blagoev EJ, et al. Interactive memory systems in the human brain. Nature. 2001;414: 546-550.
41. Poldrack RA, Prabhakaran V, Seger CA, Gabrieli JD. Striatal activation during acquisition of a cognitive skill. Neuropsychology. 1999;13: 564-574.
42. McKiernan KA, Kaufman JN, Kucera-Thompson J, Binder JR. A parametric manipulation of factors affecting taskinduced deactivation in functional neuroimaging. J Cogn Neurosci. 2003;15: 394-408.
43. Tomasi D, Volkow ND, Wang R, et al. Dopamine transporters in striatum correlate with deactivation in the default mode network during visuospatial attention. PLoS One. 2009;4: e6102.
44. Ogg RJ, Zou P, Allen DN, Hutchins SB, Dutkiewicz RM, Mulhern RK. Neural correlates of a clinical continuous performance test. Magn Reson Imaging. 2008;26: 504-512.
45. Ungar L, Nestor PG, Niznikiewicz MA, Wible CG, Kubicki M. Color Stroop and negative priming in schizophrenia: an fMRI study. Psychiatry Res. 2010;181: 24-29.
46. Sepede G, Ferretti A, Perrucci MG, et al. Altered brain response without behavioral attention deficits in healthy siblings of schizophrenic patients: an event-related fMRI study. Neuroimage. 2010;49: 1080-1090.
47. Weissman DH, Roberts KC, Visscher KM, Woldorff MG. The neural bases of momentary lapses in attention. Nat Neurosci. 2006;9: 971-978.
48. Garrity AG, Pearlson GD, McKiernan K, Lloyd D, Kiehl KA, Calhoun VD. Aberrant "default mode" functional connectivity in schizophrenia. Am J Psychiatry. 2007;164: 450-457.
49. Zhou Y, Liang M, Tian L, et al. Functional disintegration in paranoid schizophrenia using resting-state fMRI. Schizophr Res. 2007;97: 194-205.
50. Pomarol-Clotet E, Salvador R, Sarró S, et al. Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network? Psychol Med. 2008;38: 1185-1193.
51. 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.
52. Rotarska-Jagiela A, van de Ven V, Oertel-Knöchel V, Uhlhaas PJ, Vogeley K, Linden DE. Resting-state functional network correlates of psychotic symptoms in schizophrenia. Schizophr Res. 2010;117: 21-30.
53. Ramnani N, Owen AM. Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat Rev Neurosci. 2004;5: 184-194.
54. Düzel E, Cabeza R, Picton TW, et al. Task-related and itemrelated brain processes of memory retrieval. Proc Natl Acad Sci U S A. 1999;96: 1794-1799.
55. Kapur S, Craik FI, Jones C, Brown GM, Houle S, Tulving E. Functional role of the prefrontal cortex in retrieval of memories: a PET study. Neuroreport. 1995;6: 1880-1884.
56. Devinsky O, Morrell MJ, Vogt BA. Contributions of anterior cingulate cortex to behaviour. Brain. 1995;118 (Pt 1): 279-306.
57. Bush G, Luu P, Posner MI. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci. 2000;4: 215-222.
58. Vogt BA, Nimchinsky EA, Vogt LJ, Hof PR. Human cingulate cortex: surface features, flat maps, and cytoarchitecture. J Comp Neurol. 1995;359: 490-506.
59. Mega MS, Cummings JL. The cingulate and cingulate syndromes. In: Trimble MR, Cummings JL, eds. Contemporary Behavioural Neurology. Boston, MA: Butterworth- Heinemann; 1997: 189-213.
60. Rapoport JL, Gogtay N. Childhood onset schizophrenia: support for a progressive neurodevelopmental disorder. Int J Dev Neurosci. 2011;29: 251-258.