Stable signatures of schizophrenia in the cortical-subcortical-cerebellar network using fMRI of verbal working memory

Schizophrenia Research

Volumn 151, Issue 1-3, 2013, Pages 133-140

  Matsuo, Kayako ^a   Chen, Shen Hsing Annabel ^b   Liu, Chih Min ^a,c   Liu, Chen Chung ^c   Hwang, Tzung Jeng ^a,c   Hsieh, Ming H ^c   Chien, Yi Ling ^c   Hwu, Hai Gwo ^c,d   Tseng, Wen Yih Isaac ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

Cerebellum; Cognitive dysmetria; Default mode network; Left lateralization; Schizophrenia; Verbal working memory

Indexed keywords

ADULT; ANGULAR GYRUS; ARTICLE; BRAIN FUNCTION; CEREBELLUM VERMIS; CLINICAL ARTICLE; CONTROLLED STUDY; DEFAULT MODE NETWORK; DISEASE DURATION; DYSMETRIA; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HUMAN; IMAGE ANALYSIS; IMAGE QUALITY; INFERIOR FRONTAL GYRUS; INFERIOR TEMPORAL GYRUS; MALE; MIDDLE AGED; MIDDLE FRONTAL GYRUS; MIDDLE TEMPORAL GYRUS; NUCLEAR MAGNETIC RESONANCE SCANNER; OCCIPITAL GYRUS; PONS; POSTCENTRAL GYRUS; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA; TASK PERFORMANCE; THALAMUS; VERBAL MEMORY; WORKING MEMORY; YOUNG ADULT;

CEREBELLUM; COGNITIVE DYSMETRIA; DEFAULT MODE NETWORK; LEFT LATERALIZATION; SCHIZOPHRENIA; VERBAL WORKING MEMORY;

ADULT; BRAIN MAPPING; CEREBELLUM; CEREBRAL CORTEX; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; MIDDLE AGED; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; REACTION TIME; SCHIZOPHRENIA; VERBAL LEARNING; YOUNG ADULT;

EID: 84889083913     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2013.10.028     Document Type: Article

References (73)

1. Andreasen N.C., Pierson R. The role of the cerebellum in schizophrenia. Biol. Psychiatry 2008, 64(2):81-88.
2. Andreasen N.C., O'Leary D.S., Cizadlo T., Arndt S., Rezai K., Ponto L.L., Watkins G.L., Hichwa R.D. Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic-cerebellar circuitry. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(18):9985-9990.
3. Andreasen N.C., Paradiso S., O'Leary D.S. "Cognitive dysmetria" as an integrative theory of schizophrenia: a dysfunction in cortical-subcortical-cerebellar circuitry?. Schizophr. Bull. 1998, 24(2):203-218.
4. Andreasen N.C., Nopoulos P., O'Leary D.S., Miller D.D., Wassink T., Flaum M. Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biol. Psychiatry 1999, 46(7):908-920.
5. Andreasen N.C., Calarge C.A., O'Leary D.S. Theory of mind and schizophrenia: a positron emission tomography study of medication-free patients. Schizophr. Bull. 2008, 34(4):708-719.
6. Andreasen N.C., Pressler M., Nopoulos P., Miller D., Ho B.C. Antipsychotic dose equivalents and dose-years: a standardized method for comparing exposure to different drugs. Biol. Psychiatry 2010, 67(3):255-262.
7. Angrilli A., Spironelli C., Elbert T., Crow T.J., Marano G., Stegagno L. Schizophrenia as failure of left hemispheric dominance for the phonological component of language. PLoS One 2009, 4(2):e4507.
8. Bleich-Cohen M., Hendler T., Kotler M., Strous R.D. Reduced language lateralization in first-episode schizophrenia: an fMRI index of functional asymmetry. Psychiatry Res. 2009, 171(2):82-93.
9. Broyd S.J., Demanuele C., Debener S., Helps S.K., James C.J., Sonuga-Barke E.J. Default-mode brain dysfunction in mental disorders: a systematic review. Neurosci. Biobehav. Rev. 2009, 33(3):279-296.
10. Buckner R.L., Carroll D.C. Self-projection and the brain. Trends Cogn. Sci. 2007, 11(2):49-57.
11. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 2008, 1124:1-38.
12. Callicott J.H., Mattay V.S., Verchinski B.A., Marenco S., Egan M.F., Weinberger D.R. Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. Am. J. Psychiatry 2003, 160(12):2209-2215.
13. Chen S.H., Desmond J.E. Cerebrocerebellar networks during articulatory rehearsal and verbal working memory tasks. Neuroimage 2005, 24(2):332-338.
14. Chen S.H., Desmond J.E. Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task. Neuropsychologia 2005, 43(9):1227-1237.
15. Conklin H.M., Curtis C.E., Katsanis J., Iacono W.G. Verbal working memory impairment in schizophrenia patients and their first-degree relatives: evidence from the digit span task. Am. J. Psychiatry 2000, 157(2):275-277.
16. Crow T.J. Schizophrenia as failure of hemispheric dominance for language. Trends Neurosci. 1997, 20(8):339-343.
17. D'Angelo E., Casali S. Seeking a unified framework for cerebellar function and dysfunction: from circuit operations to cognition. Front. Neural Circ. 2012, 6:116.
18. Desmond J.E., Gabrieli J.D., Wagner A.D., Ginier B.L., Glover G.H. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J. Neurosci. 1997, 17(24):9675-9685.
19. E K.H., Chen S.H., Ho M.H., Desmond J.E. A meta-analysis of cerebellar contributions to higher cognition from PET and fMRI studies. Hum Brain Mapp 2013, (in press). 10.1002/hbm.22194.
20. Elsabagh S., Premkumar P., Anilkumar A.P., Kumari V. A longer duration of schizophrenic illness has sex-specific associations within the working memory neural network in schizophrenia. Behav. Brain Res. 2009, 201(1):41-47.
21. Esposito F., Aragri A., Latorre V., Popolizio T., Scarabino T., Cirillo S., Marciano E., Tedeschi G., Di Salle F. Does the default-mode functional connectivity of the brain correlate with working-memory performances?. Arch. Ital. Biol. 2009, 147(1-2):11-20.
22. Goldman-Rakic P.S. Working memory dysfunction in schizophrenia. J. Neuropsychiatry Clin. Neurosci. 1994, 6(4):348-357.
23. Guerrero-Pedraza A., McKenna P.J., Gomar J.J., Sarro S., Salvador R., Amann B., Carrion M.I., Landin-Romero R., Blanch J., Pomarol-Clotet E. First-episode psychosis is characterized by failure of deactivation but not by hypo- or hyperfrontality. Psychol. Med. 2012, 42(1):73-84.
24. Gur R.E., Resnick S.M., Gur R.C. Laterality and frontality of cerebral blood flow and metabolism in schizophrenia: relationship to symptom specificity. Psychiatry Res. 1989, 27(3):325-334.
25. Henseler I., Falkai P., Gruber O. A systematic fMRI investigation of the brain systems subserving different working memory components in schizophrenia. Eur. J. Neurosci. 2009, 30(4):693-702.
26. Honey G.D., Fletcher P.C. Investigating principles of human brain function underlying working memory: what insights from schizophrenia?. Neuroscience 2006, 139(1):59-71.
27. Honey G.D., Pomarol-Clotet E., Corlett P.R., Honey R.A., McKenna P.J., Bullmore E.T., Fletcher P.C. Functional dysconnectivity in schizophrenia associated with attentional modulation of motor function. Brain 2005, 128(Pt 11):2597-2611.
28. Ivry R.B. The representation of temporal information in perception and motor control. Curr. Opin. Neurobiol. 1996, 6(6):851-857.
29. Justus T., Ravizza S.M., Fiez J.A., Ivry R.B. Reduced phonological similarity effects in patients with damage to the cerebellum. Brain Lang. 2005, 95(2):304-318.
30. Kay S.R., Fiszbein A., Opler L.A. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987, 13(2):261-276.
31. Krienen F.M., Buckner R.L. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb. Cortex 2009, 19(10):2485-2497.
32. Lancaster J.L., Rainey L.H., Summerlin J.L., Freitas C.S., Fox P.T., Evans A.C., Toga A.W., Mazziotta J.C. Automated labeling of the human brain: a preliminary report on the development and evaluation of a forward-transform method. Hum. Brain Mapp. 1997, 5(4):238-242.
33. Lancaster J.L., Woldorff M.G., Parsons L.M., Liotti M., Freitas C.S., Rainey L., Kochunov P.V., Nickerson D., Mikiten S.A., Fox P.T. Automated Talairach atlas labels for functional brain mapping. Hum. Brain Mapp. 2000, 10(3):120-131.
34. Lee J., Park S. Working memory impairments in schizophrenia: a meta-analysis. J. Abnorm. Psychol. 2005, 114(4):599-611.
35. Lieberman M.D., Cunningham W.A. Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc. Cogn. Affect. Neurosci. 2009, 4(4):423-428.
36. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19(3):1233-1239.
37. Manoach D.S. Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophr. Res. 2003, 60(2-3):285-298.
38. Marvel C.L., Desmond J.E. Functional topography of the cerebellum in verbal working memory. Neuropsychol. Rev. 2010, 20(3):271-279.
39. Matsuo K., Chen S.H., Tseng W.Y. AveLI: a robust lateralization index in functional magnetic resonance imaging using unbiased threshold-free computation. J. Neurosci. Methods 2012, 205(1):119-129.
40. Mitchell R.L., Crow T.J. Right hemisphere language functions and schizophrenia: the forgotten hemisphere?. Brain 2005, 128(Pt 5):963-978.
41. Mouchet-Mages S., Rodrigo S., Cachia A., Mouaffak F., Olie J.P., Meder J.F., Oppenheim C., Krebs M.O. Correlations of cerebello-thalamo-prefrontal structure and neurological soft signs in patients with first-episode psychosis. Acta Psychiatr. Scand. 2011, 123(6):451-458.
42. Nixon P., Lazarova J., Hodinott-Hill I., Gough P., Passingham R. The inferior frontal gyrus and phonological processing: an investigation using rTMS. J. Cogn. Neurosci. 2004, 16(2):289-300.
43. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 1971, 9:97-113.
44. Ongur D., Lundy M., Greenhouse I., Shinn A.K., Menon V., Cohen B.M., Renshaw P.F. Default mode network abnormalities in bipolar disorder and schizophrenia. Psychiatry Res. 2010, 183(1):59-68.
45. Park I.H., Kim J.J., Chun J., Jung Y.C., Seok J.H., Park H.J., Lee J.D. Medial prefrontal default-mode hypoactivity affecting trait physical anhedonia in schizophrenia. Psychiatry Res. 2009, 171(3):155-165.
46. Passamonti L., Novellino F., Cerasa A., Chiriaco C., Rocca F., Matina M.S., Fera F., Quattrone A. Altered cortical-cerebellar circuits during verbal working memory in essential tremor. Brain 2011, 134(Pt 8):2274-2286.
47. Pomarol-Clotet E., Salvador R., Sarró S., Gomar J., Vila F., Martínez A., Guerrero A., Ortiz-Gil J., Sans-Sansa B., Capdevila A., Cebamanos J.M., McKenna P.J. Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network?. Psychol. Med. 2008, 38(8):1185-1193.
48. Pomarol-Clotet E., Canales-Rodríguez E.J., Salvador R., Sarró S., Gomar J.J., Vila F., Ortiz-Gil J., Iturria-Medina Y., Capdevila A., McKenna P.J. Medial prefrontal cortex pathology in schizophrenia as revealed by convergent findings from multimodal imaging. Mol. Psychiatry 2010, 15(8):823-830.
49. Potkin S.G., Turner J.A., Brown G.G., McCarthy G., Greve D.N., Glover G.H., Manoach D.S., Belger A., Diaz M., Wible C.G., Ford J.M., Mathalon D.H., Gollub R., Lauriello J., O'Leary D., van Erp T.G., Toga A.W., Preda A., Lim K.O. Working memory and DLPFC inefficiency in schizophrenia: the FBIRN study. Schizophr. Bull. 2009, 35(1):19-31.
50. Premkumar P., Fannon D., Kuipers E., Cooke M.A., Simmons A., Kumari V. Association between a longer duration of illness, age and lower frontal lobe grey matter volume in schizophrenia. Behav. Brain Res. 2008, 193(1):132-139.
51. Price C.J., Veltman D.J., Ashburner J., Josephs O., Friston K.J. The critical relationship between the timing of stimulus presentation and data acquisition in blocked designs with fMRI. NeuroImage 1999, 10:36-44.
52. Reichenberg A., Harvey P.D. Neuropsychological impairments in schizophrenia: Integration of performance-based and brain imaging findings. Psychol. Bull. 2007, 133(5):833-858.
53. Roy M., Grondin S., Roy M.A. Time perception disorders are related to working memory impairment in schizophrenia. Psychiatry Res. 2012, 200(2-3):159-166.
54. Rusch N., Spoletini I., Wilke M., Bria P., Di Paola M., Di Iulio F., Martinotti G., Caltagirone C., Spalletta G. Prefrontal-thalamic-cerebellar gray matter networks and executive functioning in schizophrenia. Schizophr. Res. 2007, 93(1-3):79-89.
55. Salmi J., Pallesen K.J., Neuvonen T., Brattico E., Korvenoja A., Salonen O., Carlson S. Cognitive and motor loops of the human cerebro-cerebellar system. J. Cogn. Neurosci. 2010, 22(11):2663-2676.
56. Schmahmann J.D. Dysmetria of thought: clinical consequences of cerebellar dysfunction on cognition and affect. Trends Cogn. Sci. 1998, 2(9):362-371.
57. Schmahmann J.D. The role of the cerebellum in cognition and emotion: personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol. Rev. 2010, 20(3):236-260.
58. Sommer I.E., Ramsey N.F., Kahn R.S. Language lateralization in schizophrenia, an fMRI study. Schizophr. Res. 2001, 52(1-2):57-67.
59. Stip E. From intrapsychic ataxia to cognitive dysmetria: from Stransky to Andreasen. Can. J. Psychiatry 1997, 42(7):777.
60. Stoodley C.J., Schmahmann J.D. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 2010, 46(7):831-844.
61. Stoodley C.J., Valera E.M., Schmahmann J.D. Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. Neuroimage 2012, 59(2):1560-1570.
62. Strick P.L., Dum R.P., Fiez J.A. Cerebellum and nonmotor function. Annu. Rev. Neurosci. 2009, 32:413-434.
63. Tan H.Y., Choo W.C., Fones C.S., Chee M.W. fMRI study of maintenance and manipulation processes within working memory in first-episode schizophrenia. Am. J. Psychiatry 2005, 162(10):1849-1858.
64. Tanskanen P., Ridler K., Murray G.K., Haapea M., Veijola J.M., Jaaskelainen E., Miettunen J., Jones P.B., Bullmore E.T., Isohanni M.K. Morphometric brain abnormalities in schizophrenia in a population-based sample: relationship to duration of illness. Schizophr. Bull. 2010, 36(4):766-777.
65. Thormodsen R., Jensen J., Holmen A., Juuhl-Langseth M., Emblem K.E., Andreassen O.A., Rund B.R. Prefrontal hyperactivation during a working memory task in early-onset schizophrenia spectrum disorders: an fMRI study. Psychiatry Res. 2011, 194(3):257-262.
66. Triarhou L.C. Erwin Stransky (1877-1962). J. Neurol. 2012, 259(9):2012-2013.
67. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15(1):273-289.
68. Van Hecke J., Gladwin T.E., Coremans J., Destoop M., Hulstijn W., Sabbe B. Towards a solution for performance related confounds: frontal, striatal and parietal activation during a continuous spatiotemporal working memory manipulation task. Brain Imaging Behav 2012, 7(1):85-90.
69. Varambally S., Venkatasubramanian G., Thirthalli J., Janakiramaiah N., Gangadhar B.N. Cerebellar and other neurological soft signs in antipsychotic-naive schizophrenia. Acta Psychiatr. Scand. 2006, 114(5):352-356.
70. Waters F., Jablensky A. Time discrimination deficits in schizophrenia patients with first-rank (passivity) symptoms. Psychiatry Res. 2009, 167(1-2):12-20.
71. Whitfield-Gabrieli S., Thermenos H.W., Milanovic S., Tsuang M.T., Faraone S.V., McCarley R.W., Shenton M.E., Green A.I., Nieto-Castanon A., LaViolette P., Wojcik J., Gabrieli J.D., Seidman L.J. 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(4):1279-1284.
72. Wiser A.K., Andreasen N.C., O'Leary D.S., Watkins G.L., Boles Ponto L.L., Hichwa R.D. Dysfunctional cortico-cerebellar circuits cause 'cognitive dysmetria' in schizophrenia. Neuroreport 1998, 9(8):1895-1899.
73. Zatorre R.J., Belin P., Penhune V.B. Structure and function of auditory cortex: music and speech. Trends Cogn. Sci. 2002, 6(1):37-46.