Psychiatry Research: Neuroimaging
Volume 174, Issue 1 , Pages 47-56 , 30 October 2009

Aberrant high-frequency desynchronization of cerebellar cortices in early-onset psychosis

  • Tony W. Wilson

      Affiliations

    • The MEG Center, Department of Neurological Sciences, University of Nebraska Medical Center, Omaha, NE, USA
    • Neuromagnetic Imaging Center, Department of Psychiatry, University of Colorado, Denver School of Medicine, Denver, CO, USA
    • Corresponding Author InformationCorresponding author. The MEG Center, Department of Neurological Sciences, University of Nebraska Medical Center, 982045 Nebraska Medical Center, Omaha, NE 68198-2045, USA. Tel.: +1 402 552 6431; fax: +1 402 559 5747.
    • ,
  • Erin Slason

      Affiliations

    • Neuromagnetic Imaging Center, Department of Psychiatry, University of Colorado, Denver School of Medicine, Denver, CO, USA
    • ,
  • Olivia O. Hernandez

      Affiliations

    • Neuromagnetic Imaging Center, Department of Psychiatry, University of Colorado, Denver School of Medicine, Denver, CO, USA
    • ,
  • Ryan Asherin

      Affiliations

    • Neuromagnetic Imaging Center, Department of Psychiatry, University of Colorado, Denver School of Medicine, Denver, CO, USA
    • ,
  • Martin L. Reite

      Affiliations

    • Neuromagnetic Imaging Center, Department of Psychiatry, University of Colorado, Denver School of Medicine, Denver, CO, USA
    • ,
  • Peter D. Teale

      Affiliations

    • Neuromagnetic Imaging Center, Department of Psychiatry, University of Colorado, Denver School of Medicine, Denver, CO, USA
    • ,
  • Donald C. Rojas

      Affiliations

    • Neuromagnetic Imaging Center, Department of Psychiatry, University of Colorado, Denver School of Medicine, Denver, CO, USA

Received 17 April 2008 ,Revised 19 February 2009 ,Accepted 16 March 2009.

References 

  1. Adler LE, Pachtman E, Franks RD, Pecevich M, Waldo MC, Freedman R. Neuropsychological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. Biological Psychiatry. 1982;17:639–654
  2. Altshuler LL, Ventura J, van Gorp WG, Green MF, Theberge DC, Mintz J. Neurocognitive function in clinically stable men with bipolar I disorder or schizophrenia and normal control subjects. Biological Psychiatry. 2004;56:560–569
  3. Andreasen NC. Linking mind and brain in the study of mental illness: a project for a scientific psychopathology. Science. 1997;275:1586–1593
  4. Andreasen NC. A unitary model of schizophrenia: Bleuler's “fragmented phrene” as schizencephaly. Archives of General Psychiatry. 1998;56:781–787
  5. Andreasen NC, O'Leary DS, Cizadlo T, Arndt S, Rezai K, Ponto LL, et al. Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal–thalamic–cerebellar circuitry. Proceedings of the National Academy of Sciences of the United States of America. 1996;93:9985–9990
  6. Andreasen NC, Paradiso S, O'Leary DS. “Cognitive dysmetria” as an integrative theory of schizophrenia: a dysfunction in cortical–subcortical–cerebellar circuitry?. Schizophrenia Bulletin. 1998;24:203–218
  7. Andreasen NC, Nopoulos P, O'Leary DS, Miller DD, Wassink T, Flaum M. Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biological Psychiatry. 1999;46:908–920
  8. Annett M. Left, Right, Hand and Brain: The Right Shift Theory. Hillsdale, NJ: Lawrence Erlbaum Associates; 1985;
  9. Barnes GR, Hillebrand A. Statistical flattening of MEG beamformer images. Human Brain Mapping. 2003;18:1–12
  10. Barnes GR, Hillebrand A, Fawcett IP, Singh KD. Realistic spatial sampling for MEG beamformer images. Human Brain Mapping. 2004;23:120–127
  11. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JRP, et al. Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proceedings of the National Academy of Sciences of the United States of America. 2002;99:13222–13227
  12. Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nature Reviews Neuroscience. 2007;8:45–56
  13. Blakemore SJ. Deluding the motor system. Consciousness and Cognition. 2003;12:647–655
  14. Blakemore SJ, Frith C. Self-awareness and action. Current Opinion in Neurobiology. 2003;13:219–224
  15. Bombin I, Arango C, Buchanan RW. Significance and meaning of neurological signs in schizophrenia: two decades later. Schizophrenia Bulletin. 2005;31:962–977(Review)
  16. Boroojerdi B, Topper R, Foltys H, Meincke U. Transcallosal inhibition and motor conduction studies in patients with schizophrenia using transcranial magnetic stimulation. British Journal of Psychiatry. 1999;175:375–379
  17. Bottmer C, Bachmann S, Pantel J, Essig M, Amann M, Schad LR, et al. Reduced cerebellar volume and neurological soft signs in first-episode schizophrenia. Psychiatry Research: Neuroimaging. 2005;140:239–250
  18. Bradshaw JL. Developmental Disorders of the Frontostriatal System: Neuropsychological, Neuropsychiatric, and Evolutionary Perspectives. Hove, East Sussex: Psychology Press; 2001;
  19. Bragin A, Jando G, Nadasdy Z, Hetke J, Wise K, Buzsaki G. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. Journal of Neuroscience. 1995;15:47–60
  20. Chen R. Studies of human motor neurophysiology with transcranial magnetic stimulation. Muscle & Nerve. 2000;9:S26–S32
  21. Cheyne D, Gaetz W, Garnero L, Lachaux JP, Ducorps A, Schwartz D, et al. Neuromagnetic imaging of cortical oscillations accompanying tactile stimulation. Cognitive Brain Research. 2003;17:599–608
  22. Daskalakis ZJ, Christensen BK, Chen R, Fitzgerald PB, Zipursky RB, Kapur S. Evidence for impaired cortical inhibition in schizophrenia using transcranial magnetic stimulation. Archives of General Psychiatry. 2002;59:347–354
  23. Daskalakis ZJ, Christensen BK, Fitzgerald PB, Fountain SI, Chen R. Reduced cerebellar inhibition in schizophrenia: a preliminary study. American Journal of Psychiatry. 2005;162:1203–1205
  24. Davey NJ, Puri BK, Lewis HS, Lewis SW, Ellaway PH. Effects of antipsychotic medication on electromyographic responses to transcranial magnetic stimulation of the motor cortex in schizophrenia. Journal of Neurology, Neurosurgery, and Psychiatry. 1997;63:468–473
  25. Del Arco A, Mora F. Effects of endogenous glutamate on extracellular concentrations of GABA, dopamine, and dopamine metabolites in the prefrontal cortex of the freely moving rat: involvement of NMDA and AMPA/KA receptors. Neurochemical Research. 1999;24:1027–1035
  26. Druschky K, Kaltenhauser M, Hummel C, Druschky A, Huk WJ, Neundorfer B, et al. Somatosensory evoked magnetic fields following passive movement compared with tactile stimulation of the index finger. Experimental Brain Research. 2003;148:186–195
  27. Fitzgerald PB, Brown TL, Daskalakis ZJ, Kulkarni J. A transcranial magnetic stimulation study of inhibitory deficits in the motor cortex in patients with schizophrenia. Psychiatry Research: Neuroimaging. 2002;114:11–22
  28. Fitzgerald PB, Brown TL, Daskalakis ZJ, deCastella A, Kulkarni J. A study of transcallosal inhibition in schizophrenia using transcranial magnetic stimulation. Schizophrenia Research. 2002;56:199–209
  29. Freedman R. Schizophrenia. New England Journal of Medicine. 2003;349:1738–1749(Review)
  30. Freedman R, Adler LE, Myles-Worsley M, Nagamoto HT, Miller C, Kisley M, et al. Inhibitory gating of an evoked response to repeated auditory stimuli in schizophrenia and normal subjects. Human recordings, computer simulation, and an animal model. Archives of General Psychiatry. 1996;53:1114–1121
  31. Fries P, Nikolic D, Singer W. The gamma cycle. Trends in Neuroscience. 2007;30:309–316
  32. Friston KJ. The disconnection hypothesis. Schizophrenia Research. 1998;30:115–125
  33. Friston KJ, Frith CD. Schizophrenia: a disconnection syndrome. Clinical Neuroscience. 1995;3:89–97
  34. Gaetz WC, Cheyne DO. Localization of sensorimotor cortical rhythms induced by tactile stimulation using spatially filtered MEG. Neuroimage. 2006;30:899–908
  35. Gray JA. Integrating schizophrenia. Schizophrenia Bulletin. 1998;24:249–266
  36. Gross J, Kujala J, Hamalainen M, Timmermann L, Schnitzler A, Salmelin R. Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proceedings of the National Academy of Sciences of the United States of America. 2001;98:694–699
  37. Gross J, Timmermann L, Kujala J, Salmelin R, Schnitzler A. Properties of MEG tomographic maps obtained with spatial filtering. Neuroimage. 2003;19:1329–1336
  38. Grothe B, Klump BM. Temporal processing in sensory systems. Current Opinion in Neurobiology. 2000;10:467–473
  39. Hari R, Forss N. Magnetoencephalography in the study of human somatosensory cortical processing. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 1999;354:1145–1154
  40. Hemsley DR. Schizophrenia: a cognitive model and its implications for psychological intervention. Behavior Modification. 1996;20:139–169
  41. Hillebrand A, Singh KD, Holliday IE, Furlong PL, Barnes GR. A new approach to neuroimaging with magnetoencephalography. Human Brain Mapping. 2005;25:199–211
  42. Hoechstetter K, Rupp A, Stancak A, Meinck HM, Stippich C, Berg P, et al. Interaction of tactile input in the human primary and secondary somatosensory cortex: a magnetoencephalographic study. Neuroimage. 2001;14:759–767
  43. Hoechstetter K, Bornfleth H, Weckesser D, Ille N, Berg P, Scherg M. BESA source coherence: a new method to study cortical oscillatory coupling. Brain Topography. 2004;16:233–238
  44. Hollingshead AB. Four factor index of social status. New Haven: Yale University; 1975;
  45. Hoppner J, Kunesch E, Grossman A, Tolzin CJ, Schulz M, Schlofke D, et al. Dysfunction of transcallosally mediated motor inhibition and callosal morphology in patients with schizophrenia. Acta Psychiatrica Scandinavica. 2001;104:227–235
  46. Hoy KE, Georgiou-Karistianis N, Laycock R, Fitzgerald PB. Using transcranial magnetic stimulation to investigate the cortical origins of motor overflow: a study in schizophrenia and healthy controls. Psychological Medicine. 2007;37:583–594
  47. Hutton SB, Huddy V, Barnes TRE, Robbins TW, Crawford TJ, Kennard C, et al. The relationship between antisaccades, smooth pursuit, and executive dysfunction in first-episode schizophrenia. Biological Psychiatry. 2004;56:553–559
  48. Iguchi Y, Hoshi Y, Hashimoto I. Selective spatial attention induces short-term plasticity in human somatosensory cortex. Neuroreport. 2001;12:3133–3136
  49. Ihara A, Hirata M, Yanagihara K, Ninomiya H, Imai K, Ishii R, et al. Neuromagnetic gamma-band activity in the primary and secondary somatosensory areas. Neuro- Report. 2003;14:273–277
  50. Isohanni M, Jones PB, Moilanen K, Rantakallio P, Veijola J, Oja H, et al. Early developmental milestones in adult schizophrenia and other psychoses. A 31-year follow-up of the northern Finland 1966 birth cohort. Schizophrenia Research. 2001;52:1–19
  51. Job DE, Whalley HC, Johnstone EC, Lawrie SM. Grey matter changes over time in high risk subjects developing schizophrenia. Neuroimage. 2005;25:1023–1030
  52. Just MA, Cherkassky VL, Keller TA, Minshew NJ. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of under-connectivity. Brain. 2004;127:1811–1821
  53. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, et al. Schedule for affective disorders and schizophrenia for school-age children — present and lifetime version (K-SADS-PL): initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry. 1997;36:980–988
  54. Kwon JS, O'Donnell BF, Wallenstein GV, Greene RW, Hirayasu Y, Nestor PG, et al. Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Archives of General Psychiatry. 1999;56:1001–1005
  55. Lewis DA, Pierri JN, Volk DW, Melchitzky DS, Woo TU. Altered GABA neurotransmission and prefrontal cortical dysfunction in schizophrenia. Biological Psychiatry. 1999;46:616–626
  56. Lubow RE, Kaplan O, Abramovich P, Rudnick A, Laor N. Visual search in schizophrenia: latent inhibition and novel pop-out effects. Schizophrenia Research. 2000;45:145–156
  57. MacQueen GM, Galway T, Goldberg JO, Tipper SP. Impaired distractor inhibition in patients with schizophrenia on a negative priming task. Psychological Medicine. 2003;33:121–129
  58. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19:1233–1239
  59. Maldjian JA, Laurienti PJ, Burdette JH. Precentral gyrus discrepancy in electronic versions of the talairach atlas. Neuroimage. 2004;21:450–455
  60. Mendrek A, Laurens KR, Kiehl KA, Ngan ET, Stip E, Liddle PF. Changes in distributed neural circuitry function with first-episode schizophrenia. British Journal of Psychiatry. 2004;185:205–214
  61. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping. 2002;15:1–25
  62. O'Donnell BF, Hetrick WP, Vohs JL, Krishnan GP, Carroll CA, Shekhar A. Neural synchronization deficits to auditory stimulation in bipolar disorder. Neuroreport. 2004;15:1369–1372
  63. Papp N, Ktonas P. Critical evaluation of complex demodulation techniques for the quantification of bioelectrical activity. Biomedical Sciences Instrumentation. 1977;13:135–143
  64. Pascual-Leone A, Tormos JM, Keenan J, Tarazona F, Canete C, Catala MD. Study and modulation of human cortical excitability with transcranial magnetic stimulation. Journal of Clinical Neurophysiology. 1998;15:333–343
  65. Pascual-Leone A, Manoach DS, Birnbaum R, Goff DC. Motor cortical excitability in schizophrenia. Biological Psychiatry. 2002;52:24–31
  66. Picard H, Amado I, Mouchet-Mages S, Olie JP, Krebs MO. The role of the cerebellum in schizophrenia: an update of clinical, cognitive, and functional evidences. Schizophrenia Bulletin. 2008;34:155–172
  67. Pierri JN, Chaudry AS, Woo TUW, Lewis DA. Alterations in chandelier neuron axon terminals in the prefrontal cortex of schizophrenic subjects. American Journal of Psychiatry. 1999;156:1709–1719
  68. Porjesz B, Almasy L, Edenberg HJ, Wang K, Chorlian DB, Foroud T, et al. Linkage disequilibrium between the beta frequency of the human EEG and a GABA-A receptor gene locus. Proceedings of the National Academy of Sciences of the United States of America. 2002;99:3729–3733
  69. Reite M, Teale P, Rojas DC, Benkers TL, Carlson J. Anomalous somatosensory cortical localization in schizophrenia. American Journal of Psychiatry. 2003;160:2148–2153
  70. Rojas DC, Camou SL, Reite ML, Rogers SJ. Planum temporale volume in children and adolescents with autism. Journal of Autism and Developmental Disorders. 2005;35:479–486
  71. Schmahmann JD. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. The Journal of Neuropsychiatry and Clinical Neurosciences. 2004;16:367–378
  72. Selemon LD, Goldman-Rakic PS. The reduced neurophil hypothesis: a circuit based model of schizophrenia. Biological Psychiatry. 1999;45:17–25
  73. Selemon LD, Rajkowska G, Goldman-Rakic PS. Abnormally high neuronal density in the schizophrenic cortex: a morphometric analysis of prefrontal area 9 and occipital area 17. Archives of General Psychiatry. 1995;52:805–818
  74. Sigurdsson E, Fombonne E, Sayal K, Checkley S. Neurodevelopmental antecedents of early-onset bipolar affective disorder. British Journal of Psychiatry. 1999;174:121–127
  75. Silverstein SM, Knight RA, Schwarzkopf SB, West LL, Osborn LM, Kamin D. Stimulus configuration and context effects in perceptual organization in schizophrenia. Journal of Abnormal Psychology. 1996;105:410–420
  76. Singer W. Neuronal synchrony: a versatile code for the definition of relations?. Neuron. 1999;24:49–65
  77. Singh KD, Barnes GR, Hillebrand A, Forde EME, Williams AL. Task-related changes in cortical synchronization are spatially coincident with the hemodynamic response. Neuroimage. 2002;16:103–114
  78. Singh KD, Barnes GR, Hillebrand A. Group imaging of task-related changes in cortical synchronisation using non-parametric permutation testing. Neuroimage. 2003;19:1589–1601
  79. Traub RD, Whittington MA, Stanford IM, Jefferys JA. Mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature. 1996;383:621–624
  80. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 2002;15:273–289
  81. Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. Magnetic stimulation over the cerebellum in humans. Annals of Neurology. 1995;37:703–713
  82. van Veen BD, van Drongelen W, Yuchtman M, Suzuki A. Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Transactions on Biomedical Engineering. 1997;44:867–880
  83. Vink M, Ramsey NF, Raemaekers M, Kahn RS. Negative priming in schizophrenia revisited. Schizophrenia Research. 2005;79:211–216
  84. Walter H, Vasic N, Hose A, Spitzer M, Wolf RC. Working memory dysfunction in schizophrenia compared to healthy controls and patients with depression: evidence from event-related fMRI. Neuroimage. 2007;35:1551–1561
  85. Whittington MA, Traub RD, Jefferys JG. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature. 1995;373:612–615
  86. Williams JH, Wellman NA, Geaney DP, Cowen PJ, Feldon J, Rawlins JN. Reduced latent inhibition in people with schizophrenia: an effect of psychosis or its treatment. British Journal of Psychiatry. 1998;172:243–249
  87. Wilson TW, Hernandez OO, Asherin RM, Teale PD, Reite ML, Rojas DC. Cortical gamma generators suggest abnormal auditory circuitry in early-onset psychosis. Cerebral Cortex. 2008;18:371–378
  88. Woo TU, Whitehead RE, Melchitzky DS, Lewis DA. A subclass of prefrontal gamma-aminobutyric acid axon terminals are selectively altered in schizophrenia. Sciences of the United States of America. 1998;95:5341–5346
  89. Woodruff PW, McManus IC, David AS. Meta-analysis of corpus callosum size in schizophrenia. Journal of Neurology, Neurosurgery and Psychiatry. 1995;58:457–461
  90. Yang TT, Gallen CC, Schwartz BJ, Bloom FE. Noninvasive somatosensory homunculus mapping in humans by using a large-array biomagnetometer. Proceedings of the National Academy of Sciences USA. 1993;90:3098–3102
  91. Ziemann U, Hallett M. Basic neurophysiological studies with TMS. In:  George MS,  Belmaker RH editor. Transcranial Magnetic Stimulation in Neuropsychiatry. Washington, DC: American Psychiatric Press; 2000;p. 45–98

PII: S0925-4927(09)00082-1

doi: 10.1016/j.pscychresns.2009.03.009

Psychiatry Research: Neuroimaging
Volume 174, Issue 1 , Pages 47-56 , 30 October 2009

Article Tools

* Image Usage & Resolution