Schizophrenia Research
Volume 117, Issue 1 , Pages 13-20 , March 2010

Amplitude of low-frequency oscillations in schizophrenia: A resting state fMRI study

  • Matthew J. Hoptman

      Affiliations

    • Division of Clinical Research, Nathan Kline Institute, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States
    • Department of Psychiatry, New York University School of Medicine, 650 First Ave., New York, NY 10016, United States
    • Corresponding Author InformationCorresponding author. Division of Clinical Research, Nathan Kline Institute, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States Tel.: +1 845 398 6569; fax: +1 845 398 6566.
  • ,
  • Xi-Nian Zuo

      Affiliations

    • The Phyllis Green and Randolph Cōwen Institute for Pediatric Neuroscience, New York University Child Study Center, United States
  • ,
  • Pamela D. Butler

      Affiliations

    • Program in Cognitive Neuroscience and Schizophrenia, Nathan Kline Institute, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States
    • Department of Psychiatry, New York University School of Medicine, 650 First Ave., New York, NY 10016, United States
  • ,
  • Daniel C. Javitt

      Affiliations

    • Program in Cognitive Neuroscience and Schizophrenia, Nathan Kline Institute, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States
    • Department of Psychiatry, New York University School of Medicine, 650 First Ave., New York, NY 10016, United States
  • ,
  • Debra D'Angelo

      Affiliations

    • Division of Clinical Research, Nathan Kline Institute, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States
  • ,
  • Cristina J. Mauro

      Affiliations

    • Division of Clinical Research, Nathan Kline Institute, 140 Old Orangeburg Road, Orangeburg, NY 10962, United States
  • ,
  • Michael P. Milham

      Affiliations

    • The Phyllis Green and Randolph Cōwen Institute for Pediatric Neuroscience, New York University Child Study Center, United States

Received 7 May 2009 ,Revised 19 September 2009 ,Accepted 22 September 2009.

References 

  1. Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 1986;9:357–381
  2. American Psychiatric Association. Practice guideline for the treatment of patients with schizophrenia. Am. J. Psychiat. 1997;154:1–63Suppl
  3. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR). Washington D.C: American Psychiatric Association; 2000;
  4. Andreasen NC, Nopoulos P, O'Leary DS, Miller DD, Wassink T, Flaum M. Defining the phenotype of schizophrenia: cognitive dysmetria and its neural mechanisms. Biol. Psychiatry. 1999;46:908–920
  5. Bilder RM, Goldman RS, Robinson D, Reiter G, Bell L, Bates JA, et al. Neuropsychology of first-episode schizophrenia: Initial characterization and clinical correlates. Am. J. Psychiatr. 2000;157:549–559
  6. Bilder RM, Goldman RS, Volavka J, Czobor P, Hoptman M, Sheitman B, et al. Neurocognitive effects of clozapine, olanzapine, risperidone, and haloperidol in patients with chronic schizophrenia or schizoaffective disorder. Am. J. Psychiatry. 2002;159:1018–1028
  7. Biswal B, Yetkin FZ, Haughton VM, Hyde JS. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995;34:537–541
  8. Bluhm RL, Miller J, Lanius RA, Osuch EA, Boksman K, Neufeld R, et al. Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. Schizophr. Bull. 2007;33:1004–1012
  9. Butler PD, Javitt DC. Early-stage visual processing deficits in schizophrenia. Curr. Opin. Psychiatr. 2005;18:151–157
  10. Butler PD, Zemon V, Schechter I, Saperstein AM, Hoptman MJ, Lim KO, et al. Early-stage visual processing and cortical amplification deficits in schizophrenia. Arch. Gen. Psychiatry. 2005;62:495–504
  11. Butler PD, Silverstein SM, Dakin SC. Visual perception and its impairment in schizophrenia. Biol. Psychiatry. 2008;64:40–47
  12. Buzsaki G, Draguhn A. Neuronal oscillations in cortical networks. Science. 2004;304:1926–1929
  13. Callicott JH, Mattay VS, Verchinski BA, Marenco S, Egan MF, Weinberger DR. Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. Am. J. Psychiatry. 2003;160:2209–2215
  14. Carter CS. Re-conceptualizing schizophrenia as a disorder of cognitive and emotional processing: a shot in the arm for translational research. Biol. Psychiatry. 2006;60:1169–1170
  15. Castellanos FX, Margulies DS, Kelly C, Uddin LQ, Ghaffari M, Kirsch A, et al. Cingulate-precuneus interactions: a new locus of dysfunction in adult attention-deficit/hyperactivity disorder. Biol. Psychiatry. 2008;63:332–337
  16. Cho RY, Konecky RO, Carter CS. Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 2006;103:19878–19883
  17. Cincotta CM, Seger CA. Dissociation between striatal regions while learning to categorize via feedback and via observation. J. Cogn. Neurosci. 2007;19:249–265
  18. Cox RW. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996;29:162–173
  19. Di Martino A, Ghaffari M, Curchack J, Reiss P, Hyde C, Vannucci M, et al. Decomposing intra-subject variability in children with attention-deficit/hyperactivity disorder. Biol. Psychiatry. 2008;64:607–614
  20. Doniger GM, Silipo G, Rabinowicz EF, Snodgrass JG, Javitt DC. Impaired sensory processing as a basis for object-recognition deficits in schizophrenia. Am. J. Psychiatry. 2001;158:1818–1826
  21. Ehrlichman RS, Gandal MJ, Maxwell CR, Lazarewicz MT, Finkel LH, Contreras D, et al. N-methyl-d-aspartic acid receptor antagonist-induced frequency oscillations in mice recreate pattern of electrophysiological deficits in schizophrenia. Neuroscience. 2009;158:705–712
  22. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-patient Edition (SCID-I/NP) Biometrics Division. New York: New York State Psychiatric Institute; 2001;
  23. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured Clinical Interview for DSM-IV-TR Axis I Disorders—Patient Edition (SCID-I/P, 11/2002 revision) Biometrics Research Department. New York: New York State Psychiatric Institute; 2002;
  24. Ford JM, Krystal JH, Mathalon DH. Neural synchrony in schizophrenia: from networks to new treatments. Schizophr. Bull. 2007;33:848–852
  25. Fransson P. How default is the default mode of brain function? Further evidence from intrinsic BOLD signal fluctuations. Neuropsychologia. 2006;44:2836–2845
  26. Gallinat J, Winterer G, Herrmann CS, Senkowski D. Reduced oscillatory gamma-band responses in unmedicated schizophrenic patients indicate impaired frontal network processing. Clin. Neurophysiol. 2004;115:1863–1874
  27. 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
  28. Goldman-Rakic PS. Working memory dysfunction in schizophrenia. J. Neuropsychiatry Clin. Neurosci. 1994;6:348–357
  29. Green MF, Nuechterlein KH, Mintz J. Backward masking in schizophrenia and mania. I. Specifying a mechanism. Arch. Gen. Psychiatry. 1994;51:939–944
  30. Gur RE. Left hemisphere dysfunction and left hemisphere overactivation in schizophrenia. J. Abnorm. Psychology. 1978;87:226–238
  31. Heckers S. Neuroimaging studies of the hippocampus in schizophrenia. Hippocampus. 2001;11:520–528
  32. Hoptman, M.J., D'Angelo, D., Catalano, D., Mauro, M.J., Shehzad, Z.E., Kelly, A.M.C., Castellanos, F.X., Javitt, D.C., Milham, M.P., in press. Amygdalofrontal functional disconnectivity and aggression in schizophrenia. Schizophrenia Bulletin. doi:10.1093/schbul/sbp012.
  33. Jafri MJ, Pearlson GD, Stevens M, Calhoun VD. A method for functional network connectivity among spatially independent resting-state components in schizophrenia. NeuroImage. 2008;39:1666–1681
  34. Javitt DC. Intracortical mechanisms of mismatch negativity dysfunction in schizophrenia. Audiol. Neuro-Otol. 2000;5:207–215
  35. Javitt DC. When doors of perception close: bottom–up models of disrupted cognition in schizophrenia. Annu. Rev. Clin. Psychol. 2009;5:249–275
  36. Javitt DC, Zukin SR. Recent advances in the phencyclidine model of schizophrenia. Am. J. Psychiatry. 1991;148:1301–1308
  37. Javitt DC, Doneshka P, Zylberman I, Ritter W, Vaughan HG. Impairment of early cortical processing in schizophrenia: an event-related potential confirmation study. Biol. Psychiatry. 1993;33:513–519
  38. Javitt DC, Shelley AM, Silipo G, Lieberman JA. Deficits in auditory and visual context-dependent processing in schizophrenia: defining the pattern. Arch. Gen. Psychiatry. 2000;57:1131–1137
  39. Kannurpatti SS, Biswal BB. Detection and scaling of task-induced fMRI-BOLD response using resting state fluctuations. NeuroImage. 2008;40:1567–1574
  40. Kay SR, Opler LA, Fiszbein A. Positive and Negative Syndrome Scale (PANSS) Bronx Psychiatric Center, N.Y. 1986;
  41. Kelly AMC, Uddin LQ, Biswal BB, Castellanos FX, Milham MP. Competition between functional brain networks mediates behavioral variability. NeuroImage. 2008;39:527–537
  42. Krieckhaus EE, Donahoe JW, Morgan MA. Paranoid schizophrenia may be caused by dopamine hyperactivity of CA1 hippocampus. Biol. Psychiatry. 1992;31:560–570
  43. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE. An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. J. Neurophysiol. 2005;94:1904–1911
  44. Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE. Entrainment of neuronal oscillations as a mechanism of attentional selection. Science. 2008;320:110–113
  45. Leitman DI, Foxe JJ, Butler PD, Saperstein A, Revheim N, Javitt DC. Sensory contributions to impaired prosodic processing in schizophrenia. Biol. Psychiatry. 2005;58:56–61
  46. Liang M, Zhou Y, Jiang T, Liu Z, Tian L, Liu H, et al. Widespread functional disconnectivity in schizophrenia with resting-state functional magnetic resonance imaging. NeuroReport. 2006;17:209–213
  47. Lodge DJ, Grace AA. Aberrant hippocampal activity underlies the dopamine dysregulation in an animal model of schizophrenia. J. Neurosci. 2007;27:11424–11430
  48. Margulies DS, Kelly AM, Uddin LQ, Biswal BB, Castellanos FX, Milham MP. Mapping the functional connectivity of anterior cingulate cortex. NeuroImage. 2007;37:579–588
  49. Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, Honey G, et al. Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol. Psychiatry. 2008;13:239, 267–239, 276
  50. Rabinowicz EF, Silipo G, Goldman R, Javitt DC. Auditory sensory dysfunction in schizophrenia: imprecision or distractibility?. Arch. Gen. Psychiatry. 2000;57:1149–1155
  51. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function. Proc. Natl. Acad. Sci. U. S. A. 2001;98:676–682
  52. Revheim N, Butler PD, Schechter I, Jalbrzikowski M, Silipo G, Javitt DC. Reading impairment and visual processing deficits in schizophrenia. Schizophr. Res. 2006;87:238–245
  53. Rusch N, Spoletini I, Wilke M, Bria P, Di PM, Di IF, et al. Prefrontal–thalamic–cerebellar gray matter networks and executive functioning in schizophrenia. Schizophr. Res. 2007;93:79–89
  54. Saad ZS, Reynolds RC, Argall B, Japee S, Cox RW. SUMA: an interface for surface-based intra- and inter-subject analysis with AFNI. In: 2nd IEEE International Symposium on Biomedical Imaging: Macro to Nano. vol. 2:2004;p. 1510–1513
  55. Schroeder CE, Lakatos P. Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 2009;32:9–18
  56. Seger CA, Cincotta CM. The roles of the caudate nucleus in human classification learning. J. Neurosci. 2005;25:2941–2951
  57. Shehzad Z, Kelly AM, Reiss PT, Gee DG, Gotimer K, Uddin LQ, et al. The resting brain: unconstrained yet reliable. Cereb. Cortex. 2009;19:2209–2229
  58. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsaki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron. 2008;60:683–697
  59. Spencer KM, Nestor PG, Niznikiewicz MA, Salisbury DF, Shenton ME, McCarley RW. Abnormal neural synchrony in schizophrenia. J. Neurosci. 2003;23:7407–7411
  60. Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, et al. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 2004;101:17288–17293
  61. Spencer KM, Niznikiewicz MA, Shenton ME, McCarley RW. Sensory-evoked gamma oscillations in chronic schizophrenia. Biol. Psychiatry. 2008;63:744–747
  62. Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J. Induced gamma-band activity during the delay of a visual short-term memory task in humans. J. Neurosci. 1998;18:4244–4254
  63. Tremeau F. A review of emotion deficits in schizophrenia. Dial. Clin. Neurosci. 2006;8:59–70
  64. Uhlhaas PJ, Haenschel C, Nikolic D, Singer W. The role of oscillations and synchrony in cortical networks and their putative relevance for the pathophysiology of schizophrenia. Schizophr. Bull. 2008;34:927–943
  65. Whitfield-Gabrieli S, Thermenos HW, Milanovic S, Tsuang MT, Faraone SV, McCarley RW, 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
  66. Wolf JA, Moyer JT, Lazarewicz MT, Contreras D, Benoit-Marand M, O'Donnell P, et al. NMDA/AMPA ratio impacts state transitions and entrainment to oscillations in a computational model of the nucleus accumbens medium spiny projection neuron. J. Neurosci. 2005;25:9080–9095
  67. Worsley K. Statistical analysis of activation images. In:  Jezzard P,  Matthews PM,  Smith SM editor. Functional MRI: An Introduction to Methods. Oxford, UK: Oxford University Press; 2001;
  68. Yang H, Long XY, Yang Y, Yan H, Zhu CZ, Zhou XP, et al. Amplitude of low frequency fluctuation within visual areas revealed by resting-state functional MRI. Neuroimage. 2007;36:144–152
  69. Zang YF, Yang H, Zhu CZ, Qing-Ju C, Man-Qiu S, Meng L, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 2007;92:83–91
  70. Zhou Y, Liang M, Tian L, Wang K, Hao Y, Liu H, et al. Functional disintegration in paranoid schizophrenia using resting-state fMRI. Schizophr. Res. 2007;97:194–205
  71. Zou QH, Zhu CZ, Yang Y, Zuo XN, Long XY, Cao QJ, et al. An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J. Neurosci. Methods. 2008;172:137–141
  72. Zuo XN, Di Martino A, Kelly C, Shehzad ZE, Gee D, Klein DF, et al. The oscillating brain: complex and reliable. Neuroimage. 2010;49:1432–1445

PII: S0920-9964(09)00474-5

doi: 10.1016/j.schres.2009.09.030

Schizophrenia Research
Volume 117, Issue 1 , Pages 13-20 , March 2010