Korean Journal of Biological Psychiatry (생물정신의학)

The Korean Society of Biological Psychiatry (대한생물정신의학회)
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Sex-Related Differences of EEG Coherences between Patients with Schizophrenia and Healthy Controls

조현병 환자와 건강한 대조군에서 성별에 따른 뇌파 동시성의 차이

  • Received : 2013.07.03
  • Accepted : 2013.09.23
  • Published : 2013.11.30
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Abstract

Objectives Alteration of epigenetic effects of testosterone during early development was suggested as an ancillary mechanism for the genesis of schizophrenia. EEG coherence was thought to be a marker for cerebral laterality of which important determinant was testosterone during early development. We studied sex-related differences of EEG coherences between patients with schizophrenia and controls to examine the sex effects in the genesis of schizophrenia. Methods EEG was recorded in 35 patients with schizophrenia and 46 healthy controls in the eyes closed resting state. Pair-wise EEG coherences were calculated over delta, theta, alpha, beta and gamma frequency bands. To examine the differences of EEG coherence according to sex in each group, ANCOVA was performed using Statistical Analysis system (SAS, Ver 9.3) and R (Ver 2.15.2). Results Healthy control males showed more increased right intrahemispheric coherences than healthy control females in delta, theta, alpha and beta frequency bands. In patients with schizophrenia, this male dominant pattern in right intrahemispheric coherences was attenuated especially in alpha and beta bands. Healthy control females showed more increased interhemispheric coherences than healthy control males in delta, theta, beta and gamma frequency bands. In patients with schizophrenia, these female dominant patterns in interhemispheric coherences were attenuated especially in delta, theta, and beta bands, which were commonly observed in frontal to central areas. Conclusion Sex differences in resting EEG coherences were attenuated in schizophrenia patients. These results imply that sex-related aberrant cerebral lateralization might exist in patients with schizophrenia, which are partly due to sex hormones via epigenetic mechanisms.

Keywords

References

  1. Maccoby EM, Jacklin CN. The psychology of sex differences. 1st ed. Stanford, CA: Standford University Press;1974. p.17-276.
  2. Geschwind N, Galaburda AM. Cerebral lateralization. Biological mechanisms, associations, and pathology: III. A hypothesis and a program for research. Arch Neurol 1985;42:634-654. https://doi.org/10.1001/archneur.1985.04060070024012
  3. Bianki VL, Filippova EB. Sex Differences in Lateralization in the Animal Brain. 1st ed. Amsterdam, the Neterlands: Harwood Academic Publishers;2000. p.1-18.
  4. Thatcher RW, Krause PJ, Hrybyk M. Cortico-cortical associations and EEG coherence: a two-compartmental model. Electroencephalogr Clin Neurophysiol 1986;64:123-143. https://doi.org/10.1016/0013-4694(86)90107-0
  5. Wada Y, Nanbu Y, Kadoshima R, Jiang ZY, Koshino Y, Hashimoto T. Interhemispheric EEG coherence during photic stimulation: sex differences in normal young adults. Int J Psychophysiol 1996;22:45-51. https://doi.org/10.1016/0167-8760(96)00011-6
  6. Beaumont JG, Mayes AR, Rugg MD. Asymmetry in EEG alpha coherence and power: effects of task and sex. Electroencephalogr Clin Neurophysiol 1978;45:393-401. https://doi.org/10.1016/0013-4694(78)90190-6
  7. Marosi E, Harmony T, Becker J, Bernal J, Reyes A, Rodriguez M, et al. Sex differences in EEG coherence in normal children. Int J Neurosci 1993;72:115-121. https://doi.org/10.3109/00207459308991628
  8. Vogel F. The genetic basis of the normal human electroencephalogram (EEG). Humangenetik 1970;10:91-114. https://doi.org/10.1007/BF00295509
  9. Kim A, Kim SK, Youn J, Jeong JS, Lee JH, Chae JH, et al. A study of the relationships between the ratio of 2nd to 4th digit length and cerebral laterality. Korean J Biol Psychiatry 2011;18:25-35.
  10. Abel KM, Drake R, Goldstein JM. Sex differences in schizophrenia. Int Rev Psychiatry 2010;22:417-428. https://doi.org/10.3109/09540261.2010.515205
  11. Leung A, Chue P. Sex differences in schizophrenia, a review of the literature. Acta Psychiatr Scand Suppl 2000;401:3-38.
  12. Mendrek A, Stip E. Sexual dimorphism in schizophrenia: is there a need for gender-based protocols? Expert Rev Neurother 2011;11:951- 959. https://doi.org/10.1586/ern.11.78
  13. Shtasel DL, Gur RE, Gallacher F, Heimberg C, Gur RC. Gender differences in the clinical expression of schizophrenia. Schizophr Res 1992;7:225-231. https://doi.org/10.1016/0920-9964(92)90016-X
  14. Szymanski S, Lieberman JA, Alvir JM, Mayerhoff D, Loebel A, Geisler S, et al. Gender differences in onset of illness, treatment response, course, and biologic indexes in first-episode schizophrenic patients. Am J Psychiatry 1995;152:698-703. https://doi.org/10.1176/ajp.152.5.698
  15. Andia AM, Zisook S, Heaton RK, Hesselink J, Jernigan T, Kuck J, et al. Gender differences in schizophrenia. J Nerv Ment Dis 1995;183: 522-528. https://doi.org/10.1097/00005053-199508000-00005
  16. Seeman MV. Schizophrenia: women bear a disproportionate toll of antipsychotic side effects. J Am Psychiatr Nurses Assoc 2010;16:21- 29. https://doi.org/10.1177/1078390309350918
  17. Andersen SW, Clemow DB, Corya SA. Long-term weight gain in patients treated with open-label olanzapine in combination with fluoxetine for major depressive disorder. J Clin Psychiatry 2005;66:1468- 1476. https://doi.org/10.4088/JCP.v66n1118
  18. Covell NH, Weissman EM, Essock SM. Weight gain with clozapine compared to first generation antipsychotic medications. Schizophr Bull 2004;30:229-240. https://doi.org/10.1093/oxfordjournals.schbul.a007074
  19. St Clair D, Xu M, Wang P, Yu Y, Fang Y, Zhang F, et al. Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959-1961. JAMA 2005;294:557-562. https://doi.org/10.1001/jama.294.5.557
  20. Murray EK, Hien A, de Vries GJ, Forger NG. Epigenetic control of sexual differentiation of the bed nucleus of the stria terminalis. Endocrinology 2009;150:4241-4247. https://doi.org/10.1210/en.2009-0458
  21. Flor-Henry P, Koles ZJ. Statistical quantitative EEG studies of depression, mania, schizophrenia and normals. Biol Psychol 1984;19: 257-279. https://doi.org/10.1016/0301-0511(84)90042-5
  22. Ford JM, Mathalon DH, Whitfield S, Faustman WO, Roth WT. Reduced communication between frontal and temporal lobes during talking in schizophrenia. Biol Psychiatry 2002;51:485-492. https://doi.org/10.1016/S0006-3223(01)01335-X
  23. Hoffman RE, Buchsbaum MS, Escobar MD, Makuch RW, Nuechterlein KH, Guich SM. EEG coherence of prefrontal areas in normal and schizophrenic males during perceptual activation. J Neuropsychiatry Clin Neurosci 1991;3:169-175. https://doi.org/10.1176/jnp.3.2.169
  24. Merrin EL, Floyd TC. Negative symptoms and EEG alpha activity in schizophrenic patients. Schizophr Res 1992;8:11-20. https://doi.org/10.1016/0920-9964(92)90056-B
  25. Norman RM, Malla AK, Williamson PC, Morrison-Stewart SL, Helmes E, Cortese L. EEG coherence and syndromes in schizophrenia. Br J Psychiatry 1997;170:411-415. https://doi.org/10.1192/bjp.170.5.411
  26. Tauscher J, Fischer P, Neumeister A, Rappelsberger P, Kasper S. Low frontal electroencephalographic coherence in neuroleptic-free schizophrenic patients. Biol Psychiatry 1998;44:438-447. https://doi.org/10.1016/S0006-3223(97)00428-9
  27. Mann K, Maier W, Franke P, Roschke J, Gansicke M. Intra- and interhemispheric electroencephalogram coherence in siblings discordant for schizophrenia and healthy volunteers. Biol Psychiatry 1997; 42:655-663. https://doi.org/10.1016/S0006-3223(96)00497-0
  28. Wada Y, Nanbu Y, Kikuchi M, Koshino Y, Hashimoto T. Aberrant functional organization in schizophrenia: analysis of EEG coherence during rest and photic stimulation in drug-naive patients. Neuropsychobiology 1998;38:63-69. https://doi.org/10.1159/000026518
  29. Nagase Y, Okubo Y, Matsuura M, Kojima T, Toru M. EEG coherence in unmedicated schizophrenic patients: topographical study of predominantly never medicated cases. Biol Psychiatry 1992;32:1028- 1034. https://doi.org/10.1016/0006-3223(92)90064-7
  30. Winterer G, Egan MF, Rädler T, Hyde T, Coppola R, Weinberger DR. An association between reduced interhemispheric EEG coherence in the temporal lobe and genetic risk for schizophrenia. Schizophr Res 2001;49:129-143. https://doi.org/10.1016/S0920-9964(00)00128-6
  31. Higashima M, Takeda T, Kikuchi M, Nagasawa T, Hirao N, Oka T, et al. State-dependent changes in intrahemispheric EEG coherence for patients with acute exacerbation of schizophrenia. Psychiatry Res 2007;149:41-47. https://doi.org/10.1016/j.psychres.2005.05.020
  32. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971;9:97-113. https://doi.org/10.1016/0028-3932(71)90067-4
  33. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 2004;134:9-21. https://doi.org/10.1016/j.jneumeth.2003.10.009
  34. Thatcher RW, Krause PJ, Hrybyk M. Cortico-cortical associations and EEG coherence: a two-compartmental model. Electroencephalogr Clin Neurophysiol 1986;64:123-143. https://doi.org/10.1016/0013-4694(86)90107-0
  35. Coben LA, Danziger W, Storandt M. A longitudinal EEG study of mild senile dementia of Alzheimer type: changes at 1 year and at 2.5 years. Electroencephalogr Clin Neurophysiol 1985;61:101-112. https://doi.org/10.1016/0013-4694(85)91048-X
  36. Jorge MS, Botelho RV, Melo AC. Study of interhemispheric coherence on healthy adults. Arq Neuropsiquiatr 2007;65:377-380. https://doi.org/10.1590/S0004-282X2007000300002
  37. McGue M, Gottesman II. The genetic epidemiology of schizophrenia and the design of linkage studies. Eur Arch Psychiatry Clin Neurosci 1991;240:174-181. https://doi.org/10.1007/BF02190760
  38. Tsuang M. Schizophrenia: genes and environment. Biol Psychiatry 2000;47:210-220. https://doi.org/10.1016/S0006-3223(99)00289-9
  39. Yeragani VK, Cashmere D, Miewald J, Tancer M, Keshavan MS. Decreased coherence in higher frequency ranges (beta and gamma) between central and frontal EEG in patients with schizophrenia: A preliminary report. Psychiatry Res 2006;141:53-60. https://doi.org/10.1016/j.psychres.2005.07.016
  40. Ray WJ, Cole HW. EEG alpha activity reflects attentional demands, and beta activity reflects emotional and cognitive processes. Science 1985;228:750-752. https://doi.org/10.1126/science.3992243
  41. Uhlhaas PJ, Haenschel C, Nikolić 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. https://doi.org/10.1093/schbul/sbn062
  42. Knyazev GG. EEG delta oscillations as a correlate of basic homeostatic and motivational processes. Neurosci Biobehav Rev 2012;36: 677-695. https://doi.org/10.1016/j.neubiorev.2011.10.002
  43. Rodriguez E, George N, Lachaux JP, Martinerie J, Renault B, Varela FJ. Perception's shadow: long-distance synchronization of human brain activity. Nature 1999;397:430-433. https://doi.org/10.1038/17120
  44. Tallon-Baudry C, Bertrand O. Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 1999;3: 151-162. https://doi.org/10.1016/S1364-6613(99)01299-1
  45. Fries P, Nikolić D, Singer W. The gamma cycle. Trends Neurosci 2007; 30:309-316. https://doi.org/10.1016/j.tins.2007.05.005
  46. Singer W. Neuronal synchrony: a versatile code for the definition of relations? Neuron 1999;24:49-65, 111-125. https://doi.org/10.1016/S0896-6273(00)80821-1
  47. Bandyopadhyaya D, Nizamie SH, Pradhan N, Bandyopadhyaya A. Spontaneous gamma coherence as a possible trait marker of schizophrenia- An explorative study. Asian J Psychiatr 2011;4:172-177. https://doi.org/10.1016/j.ajp.2011.06.006
  48. Rossi A, Serio A, Stratta P, Petruzzi C, Schiazza G, Mancini F, et al. Planum temporale asymmetry and thought disorder in schizophrenia. Schizophr Res 1994;12:1-7. https://doi.org/10.1016/0920-9964(94)90078-7
  49. Petty RG, Barta PE, Pearlson GD, McGilchrist IK, Lewis RW, Tien AY, et al. Reversal of asymmetry of the planum temporale in schizophrenia. Am J Psychiatry 1995;152:715-721. https://doi.org/10.1176/ajp.152.5.715
  50. Barta PE, Pearlson GD, Brill LB 2nd, Royall R, McGilchrist IK, Pulver AE, et al. Planum temporale asymmetry reversal in schizophrenia: replication and relationship to gray matter abnormalities. Am J Psychiatry 1997;154:661-667. https://doi.org/10.1176/ajp.154.5.661
  51. Kwon JS, McCarley RW, Hirayasu Y, Anderson JE, Fischer IA, Kikinis R, et al. Left planum temporale volume reduction in schizophrenia. Arch Gen Psychiatry 1999;56:142-148. https://doi.org/10.1001/archpsyc.56.2.142
  52. Hirayasu Y, McCarley RW, Salisbury DF, Tanaka S, Kwon JS, Frumin M, et al. Planum temporale and Heschl gyrus volume reduction in schizophrenia: a magnetic resonance imaging study of first-episode patients. Arch Gen Psychiatry 2000;57:692-699. https://doi.org/10.1001/archpsyc.57.7.692
  53. Gaser C, Nenadic I, Volz HP, Büchel C, Sauer H. Neuroanatomy of "hearing voices": a frontotemporal brain structural abnormality associated with auditory hallucinations in schizophrenia. Cereb Cortex 2004;14:91-96. https://doi.org/10.1093/cercor/bhg107
  54. Levitan C, Ward PB, Catts SV. Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia. Biol Psychiatry 1999;46:955-962. https://doi.org/10.1016/S0006-3223(98)00373-4
  55. Sumich A, Chitnis XA, Fannon DG, O'Ceallaigh S, Doku VC, Faldrowicz A, et al. Unreality symptoms and volumetric measures of Heschl's gyrus and planum temporal in first-episode psychosis. Biol Psychiatry 2005;57:947-950. https://doi.org/10.1016/j.biopsych.2004.12.041
  56. Artiges E, Martinot JL, Verdys M, Attar-Levy D, Mazoyer B, Tzourio N, et al. Altered hemispheric functional dominance during word generation in negative schizophrenia. Schizophr Bull 2000;26:709- 721. https://doi.org/10.1093/oxfordjournals.schbul.a033488
  57. Sommer IE, Ramsey NF, Kahn RS. Language lateralization in schizophrenia, an fMRI study. Schizophr Res 2001;52:57-67. https://doi.org/10.1016/S0920-9964(00)00180-8
  58. Oertel V, Knochel C, Rotarska-Jagiela A, Schonmeyer R, Lindner M, van de Ven V, et al. Reduced laterality as a trait marker of schizophrenia-- evidence from structural and functional neuroimaging. J Neurosci 2010;30:2289-2299. https://doi.org/10.1523/JNEUROSCI.4575-09.2010
  59. Dolan RJ, Fletcher PC, McKenna P, Friston KJ, Frith CD. Abnormal neural integration related to cognition in schizophrenia. Acta Psychiatr Scand Suppl 1999;395:58-67.
  60. John JP. Fronto-temporal dysfunction in schizophrenia: A selective review. Indian J Psychiatry 2009;51:180-190. https://doi.org/10.4103/0019-5545.55084
  61. Friston KJ, Frith CD. Schizophrenia: a disconnection syndrome? Clin Neurosci 1995;3:89-97.
  62. Volkow ND, Wolf AP, Brodie JD, Cancro R, Overall JE, Rhoades H, et al. Brain interactions in chronic schizophrenics under resting and activation conditions. Schizophr Res 1988;1:47-53. https://doi.org/10.1016/0920-9964(88)90039-4
  63. Weinberger DR, Berman KF, Suddath R, Torrey EF. Evidence of dysfunction of a prefrontal-limbic network in schizophrenia: a magnetic resonance imaging and regional cerebral blood flow study of discordant monozygotic twins. Am J Psychiatry 1992;149:890-897. https://doi.org/10.1176/ajp.149.7.890
  64. Tononi G, Edelman GM. Schizophrenia and the mechanisms of conscious integration. Brain Res Brain Res Rev 2000;31:391-400. https://doi.org/10.1016/S0165-0173(99)00056-9
  65. Crow TJ. Schizophrenia as failure of hemispheric dominance for language. Trends Neurosci 1997;20:339-343. https://doi.org/10.1016/S0166-2236(97)01071-0
  66. Geschwind N, Levitsky W. Human brain: left-right asymmetries in temporal speech region. Science 1968;161:186-187. https://doi.org/10.1126/science.161.3837.186
  67. Nasrallah HA. The unintegrated right cerebral hemispheric consciousness as alien intruder: a possible mechanism for Schneiderian delusions in schizophrenia. Compr Psychiatry 1985;26:273-282. https://doi.org/10.1016/0010-440X(85)90072-0
  68. Shapleske J, Rossell SL, Woodruff PW, David AS. The planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Brain Res Rev 1999;29:26-49. https://doi.org/10.1016/S0165-0173(98)00047-2
  69. Sommer I, Ramsey N, Kahn R, Aleman A, Bouma A. Handedness, language lateralisation and anatomical asymmetry in schizophrenia: meta-analysis. Br J Psychiatry 2001;178:344-351. https://doi.org/10.1192/bjp.178.4.344
  70. Friston KJ. The disconnection hypothesis. Schizophr Res 1998;30: 115-125. https://doi.org/10.1016/S0920-9964(97)00140-0
  71. Stephan KE, Baldeweg T, Friston KJ. Synaptic plasticity and dysconnection in schizophrenia. Biol Psychiatry 2006;59:929-939. https://doi.org/10.1016/j.biopsych.2005.10.005
  72. Winterer G, Coppola R, Goldberg TE, Egan MF, Jones DW, Sanchez CE, et al. Prefrontal broadband noise, working memory, and genetic risk for schizophrenia. Am J Psychiatry 2004;161:490-500. https://doi.org/10.1176/appi.ajp.161.3.490
  73. Manning JT, Scutt D, Wilson J, Lewis-Jones DI. The ratio of 2nd to 4th digit length: a predictor of sperm numbers and concentrations of testosterone, luteinizing hormone and oestrogen. Hum Reprod 1998; 13:3000-3004. https://doi.org/10.1093/humrep/13.11.3000
  74. Collinson SL, Lim M, Chaw JH, Verma S, Sim K, Rapisarda A, et al. Increased ratio of 2nd to 4th digit (2D:4D) in schizophrenia. Psychiatry Res 2010;176:8-12. https://doi.org/10.1016/j.psychres.2009.08.023
  75. Geschwind N, Galaburda AM. Cerebral lateralization; biological mechanism, associations, and pathology. Cambridge, MA: An MIT Press Classic;1987. p.223-239.
  76. John JP, Khanna S, Pradhan N, Mukundan CR. EEG alpha coherence and psychopathological dimensions of schizophrenia. Indian J Psychiatry 2002;44:97-107.
  77. Higashima M, Takeda T, Kikuchi M, Nagasawa T, Koshino Y. Functional connectivity between hemispheres and schizophrenic symptoms: a longitudinal study of interhemispheric EEG coherence in patients with acute exacerbations of schizophrenia. Clin EEG Neurosci 2006;37:10-15. https://doi.org/10.1177/155005940603700104
  78. Ray D, Ram D. Electrophysiological examination of formal thought disorder in schizophrenia. Asian J Psychiatr 2012;5:327-338. https://doi.org/10.1016/j.ajp.2012.07.005