Korean Journal of Biological Psychiatry (생물정신의학)

The Korean Society of Biological Psychiatry (대한생물정신의학회)
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The Sex-Related Differences of Relationships between 2D : 4D Ratio and Electroencephalographic Coherence in Patients with Schizophrenia Compared with Controls

조현병 환자에서 성별에 따른 검지 대 약지의 길이 비율과 뇌파 동시성의 관련성

  • 최병하 (용인정신병원 정신건강의학과) ;
  • 이유상 (용인정신병원 정신건강의학과) ;
  • 한은선 (용인정신병원 정신건강의학과) ;
  • 김성균 (한국과학기술원 바이오및뇌공학과) ;
  • 정재승 (한국과학기술원 바이오및뇌공학과) ;
  • 이승연 (세종대학교 수학통계학부) ;
  • 김범준 (서울아산병원 신경과)
  • Received : 2014.08.13
  • Accepted : 2014.09.30
  • Published : 2014.11.30
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Abstract

Objectives Prenatal testosterone is known to influence both cerebral laterality and 2nd to 4th digit ratio (2D : 4D). Epigenetic changes are thought to play some role in it. We studied sex-related differences between 2D : 4D and cerebral laterality in patients with schizophrenia and controls to examine the effects of prenatal testosterone in the development of schizophrenia. Methods Forty one men (18 schizophrenic patients and 23 controls) and 40 women (17 schizophrenic patients and 23 controls) were recruited from one psychiatric hospital in Korea. The 2D : 4D and electroencephalographic (EEG) coherence in 19 channels (66 pairs of interhemispheric coherence and 54 pairs of intrahemispheric coherence) were measured. The sex-related statistical analyses between 2D : 4D and EEG coherence in controls and patients with schizophrenia were performed using multiple regression. Results In male patients, the relationship between 2D : 4D and right intrahemispheric EEG coherence showed mainly positive correlation in delta and theta frequency bands, while it showed negative correlation in male controls. In female patients, the relationship between 2D : 4D and interhemispheric EEG coherence showed stronger positive correlation in alpha and beta frequency bands, while it showed weaker positive correlation in female controls. Conclusions Low prenatal testosterone may play certain roles in altered correlation between 2D : 4D and cerebral laterality in schizophrenia and the development of schizophrenia by epigenetic mechanism.

Keywords

References

  1. Rodenhiser D, Mann M. Epigenetics and human disease: translating basic biology into clinical applications. CMAJ 2006;174:341-348. https://doi.org/10.1503/cmaj.050774
  2. 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
  3. Petronis A. Human morbid genetics revisited: relevance of epigenetics. Trends Genet 2001;17:142-146. https://doi.org/10.1016/S0168-9525(00)02213-7
  4. 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
  5. Manning JT. Digit ratio: a pointer to fertility, behavior, and health. New Brunswick, NJ: Rutgers University Press;2002.
  6. 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
  7. Manning JT, Bundred PE. The ratio of 2nd to 4th digit length: a new predictor of disease predisposition? Med Hypotheses 2000;54:855-857. https://doi.org/10.1054/mehy.1999.1150
  8. Csatho A, Osvath A, Bicsak E, Karadi K, Manning J, Kallai J. Sex role identity related to the ratio of second to fourth digit length in women. Biol Psychol 2003;62:147-156. https://doi.org/10.1016/S0301-0511(02)00127-8
  9. Hampson E, Ellis CL, Tenk CM. On the relation between 2D:4D and sex-dimorphic personality traits. Arch Sex Behav 2008;37:133-144. https://doi.org/10.1007/s10508-007-9263-3
  10. Shin AY, Lee YS, Chae JH, Park JY, Kim SK, Lee SI, et al. A relationship between 2nd to 4th digit length ratio and aggression relatedsports entries characteristics in female athletics of Korean national teams. Korean J Biol Psychiatry 2010;17:44-48.
  11. Manning JT, Taylor RP. Second to fourth digit ratio and male ability in sport: implications for sexual selection in humans. Evol Hum Behav 2001;22:61-69. https://doi.org/10.1016/S1090-5138(00)00063-5
  12. Fink B, Grammer K, Mitteroecker P, Gunz P, Schaefer K, Bookstein FL, et al. Second to fourth digit ratio and face shape. Proc Biol Sci 2005;272:1995-2001. https://doi.org/10.1098/rspb.2005.3179
  13. Jeon SW, Kim SH, Oh DH, Lee YS, Lee SH. The correlation between 2nd to 4th digit length ratio and characteristics of temperament and character in university students. Korean J Biol Psychiatry 2010;17: 136-144.
  14. Stevenson JC, Everson PM, Williams DC, Hipskind G, Grimes M, Mahoney ER. Attention deficit/hyperactivity disorder (ADHD) symptoms and digit ratios in a college sample. Am J Hum Biol 2007;19: 41-50. https://doi.org/10.1002/ajhb.20571
  15. Han C, Lee YS, Hahm W, Won SD. The difference of the 2nd to 4th digit length ratio between type I and type II alcoholism. Korean J Biol Psychiatry 2011;18:260-266.
  16. 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
  17. Cho HW, Chae JH, Lee YS. The differences of 2nd to 4th digit length ratio between schizophrenia patients and normal controls. J Korean Neuropsychiatr Assoc 2009;48:496-501.
  18. Shaywitz BA, Shaywitz SE, Pugh KR, Constable RT, Skudlarski P, Fulbright RK, et al. Sex differences in the functional organization of the brain for language. Nature 1995;373:607-609. https://doi.org/10.1038/373607a0
  19. Toga AW, Thompson PM. Mapping brain asymmetry. Nat Rev Neurosci 2003;4:37-48. https://doi.org/10.1038/nrn1009
  20. 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
  21. Lust JM, Geuze RH, Van de Beek C, Cohen-Kettenis PT, Bouma A, Groothuis TG. Differential effects of prenatal testosterone on lateralization of handedness and language. Neuropsychology 2011;25: 581-589. https://doi.org/10.1037/a0023293
  22. 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
  23. 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
  24. Kim A, Kim S, Youn J, Jeong J, 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.
  25. Cardno AG, Marshall EJ, Coid B, Macdonald AM, Ribchester TR, Davies NJ, et al. Heritability estimates for psychotic disorders: the Maudsley twin psychosis series. Arch Gen Psychiatry 1999;56:162-168. https://doi.org/10.1001/archpsyc.56.2.162
  26. Jung HM, Lee YS, Kim S, Kim S, Jeong J, Oh JS, et al. Sex-related differences of EEG coherences between patients with schizophrenia and healthy controls. Korean J Biol Psychiatry 2013;20:166-178.
  27. 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
  28. 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
  29. Winterer G, Egan MF, Radler 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
  30. Kawasaki Y, Suzuki M, Takahashi T, Nohara S, McGuire PK, Seto H, et al. Anomalous cerebral asymmetry in patients with schizophrenia demonstrated by voxel-based morphometry. Biol Psychiatry 2008;63:793-800. https://doi.org/10.1016/j.biopsych.2007.08.008
  31. 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
  32. 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
  33. 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
  34. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR. 4th ed., text revision. Washington, DC: American Psychiatric Association;2000.
  35. 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
  36. McFadden D, Shubel E. Relative lengths of fingers and toes in human males and females. Horm Behav 2002;42:492-500. https://doi.org/10.1006/hbeh.2002.1833
  37. AutoMetric software for measurement of 2D:4D ratios [hompage on the Internet]. Glasgow: The Face Research Lab of the Institute of Neuroscience and Psychology at the University of Glasgow [cited 2012 Nov 23]. Available from: http://facelab.org/debruine/Programs/autometric.
  38. Hales RE, Yudofsky SC, Gabbard GO. The American Psychiatric Publishing textbook of psychiatry. Washington, DC: American Psychiatric Pub.;2008. p.1086.
  39. Sadock BJ, Kaplan HI, Sadock VA. Kaplan & Sadock's synopsis of psychiatry: behavioral sciences/clinical psychiatry. 10th ed. Philadelphia: Wolter Kluwer/Lippincott Williams & Wilkins;2007.
  40. Arato M, Frecska E, Beck C, An M, Kiss H. Digit length pattern in schizophrenia suggests disturbed prenatal hemispheric lateralization. Prog Neuropsychopharmacol Biol Psychiatry 2004;28:191-194. https://doi.org/10.1016/j.pnpbp.2003.09.020
  41. Leung A, Chue P. Sex differences in schizophrenia, a review of the literature. Acta Psychiatr Scand Suppl 2000;401:3-38.
  42. Aleman A, Kahn RS, Selten JP. Sex differences in the risk of schizophrenia: evidence from meta-analysis. Arch Gen Psychiatry 2003;60: 565-571. https://doi.org/10.1001/archpsyc.60.6.565
  43. Lee HK, Chou SP, Cho MJ, Park JI, Dawson DA, Grant BF. The prevalence and correlates of alcohol use disorders in the United States and Korea--a cross-national comparative study. Alcohol 2010;44:297-306. https://doi.org/10.1016/j.alcohol.2010.02.005
  44. Kornhuber J, Erhard G, Lenz B, Kraus T, Sperling W, Bayerlein K, et al. Low digit ratio 2D:4D in alcohol dependent patients. PLoS One 2011;6:e19332. https://doi.org/10.1371/journal.pone.0019332
  45. Walder DJ, Andersson TL, McMillan AL, Breedlove SM, Walker EF. Sex differences in digit ratio (2D:4D) are disrupted in adolescents with schizotypal personality disorder: altered prenatal gonadal hormone levels as a risk factor. Schizophr Res 2006;86:118-122. https://doi.org/10.1016/j.schres.2006.04.006
  46. Zhu YK, Li CB, Jin J, Wang JJ, Lachmann B, Sariyska R, et al. The 2D:4D ratio of the hand and schizotypal personality traits in schizophrenia patients and healthy control persons. Asian J Psychiatr 2014; 9:67-72. https://doi.org/10.1016/j.ajp.2014.01.005
  47. Okten A, Kalyoncu M, Yaris N. The ratio of second-and fourth-digit lengths and congenital adrenal hyperplasia due to 21-hydroxylase deficiency. Early Hum Dev 2002;70:47-54. https://doi.org/10.1016/S0378-3782(02)00073-7
  48. Manning JT, Bundred PE, Newton DJ, Flanagan BF. The second to fourth digit ratio and variation in the androgen receptor gene. Evol Hum Behav 2003;24:399-405. https://doi.org/10.1016/S1090-5138(03)00052-7
  49. Manning JT, Bundred PE, Flanagan BF. The ratio of 2nd to 4th digit length: a proxy for transactivation activity of the androgen receptor gene? Med Hypotheses 2002;59:334-336. https://doi.org/10.1016/S0306-9877(02)00181-0
  50. Cooke BM, Breedlove SM, Jordan CL. Both estrogen receptors and androgen receptors contribute to testosterone-induced changes in the morphology of the medial amygdala and sexual arousal in male rats. Horm Behav 2003;43:336-346. https://doi.org/10.1016/S0018-506X(02)00047-8
  51. 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
  52. 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
  53. 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
  54. Jausovec N, Jausovec K. EEG activity during the performance of complex mental problems. Int J Psychophysiol 2000;36:73-88. https://doi.org/10.1016/S0167-8760(99)00113-0
  55. Paul SN, Kato BS, Cherkas LF, Andrew T, Spector TD. Heritability of the second to fourth digit ratio (2d:4d): A twin study. Twin Res Hum Genet 2006;9:215-219. https://doi.org/10.1375/twin.9.2.215
  56. Gobrogge KL, Breedlove SM, Klump KL. Genetic and environmental influences on 2D:4D finger length ratios: a study of monozygotic and dizygotic male and female twins. Arch Sex Behav 2008;37:112-118. https://doi.org/10.1007/s10508-007-9272-2