Early hyperandrogenism affects the development of hippocampal function: Preliminary evidence from a functional magnetic resonance imaging study of boys with familial male precocious puberty

Journal of Child and Adolescent Psychopharmacology

Volumn 19, Issue 1, 2009, Pages 41-50

  Mueller, Sven C ^a   Mandell, Darcy ^a   Leschek, Ellen W ^b   Pine, Daniel S ^a   Merke, Deborah P ^c   Ernst, Monique ^a,d  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GONADOTROPIN; SEX HORMONE; TESTOSTERONE;

ADOLESCENT; AMYGDALOID NUCLEUS; ANXIETY; ARTICLE; BRAIN DEVELOPMENT; BRAIN FUNCTION; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; EMOTIONALITY; FACIAL EXPRESSION; FEAR; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HORMONE ACTION; HOSTILITY; HUMAN; HYPERANDROGENISM; MALE; NOSE; PRECOCIOUS PUBERTY; TESTOSTERONE RELEASE; THREAT;

ADOLESCENT; AGE OF ONSET; CHILD; EMOTIONS; FACIAL EXPRESSION; HIPPOCAMPUS; HUMANS; HYPERANDROGENISM; MAGNETIC RESONANCE IMAGING; MALE; PHOTIC STIMULATION; PUBERTY, PRECOCIOUS; REACTION TIME;

EID: 60749137154     PISSN: 10445463     EISSN: None     Source Type: Journal    
DOI: 10.1089/cap.2008.031     Document Type: Article

References (56)

1. Abdelgadir SE, Roselli CE, Choate JV, Resko JA: Androgen receptor messenger ribonucleic acid in brains and pituitaries of male rhesus monkeys: Studies on distribution, hormonal control, and relationship to luteinizing hormone secretion. Biol Reprod 60:1251-1256, 1999.
2. Bannerman DM, Deacon RM, Offen S, Friswell J, Grubb M, Rawlins JN: Double dissociation of function within the hippocampus: Spatial memory and hyponeophagia. Behav Neurosci 116:884-901, 2002.
3. Baron-Cohen S: The extreme male brain theory of autism. Trends Cogn Sci 6:248-254, 2002.
4. Beyenburg S, Watzka M, Clusmann H, Blumcke I, Bidlingmaier F, Elger CE, Stoffel-Wagner B: Androgen receptor mRNA expression in the human hippocampus. Neurosci Lett 294:25-28, 2000.
5. Booth A, Johnson DR, Granger DA: Testosterone and men's depression: The role of social behavior. J Health Soc Behav 40:130-140, 1999.
6. Charmandari E, Merke DP, Negro PJ, Keil MF, Martinez PE, Haim A, Gold PW, Chrousos GP: Endocrinologic and psychologic evaluation of 21-hydroxylase deficiency carriers and matched normal subjects: Evidence for physical and/or psychologic vulnerability to stress. J Clin Endocrinol Metab 89:2228-2236, 2004.
7. Cohen J: A power primer. Psycholog Bull 112:155-159, 1992.
8. Dohler KD, Coquelin A, Davis F, Hines M, Shryne JE, Gorski RA: Differentiation of the sexually dimorphic nucleus in the preoptic area of the rat brain is determined by the perinatal hormone environment. Neurosci Lett 33:295-298, 1982.
9. Edwards DE: Mice: Fighting by neonatally androgenized females. Science 161:1027-1028, 1968.
10. Ekman P, Friesen W: Pictures of facial affect. Palo Alto (California): Consulting Psychologists Press, 1976.
11. Ernst M, Maheu FS, Schroth E, Hardin J, Golan LG, Cameron J, Allen R, Holzer S, Nelson E, Pine DS, Merke DP: Amygdala function in adolescents with congenital adrenal hyperplasia: A model for the study of early steroid abnormalities. Neuropsychologia 45:2104-2113, 2007.
12. Friston KJ, Josephs O, Zarahn E, Holmes AP, Rouquette S, Poline J: To smooth or not to smooth? Bias and efficiency in fMRI time-series analysis. Neuroimage 12:196-208, 2000.
13. Gray J, McNaughton N: The Neuropsychology of Anxiety. Oxford, Oxford University Press, 2000.
14. Gur RC, Erwin RJ, Gur RE, Zwil AS, Heimberg C, Kraemer HC: Facial emotion discrimination: II. Behavioral findings in depression. Psychiatry Res 42:241-251, 1992.
15. Halasz J, Toth M, Mikics E, Hrabovszky E, Barsy B, Barsvari B, Haller J: The effect of neurokinin1 receptor blockade on territorial aggression and in a model of violent aggression. Biol Psychiatry 63:271-278, 2008.
16. Hines M, Fane BA, Pasterski VL, Mathews GA, Conway GS, Brook C: Spatial abilities following prenatal androgen abnormality: Targeting and mental rotations performance in individuals with congenital adrenal hyperplasia. Psychoneuroendocrinology 28:1010-1026, 2003.
17. Jacobsen L, Sapolsky R: The role of the hippocampus in feedback regulation of the hypothalamic- pituitary-adrenocortical axis. Endocr Rev 12:118-134, 1991.
18. Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P, Williamson D, Ryan N: Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36:980-988, 1997.
19. Laue L, Kenigsberg D, Pescovitz OH, Hench KD, Barnes KM, Loriaux DL, Cutler GB Jr.: Treatment of familial male precocious puberty with spironolactone and testolactone. N Engl J Med 320:496-502, 1989.
20. LeDoux JE: Emotion circuits in the brain. Annu Rev Neurosci 23:155-184, 2000.
21. Leschek EW: Familial male-limited precocious puberty. The Endocrinologist 14:148-151, 2004.
22. Maki PM, Ernst M, London ED, Mordecai KL, Perschler P, Durso SC, Brandt J, Dobs A, Resnick SM: Intramuscular testosterone treatment in elderly men: Evidence of memory decline and altered brain function. J Clin Endocrinol Metab 92:4107-4114, 2007.
23. Mazur T, Clopper RR: Pubertal disorders. Psychology and clinical management. Endocrinol Metab Clin North Am 20:211-230, 1991.
24. McClure EB, Monk CS, Nelson EE, Parrish JM, Adler A, Blair RJ, Fromm S, Charney DS, Leibenluft E, Ernst M, Pine DS: Abnormal attention modulation of fear circuit function in pediatric generalized anxiety disorder. Arch Gen Psychiatry 64:97-106, 2007.
25. Merke DP, Bornstein SR: Congenital adrenal hyperplasia. Lancet 365:2125-2136, 2005.
26. Merke DP, Fields JD, Keil MF, Vaituzis AC, Chrousos GP, Giedd JN: Children with classic congenital adrenal hyperplasia have decreased amygdala volume: Potential prenatal and postnatal hormonal effects. J Clin Endocrinol Metab 88:1760-1765, 2003.
27. Mueller SC, Temple V, Oh E, VanRyzin C, Williams A, Cornwell B, Grillon C, Pine DS, Ernst M, Merke D: Early androgen exposure modulates spatial cognition in congenital adrenal hyperplasia (CAH). Psychoneuroendocrinology 33:973-980, 2008.
28. Nakamura K, Kikusui T, Takeuchi Y, Mori Y: Changes in social instigation- and food restriction-induced aggressive behaviors and hippocampal 5HT1B mRNA receptor expression in male mice from early weaning. Behav Brain Res 187:442-448, 2008.
29. Nelson EE, McClure EB, Monk CS, Zarahn E, Leibenluft E, Pine DS, Ernst M: Developmental differences in neuronal engagement during implicit encoding of emotional faces: An event-related fMRI study. J Child Psychol Psychiatry 44:1015-1024, 2003.
30. Papez JW: A proposed mechanism of emotion. Arch Neurol Pathol 38:725-743, 1937.
31. Pasterski V, Hindmarsh P, Geffner M, Brook C, Brain C, Hines M: Increased aggression and activity level in 3- to 11-year-old girls with congenital adrenal hyperplasia (CAH). Horm Behav 52:368-374, 2007.
32. Peterson BS, Leckman JF, Scahill L, Naftolin F, Keefe D, Charest NJ, Cohen DJ: Steroid hormones and CNS sexual dimorphisms modulate symptom expression in Tourette's syndrome. Psychoneuroendocrinology 17:553-563, 1992.
33. Phelps EA: Human emotion and memory: Interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 14:198-202, 2004.
34. Pitkanen A, Pikkarainen M, Nurminen N, Ylinen A: Reciprocal connections between the amygdala and the hippocampal formation, perirhinal cortex, and postrhinal cortex in rat. A review. Ann NY Acad Sci 911:369-391, 2000.
35. Poletti CE, Sujatanond M: Evidence for a second hippocampal efferent pathway to hypothalamus and basal forebrain comparable to fornix system: A unit study in the awake monkey. J Neurophysiol 44:514-531, 1980.
36. Reinders AA, Glascher J, de Jong JR, Willemsen AT, den Boer JA, Buchel C: Detecting fearful and neutral faces: BOLD latency differences in amygdala-hippocampal junction. Neuroimage 33:805-814, 2006.
37. Resnick SM, Berenbaum SA, Gottesman II, Bouchard TJ: Early hormonal influences on cognitive functioning in congenital adrenal hyperplasia. Dev Psychol 22:191-198, 1986.
38. Rich BA, Vinton DT, Roberson-Nay R, Hommer RE, Berghorst LH, McClure EB, Fromm SJ, Pine DS, Leibenluft E: Limbic hyperactivation during processing of neutral facial expressions in children with bipolar disorder. Proc Natl Acad Sci USA 103:8900-8905, 2006.
39. Romeo RD: Puberty: A period of both organizational and activational effects of steroid hormones on neurobehavioural development. J Neuroendocrinol 15:1185-1192, 2003.
40. Rubinow DR, Schmidt PJ: Androgens, brain, and behavior. Am J Psychiatry 153:974-984, 1996.
41. Scoville WB, Milner B: Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11-21, 1957.
42. Shenker A, Laue L, Kosugi S, Merendino JJ Jr, Minegishi T, Cutler GB Jr: A constitutively activating mutation of the luteinizing hormone receptor in familial male precocious puberty. Nature 365:652-654, 1993.
43. Simerly RB, Chang C, Muramatsu M, Swanson LW: Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: An in situ hybridization study. J Comp Neurol 294:76-95, 1990.
44. Sisk CL, Foster DL: The neural basis of puberty and adolescence. Nature Neurosci 7:1040-1047, 2004.
45. Sonis WA, Comite F, Pescovitz OH, Hench K, Rahn CW, Cutler GB Jr, Loriaux DL, Klein RP: Biobehavioral aspects of precocious puberty. J Am Acad Child Psychiatry 25:674-679, 1986.
46. Sterzer P, Stadler C, Krebs A, Kleinschmidt A, Poustka F: Abnormal neural responses to emotional visual stimuli in adolescents with conduct disorder. Biol Psychiatry 57:7-15, 2005.
47. Stevens MC, Clark VP, Prestwood KM: Low-dose estradiol alters brain activity. Psychiatry Res 139:199-217, 2005.
48. Su TP, Pagliaro M, Schmidt PJ, Pickar D, Wolkowitz O, Rubinow DR: Neuropsychiatric effects of anabolic steroids in male normal volunteers. JAMA 269:2760-2764, 1993.
49. Surguladze S, Brammer MJ, Keedwell P, Giampietro V, Young AW, Travis MJ, Williams SC, Phillips ML: A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder. Biol Psychiatry 57:201-209, 2005.
50. Swanson LW, Cowan WM: An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49-84, 1977.
51. Szeszko PR, Robinson D, Alvir JM, Bilder RM, Lencz T, Ashtari M, Wu H, Bogerts B: Orbital frontal and amygdala volume reductions in obsessive-compulsive disorder. Arch Gen Psychiatry 56:913-919, 1999.
52. van Honk J, Peper JS, Schutter DJ: Testosterone reduces unconscious fear but not consciously experienced anxiety: Implications for the disorders of fear and anxiety. Biol Psychiatry 58:218-225, 2005.
53. Wechsler D: Wechsler Abbreviated Scale of Intelligence (WASI). San Antonio (Texas): Harcourt Assessment, 1999.
54. Weissenberger AA, Leschek EW, Zametkin AJ: Case study: Sexual hyperactivity treated with psychostimulants in familial male precocious puberty. J Am Acad Child Adolesc Psychiatry 40:373-376, 2001.
55. Wittchen HU, Nelson CB, Lachner G: Prevalence of mental disorders and psychosocial impairments in adolescents and young adults. Psychol Med 28:109-126, 1998.
56. Zarahn E, Aguirre GK, D'Esposito M: Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. Neuroimage 5:179-197, 1997.