Neonatal amygdala lesions alter basal cortisol levels in infant rhesus monkeys

Psychoneuroendocrinology

Volumn 38, Issue 6, 2013, Pages 818-829

  Raper, Jessica ^a   Bachevalier, Jocelyne ^a   Wallen, Kim ^a   Sanchez, Mar ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amygdala; HPA axis; Sex difference; Testosterone

Indexed keywords

HYDROCORTISONE; TESTOSTERONE;

ADULT ANIMAL; AGE; AMYGDALECTOMY; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN SURGERY; CIRCADIAN RHYTHM; CONTROLLED STUDY; CORRELATION ANALYSIS; HYDROCORTISONE BLOOD LEVEL; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; MOTHER; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RHESUS MONKEY; SEX DIFFERENCE; TESTOSTERONE BLOOD LEVEL;

AMYGDALA; ANIMALS; ANIMALS, NEWBORN; CIRCADIAN RHYTHM; FEMALE; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MACACA MULATTA; MALE; PITUITARY-ADRENAL SYSTEM; SEX CHARACTERISTICS; TESTOSTERONE;

EID: 84877043243     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2012.09.004     Document Type: Article

References (54)

1. Allen J.P., Allen C.F. Amygdalar participation in tonic ACTH section in the rat. Neuroendocrinology 1975, 19:115-125.
2. Anand K.J.S., Aynsley-Green A. Measuring the severity of surgical stress in newborn infants. J. Pediatr. Surg. 1988, 23:297-305.
3. Barrett C.E., Noble P., Hanson E., Pine D.S., Winslow J.T., Nelson E.E. Early adverse rearing experiences alter sleep-wake patterns and plasma cortisol levels in juvenile rhesus monkeys. Psychoneuroendocrinology 2009, 34:1029-1040.
4. Boas M., Boisen K.A., Virtanen H.E., Kaleva M., Suomi A.-M., Schmidt I.M., Damgaard I.N., Kai C.M., Chellakooty M., Skakkebaek N.S., Toppari J., Main K.M. Postnatal penile length and growth rate correlate to serum testosterone levels: a longitudinal study of 1962 normal boys. Eur. J. Endocrinol. 2006, 154:125-129.
5. Bouvattier C., Carel J.-C., Lecointre C., David A., Sultan C., Bertrand A.-M., Morel Y., Chaussain J.-L. Postnatal changes in T, LH, and FSH in 46,XY infants with mutations in the AR gene. J. Clin. Endocrinol. Metab. 2002, 87:29-32.
6. Boyce W.T., Champoux M., Suomi S.J., Gunnar M.R. Salivary cortisol in nursery-reared rhesus monkeys: reactivity to peer interactions and altered circadian activity. Dev. Psychobiol. 1995, 28:257-267.
7. Burgess L.H., Handa R.J. Chronic estrogen-induced alteration in adrenocorticotropin and corticosterone secretion, and glucocorticoid receptor-mediated functions in female rats. Endocrinology 1992, 131:1261-1269.
8. Capitanio J.P., Mendoza S.P., Mason W.A., Maninger N. Rearing environment and hypothalamic-pituitary-adrenal regulation in young rhesus monkeys (Macaca mulatta). Dev. Psychobiol. 2005, 46:318-330.
9. Champoux M., Coe C.L., Schanberg S.M., Kuhn C.M., Suomi S.J. Hormonal effects of early rearing conditions in the infant rhesus monkey. Am. J. Primatol. 1989, 19:111-117.
10. Choate J.V., Slayden O.D., Resko J.A. Immunocytochemical localization of androgen receptors in brains of developing and adult male rhesus monkeys. Endocrine 1998, 8:51-60.
11. Clarke A.S. Social rearing effects on HPA axis activity over early development and in response to stress in rhesus monkeys. Dev. Psychobiol. 1993, 26:433-446.
12. Conley A.J., Bernstein R.M., Nguyen A.D. Adrenarche in nonhuman primates: the evidence for it and the need to redefine it. J. Endocrinol. 2012, 214:121-131.
13. Conley A.J., Moeller B.C., Nguyen A.D., Stanley S.D., Plant T.M., Abbott D.H. Defining adrenarche in the rhesus macaque (Macaca mulatta), a non-human primate model for adrenal androgen secretion. Mol. Cell. Endocrinol. 2011, 336:110-116.
14. Conley A.J., Plant T.M., Abbott D.H., Moeller B.C., Stanley A.D.S.D. Adrenal androgen concentrations increase during infancy in male rhesus macaques (Macaca mulatta). Am. J. Physiol. Endocrinol. Metab. 2011, 301:E1229-E1235.
15. Davis M., Emory E. Sex differences in neonatal stress reactivity. Child Dev. 1995, 66:14-27.
16. Elmlinger M.W., Kühnel W., Ranke M.B. Reference ranges for serum concentrations of lutropin (LH), follitropin (FSH), estradiol (E2), prolactin, progesterone, sex hormone-binding globulin (SHBG), dehydroepiandrosterone sulfate (DHEAS), cortisol, and ferritin in neonates, children and young adults. Clin. Chem. Lab. Med. 2002, 40:1151-1160.
17. Essex M.J., Klein M.H., Cho E., Kalin N.H. Maternal stress beginning in infancy may sensitize children to later stress exposure: effects on cortisol and behavior. Biol. Psychiatry 2002, 52:776-784.
18. Forest M.G. Plasma androgens (testosterone and 4-androstenedione) and 17-hydroxyprogesterone in the neonatal, prepubertal, and peripubertal periods in the human and the rat: differences between species. J. Steroid Biochem. 1979, 11:543-548.
19. Freese J.L., Amaral D.G. Neuroanatomy of the primate amygdala. The Human Amygdala 2009, 1-42. Gilford Press, Inc., New York. P.J. Whalen, E.A. Phelps (Eds.).
20. Geoffroy M.-C., Côté S.M., Parent S., Séguin J.R. Daycare attendance, stress, and mental health. Can. J. Psychiatry 2006, 51:607-615.
21. Goursaud A-P.S., Mendoza S.P., Capitanio J.P. Do neonatal bilateral ibotenic acid lesions of the hippocampal formation or of the amygdala impair HPA axis responsiveness and regulation in infant rhesus macaques (Macaca mulatta)?. Brain Res. 2006, 1071:97-104.
22. Gunnar M.R., Kryzer E., Van Ryzin M.J., Phillips D.A. The import of the cortisol rise in child care differs as a function of behavioral inhibition. Dev. Psychol. 2011, 47:792-803.
23. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., Cullinan W.E. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front. Neuroendocrinol. 2003, 24:151-180.
24. Higley J.D., Suomi S.J., Linnoila M. A longitudinal assessment of CSF monoamine metabolite and plasma cortisol concentrations in young rhesus monkeys. Biol. Psychiatry 1992, 32:127-145.
25. Jonetz-Mentzel L., Wiedemann G. Establishment of reference ranges for cortisol in neonates, infants, children, and adolescents. Eur. J. Clin. Chem. Clin. 1993, 31:525-529.
26. Kalin N.H., Shelton S.E., Davidson R.J. The role of the central nucleus of the amygdala in mediating fear and anxiety in the primate. J. Neurosci. 2004, 24:5506-5515.
27. Knutsson U., Dahlgren J., Marcus C., Rosberg S., Brönnegard M., Stierna P., Albertsson-Wikland K. Circadian cortisol rhythm in healthy boys and girls: relationship with age, growth, body composition, and pubertal development. J. Clin. Endocrinol. Metab. 1997, 82:536-540.
28. Koupil I., Mann V., Leon D.A., Lundberg U., Byberg L., Vågerö D. Morning cortisol does not mediate the association of size at birth with blood pressure in children born from full-term pregnancies. Clin. Endocrinol. 2005, 62:661-666.
29. Larson M.C., White B.P., Chochran A., Donzella B., Gunnar M. Dampening of the cortisol response to handling at 3 months in human infants and its relation to sleep, circadian cortisol activity, and behavioral distress. Dev. Psychobiol. 1998, 33:327-337.
30. Machado C.J., Bachevalier J. Behavioral and hormonal reactivity to threat: effects of selective amygdala, hippocampal, or orbital frontal lesions in monkeys. Psychoneuroendocrinology 2008, 33:926-941.
31. Mann D.R., Gould K.G., Collins D.C., Wallen K. Blockade of neonatal activation of the pituitary-testicular axis: effect on peripubertal luteinizing hormone and testosterone secretion and on testicular development in male monkeys. J. Clin. Endocrinol. Metab. 1989, 68:600-607.
32. Mason J.W. Plasma 17-hydroxycorticosteroid levels during electrical stimulation of the amygdaloid complex in conscious monkeys. Am. J. Physiol. 1959, 196:44-48.
33. McCormack K., Newman T.K., Higley J.D., Maestripieri D., Sanchez M.M. Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Horm. Behav. 2009, 55:538-547.
34. Nemanic S., Alvarado M.C., Price R.E., Jackson E.F., Bachevalier J. Assessment of locus and extent of neurotoxic lesions in monkeys using neuroimaging techniques: a replication. J. Neurosci. Methods 2002, 121:199-209.
35. Netherton C., Goodyer I., Tamplin A., Herbert J. Salivary cortisol and dehydroepiandrosterone in relations to puberty and gender. Psychoneuroendocrinology 2004, 29:125-140.
36. Norman R.L., Spies H.G. Brain lesions in infant female rhesus monkeys: effects on menarche and first ovulation and on diurnal rhythms of prolactin and cortisol. Endocrinology 1981, 108:1723-1729.
37. Ouellet-Morin I., Tremblay R.E., Boivin M., Meaney M., Kramer M., Côté S.M. Diurnal cortisol secretion at home and in child care: a prospective study of 2-year-old toddlers. J. Child Psychol. Psychiatry 2010, 51:295-303.
38. Pomerantz S.M., Sholl S.A. Analysis of sex and regional differences in androgen receptors in fetal rhesus monkey brain. Dev. Brain Res. 1987, 36:151-154.
39. Raper, J., Wilson, M., Sanchez, M., Machado, C., Bachevalier, J., 2012. Pervasive alterations of emotional and neuroendocrine responses to an acute stressor after neonatal amygdala lesions in rhesus monkeys. Psychoneuroendocrinology,. doi:10.1016/j.psyneuen.2012.10.008.
40. Regev L., Tsoory M., Gil S., Chen A. Site-specific genetic manipulation of amygdala corticotropin-releasing factor reveals its imperative role in mediating behavioral response to challenge. Biol. Psychiatry 2012, 71:317-326.
41. Robinson J.A., Bridson W.E. Neonatal hormone patterns in the macaque. I. Steroids. Biol. Reprod. 1978, 19:773-778.
42. Sapolsky R.M., Zola-Morgan S., Squire L.R. Inhibition of glucocorticoid secretion by the hippocampal formation in the primate. J. Neurosci. 1991, 11:3695-3704.
43. Sanchez M.M., McCormack K., Grand A.P., Fulks R., Graff A., Maestripieri D. Effects of sex and early maternal abuse on adrenocorticotropin hormone and cortisol responses to the corticotrophin-releasing hormone challenge during the first 3 years of life in group-living rhesus monkeys. Dev. Psychopathol. 2010, 22:45-53.
44. Sanchez M.M., Noble P.M., Lyon C.K., Plotsky P.M., Davis M., Nemeroff C.B., Winslow J.T. Alterations in diurnal cortisol rhythm and acoustic startle response in nonhuman primates with adverse rearing. Biol. Psychiatry 2005, 57:373-381.
45. Seale J.V., Wood S.A., Atkinson H.C., Harbuz M.S., Lightman S.L. Gonadal steroid replacement reverses gonadectomy-induced changes in the corticosterone pulse profile and stress-induced hypothalamic-pituitary-adrenal axis activity of male and female rats. J. Neuroendocrinol. 2004, 16:989-998.
46. Smith C.J., Norman R.L. Circadian periodicity in circulating cortisol is absent after orchidectomy in rhesus macaques. Endocrinology 1987, 121:2186-2191.
47. Sondeijker F.E.P.L., Ferdinand R.F., Oldehinkel A.J., Veenstra R., Tiemeier H., Ormel J., Verhulst F.C. Disruptive behaviors and HPA-axis activity in young adolescent boys and girls from the general population. J. Psychiatr. Res. 2007, 41:570-578.
48. Stavisky R.C., Waston S.L., Anthony M.S., Manuck S.B., Adams M.R., Kaplan J.R. Influence of estradiol on cortisol secretion in ovariectomized cynomologus macaques (Macaca fascicularis). Am. J. Primatol. 2003, 60:17-22.
49. Tarullo A.R., Gunnar M.R. Child maltreatment and the developing HPA axis. Horm. Behav. 2006, 50:632-639.
50. Watamura S.E., Donzella B., Kertes D.A., Gunnar M.R. Developmental changes in baseline cortisol activity in early childhood: relations with napping and effortful control. Dev. Psychobiol. 2004, 45:125-133.
51. Wallen K., Maestripieri D., Mann D.R. Effects of neonatal testicular suppression with a GnRH antagonists on social behavior in group-living juvenile rhesus monkeys. Horm. Behav. 1995, 29:322-337.
52. Weisz J., Ward I.L. Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology 1980, 106:306-316.
53. Wilson M.E., Gordon T.P., Collins D.C. Ontogeny of lutenizing hormone secretion and first ovulation in seasonal breeding rhesus monkeys. Endocrinology 1986, 118:293-301.
54. Wolfram M., Bellingrath S., Kudielka B.M. The cortisol awakening response (CAR) across the female menstrual cycle. Psychoneuroendocrinology 2011, 36:905-912.