The effect of gonadectomy on prepulse inhibition and fear-potentiated startle in adolescent rhesus macaques

Psychoneuroendocrinology

Volumn 35, Issue 6, 2010, Pages 896-905

  Morris, Richard W ^a,b,c   Fung, Samantha J ^a,b,c   Rothmond, Debora A ^a,b,c,d   Richards, Brent ^d   Ward, Sarah ^d   Noble, Pamela L ^e   Woodward, Ruth A ^f   Weickert, Cynthia Shannon ^a,b,c,d   Winslow, James T ^e  

^a SCHIZOPHRENIA RESEARCH INSTITUTE   (Australia)

^b NEUROSCIENCE RESEARCH AUSTRALIA   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^e NIMH IRP Non Human Primate Core   (United States)

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

Author keywords

Estrogen; Preclinical; Puberty; Schizophrenia; Sensorimotor gating; Sex steroids; Testosterone

Indexed keywords

DOPAMINE; ESTRADIOL; LUTEINIZING HORMONE; TESTOSTERONE; TYROSINE 3 MONOOXYGENASE;

ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONDITIONING; CONTROLLED STUDY; DOPAMINE METABOLISM; FEAR POTENTIATED STARTLE; GONADECTOMY; HORMONE DETERMINATION; HORMONE RESPONSE; IMMUNOREACTIVITY; MALE; NONHUMAN; PREPULSE INHIBITION; PRIORITY JOURNAL; PUBERTY; PUTAMEN; STIMULUS RESPONSE; TESTOSTERONE BLOOD LEVEL;

AGE FACTORS; ANIMALS; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; FEAR; GONADS; INHIBITION (PSYCHOLOGY); MACACA MULATTA; MALE; PREFRONTAL CORTEX; PUBERTY; PUTAMEN; STARTLE REACTION; TESTOSTERONE; TYROSINE 3-MONOOXYGENASE;

EID: 77953023812     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2009.12.002     Document Type: Article

References (59)

1. Blumenthal T.D., Elden A., Flaten M.A. A comparison of several methods used to quantify prepulse inhibition of eyeblink responding. Psychophysiology 2004, 41:326-332.
2. Braff D.L., Geyer M.A., Swerdlow N.R. Human studies of prepulse inhibition of startle: normal subjects, patient groups and pharmacological studies. Psychopharmacology 2001, 156:234-258.
3. Gogos A., van den Buuse M. Castration reduces the effect of serotonin-1A receptor stimulation on prepulse inhibition in rats. Behav. Neurosci. 2003, 117:1407-1415.
4. Casey B.J., Jones R.M., Hare T.A. The adolescent brain. Ann. N. Y. Acad. Sci. 2008, 1124:111-126.
5. Christie K.A., Burke J.D., Regier D.A., Rae D.S., Boyd J.H., Locke B.Z. Epidemiologic evidence for early onset of mental disorders and higher risk of drug abuse in young adults. Am. J. Psychiatry 1988, 145:971-975.
6. Cossette M., Levesque D., Parent A. Neurochemical characterization of dopaminergic neurons in human striatum. Parkinsonism Relat. Dis. 2005, 11:277-286.
7. Davis M., Antoniadis E.A., Amaral D.G., Winslow J.T. Acoustic startle reflex in rhesus monkeys: a review. Rev. Neurosci. 2008, 19:171-185.
8. Ellwanger J., Geyer M.A., Braff D.L. The relationship of age to prepulse inhibition and habituation of the acoustic startle response. Biol. Psychol. 2003, 62:175-195.
9. Galvan A., Hare T.A., Parra C.E., Penn J., Voss H.U., Glover G.H., Casey B.J. Earlier development of the accumbens relative to orbitofrontal cortex might underlie risk-taking behavior in adolescents. J. Neurosci. 2006, 26:6885-6892.
10. Gattaz W.F., Vogel P., Riecher-Rossler A., Soddu G. Influence of the menstrual cycle phase on the therapeutic response in schizophrenia. Biol. Psychiatry 1994, 36:137-139.
11. Geyer M.A., Braff D.L. Startle habituation and sensorimotor gating in schizophrenia and related animal models. Schizophr. Bull. 1987, 13:643-668.
12. Grillon C., Warner V., Hille J., Merikangas K.R., Bruder G.E., Tenke C.E., Nomura Y., Leite P., Weissman M.M. Families at high and low risk for depression: a three-generation study. Biol. Psychiatry 2005, 57:953-960.
13. Hafner H. Gender differences in schizophrenia. Psychoneuroendocrinology 2003, 28(Suppl. 2):17-54.
14. Hallonquist J.D., Seeman M.V., Lang M., Rector N.A. Variation in symptom severity over the menstrual cycle of schizophrenics. Biol. Psychiatry 1993, 33:207-209.
15. Haycock J.W., Becker L., Ang L., Furukawa Y., Hornykiewicz O., Kish S.J. Marked disparity between age-related changes in dopamine and other presynaptic dopaminergic markers in human striatum. J. Neurochem. 2003, 87:574-585.
16. Hendrick V., Altshuler L.L., Burt V.K. Course of psychiatric disorders across the menstrual cycle. Harv. Rev. Psychiatry 1996, 4:200-207.
17. Jeong H., Kim M.S., Kwon J., Kim K.S., Seol W. Regulation of the transcriptional activity of the tyrosine hydroxylase gene by androgen receptor. Neurosci. Lett. 2006, 396:57-61.
18. Jovanovic T., Szilagyi S., Chakravorty S., Fiallos A.M., Lewison B.J., Parwani A., Schwartz M.P., Gonzenbach S., Rotrosen J.P., Duncan E.J. Menstrual cycle phase effects on prepulse inhibition of acoustic startle. Psychophysiology 2004, 41:401-406.
19. Karper L.P., Freeman G.K., Grillon C., Morgan C.A., Charney D.S., Krystal J.H. Preliminary evidence of an association between sensorimotor gating and distractability in psychosis. J. Neuropsychiatry Clin. Neurosci. 1996, 8:60-66.
20. Kaushik P., Gorin F., Vali S. Dynamics of tyrosine hydroxylase mediated regulation of dopamine synthesis. J. Comput. Neurosci. 2007, 22:147-160.
21. Kendell R.E., Chalmers J.C., Platz C. Epidemiology of puerperal psychoses. Br. J. Psychiatry 1987, 150:662-673.
22. Ko Y.H., Jung S.W., Joe S.H., Lee C.H., Jung H.G., Jung I.K., Kim S.H., Lee M.S. Association between serum testosterone levels and the severity of negative symptoms in male patients with chronic schizophrenia. Psychoneuroendocrinology 2007, 32:385-391.
23. Koch M. Sensorimotor gating changes across the estrous cycle in female rats. Physiol. Behav. 1998, 64:625-628.
24. Kritzer M.F., Kohoma S.G. Ovarian hormones influence the morphology, distribution and density of tyrosine hydroxylase immunoreactive axons in the dorsolateral prefrontal cortex of adult rhesus monkeys. J. Comp. Neurol. 1998, 395:1-17.
25. Kulkarni J., de Castella A., Fitzgerald P.B., Gurvich C.T., Bailey M., Bartholomeusz C., Burger H. Estrogen in severe mental illness: a potential new treatment approach. Arch. Gen. Psychiatry 2008, 65:955-960.
26. Kulkarni J., de Castella A., Smith D., Taffe J., Keks N., Copolov D. A clinical trial of the effects of estrogen in acutely psychotic women. Schizophr. Res. 1996, 20:247-252.
27. Kulkarni J., Riedel A., de Castella A.R., Fitzgerald P.B., Rolfe T.J., Taffe J., Burger H. Estrogen-a potential treatment for schizophrenia. Schizophr. Res. 2001, 48:137-144.
28. Kulkarni J., Riedel A., de Castella A.R., Fitzgerald P.B., Rolfe T.J., Taffe J., Burger H. A clinical trial of adjunctive oestrogen treatment in women with schizophrenia. Arch. Women Ment. Health 2002, 5:99-104.
29. Leranth C., Roth R.H., Elsworth J.D., Naftolin F., Horvath T.L., Redmond D.E.J. Estrogen is essential for maintaining nigrostriatal dopamine neurons in primates: implications for Parkinson's disease and memory. J. Neurosci. 2000, 20:86404-86409.
30. Lewis D.A., Foote S.L., Goldstein M., Morrison J.H. The dopaminergic innervation of monkey prefrontal cortex: a tyrosine hydroxylase immunohistochemical study. Brain Res. 1988, 449:225-243.
31. Ludewig K., Geyer M.A., Vollenweider F.X. Deficits in prepulse inhibition and habituation in never-medicated, first-episode schizophrenia. Biol. Psychiatry 2003, 54:121-128.
32. Martinez Z.A., Platten A., Pollack E., Shoemaker J., Ro H., Pitcher L., Geyer M.A., Swerdlow N.R. " Typical" but not " atypical" antipsychotic effects on startle gating deficits in prepubertal rats. Psychopharmacology (Berl.) 2002, 161:38-46.
33. Melchitzky D.S., Lewis D.A. Tyrosine hydroxylase- and dopamine transporter-immunoreactive axons in the primate cerebellum. Evidence for a lobular- and laminar-specific dopamine innervation. Neuropsychopharmacology 2000, 22:466-472.
34. Meng S.Z., Ozawa Y., Masayuki I., Takashima S. Developmental and age-related changes of dopamine transporter, and dopamine D1 and D2 receptors in human basal ganglia. Brain Res. 1999, 843:136-144.
35. Montague D.M., Lawler C.P., Mailman R.B., Gilmore J.H. Developmental regulation of the dopamine D1 receptor in human caudate and putamen. Neuropsychopharmacology 1999, 21:641-649.
36. Morgan C.A.R., Grillon C., Southwick S.M., Davis M., Charney D.S. Fear-potentiated startle in posttraumatic stress disorder. Biol. Psychiatry 1995, 15:378-385.
37. Muller J.F., Mascagni F., McDonald A.J. Dopaminergic innervation of pyramidal cells in the rat basolateral amygdala. Brain Struct. Funct. 2009, 213:275-288.
38. Ornitz E.M., Guthrie D., Kaplan A.R., Lane S.J., Norman R.J. Maturation of startle modulation. Psychophysiology 1986, 23:624-634.
39. Paxinos G., Xu-Feng H., Petrides M., Toga A.W. The Rhesus Monkey Brain In Stereotaxic Coordinates 2000, Elsevier, London.
40. Perlman W.R., Matsumoto M., Beltaifa S., Hyde T.M., Saunders R.C., Webster M.J., Rubinow D.R., Kleinman J.E., Weickert C.S. Expression of estrogen receptor alpha exon-deleted mRNA variants in the human and non-human primate frontal cortex. Neuroscience 2005, 134:81-95.
41. Perlman W.R., Tomaskovic-Crook E., Montague D.M., Webster M.J., Rubinow D.R., Kleinman J.E., Weickert C.S. Alteration in estrogen receptor alpha mRNA levels in frontal cortex and hippocampus of patients with major mental illness. Biol. Psychiatry 2005, 58:812-824.
42. Perry W., Braff D.L. Information-processing deficits and thought disorder in schizophrenia. Am. J. Psychiatry 1994, 151:363-367.
43. Perry W., Minassian A., Feifel D. Prepulse inhibition in patients with non-psychotic major depressive disorder. J. Affect. Disord. 2004, 81:179-184.
44. Plant T.M. The male monkey as a model for the study of the neurobiology of puberty onset in man. Mol. Cell Endocrinol. 2006, 254-255:97-102.
45. Quednow B.B., Westheide J., Kuhn K.U., Werner P., Maier W., Hawellek P., Wagner M. Normal prepulse inhibition and habituation of acoustic startle response in suicidal depressive patients without psychotic symptoms. J. Affect. Disord. 2006, 92:299-303.
46. Raab H., Pilgrim C., Reisert I. Effects of sex and estrogen on tyrosine hydroxylase mRNA in cultured embryonic rat mesencephalon. Brain Res. Mol. Brain Res. 1995, 33:157-164.
47. Richards A.B., Morris R.W., Ward S., Schmitz S., Rothmond D.A., Noble P.L., Woodward R.A., Winslow J.T., Weickert C.S. Gonadectomy negatively impacts social behavior of adolescent male primates. Horm. Behav. 2009.
48. Riecher-Rossler A., Hafner H., Dutsch-Strobel A., Oster M., Stumbaum M., van Gulick-Bailer M., Loffler W. Further evidence for a specific role of estradiol in schizophrenia?. Biol. Psychiatry 1994, 36:492-494.
49. Seeman M.V. Schizophrenia, gender, and affect. Can. J. Psychiatry 1996, 41:263-264.
50. Seeman M.V., Lang M. The role of estrogens in schizophrenia gender differences. Schizophr. Bull. 1990, 16:185-194.
51. Toufexis D.J., Myers K.M., Davis M. The effect of gonadal hormones and gender on anxiety and emotional learning. Horm. Behav. 2006, 50:539-549.
52. Usall J., Busquets E., Araya S., Ochoa S., Gost A. Gender differences in schizophrenia. A literature review. Actas Espanolas Psiquiatria 2000, 28:178-185.
53. van den Buuse M., Eikelis N. Estrogen increases prepulse inihibition of acoustic startle in rats. Eur. J. Pharmacol. 2001, 425:33-41.
54. van den Buuse M., Simpson E.R., Jones M.E. Prepulse inhibition of acoustic startle in aromatase knock-out mice: effects of age and gender. Genes Brain Behav. 2003, 2:93-102.
55. Walker D.L., Davis M. Quantifying fear potentiated startle using absolute versus proportional increase scoring methods: implications for the neurocircuitry of fear and anxiety. Psychopharmacology 2002, 164:318-328.
56. Weickert C.S., Miranda-Angulo A.L., Wong J., Perlman W.R., Ward S.E., Radhakrishna V., Straub R.E., Weinberger D.R., Kleinman J.E. Variants in the estrogen receptor alpha gene and its mRNA contribute to risk for schizophrenia. Hum. Mol. Genet. 2008, 17:2293-2309.
57. Weickert C.S., Webster M.J., Gondipalli P., Rothmond D., Fatula R.J., Herman M.M., Kleinman J.E., Akil M. Postnatal alterations in dopaminergic markers in the human prefrontal cortex. Neuroscience 2007, 144:1109-1119.
58. Winslow J.T., Noble P.L., Davis M. Modulation of fear-potentiated startle and vocalizations in juvenile rhesus monkeys by morphine, diazepam, and buspirone. Biol. Psychiatry 2007, 61:389-395.
59. Winslow J.T., Parr L.A., Davis M. Acoustic startle, prepulse inhibition and fear-potentiated startle measured in Rhesus monkeys. Biol. Psychiatry 2002, 51:859-866.