Sexually dimorphic patterns of neural activity in response to juvenile social subjugation

Behavioural Brain Research

Volumn 256, Issue , 2013, Pages 464-471

  Weathington, Jill M ^a   Puhy, Chandler ^a   Hamki, Ali ^a   Strahan, J Alex ^a   Cooke, Bradley M ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Amygdala; Bed nucleus of the stria terminalis; Laterality; Paraventricular nucleus of the hypothalamus; Sex differences; Stress

Indexed keywords

PROTEIN FOS;

ADOLESCENT; AGGRESSION; AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL TISSUE; ANXIETY; ARTICLE; BASOLATERAL AMYGDALA; BRAIN NERVE CELL; BRAIN REGION; BRAIN SIZE; CELL COUNT; CONTROLLED STUDY; FEMALE; HEMISPHERIC DOMINANCE; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; JUVENILE SOCIAL SUBJUGATION; LEFT HEMISPHERE; MALE; NONHUMAN; PREPUBERTY; PRIORITY JOURNAL; SEX DIFFERENCE; SOCIAL ASPECT; STEREOLOGY; STRIA TERMINALIS;

AMYGDALA; BED NUCLEUS OF THE STRIA TERMINALIS; LATERALITY; PARAVENTRICULAR NUCLEUS OF THE HYPOTHALAMUS; SEX DIFFERENCES; STRESS;

AGGRESSION; AMYGDALA; ANIMALS; BRAIN; FEMALE; MALE; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; RATS; SEX CHARACTERISTICS; SOCIAL DOMINANCE;

EID: 84884293881     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.08.042     Document Type: Article

References (72)

1. Kessler R.C. Epidemiology of women and depression. J Affect Disord 2003, 74:5-13.
2. Tolin D.F., Foa E.B. Sex differences in trauma and posttraumatic stress disorder: a quantitative review of 25 years of research. Psychol Bull 2006, 132:959-992.
3. Nolen-Hoeksema S., Girgus J.S. The emergence of gender differences in depression during adolescence. Psychol Bull 1994, 115:424-443.
4. Widom C.S., DuMont K., Czaja S.J. A prospective investigation of major depressive disorder and comorbidity in abused and neglected children grown up. Arch Gen Psychiatry 2007, 64:49-56.
5. Kendler K.S., Karkowski L.M., Prescott C.A. Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 1999, 156:837-841.
6. De Bellis M.D., Baum A.S., Birmaher B., Keshavan M.S., Eccard C.H., Boring A.M., et al. A.E. Bennett research award. Developmental traumatology. Part I. Biological stress systems. Biol Psychiatry 1999, 45:1259-1270.
7. Tarullo A.R., Gunnar M.R. Child maltreatment and the developing HPA axis. Horm Behav 2006, 50:632-639.
8. MacMillan H.L., Fleming J.E., Streiner D.L., Lin E., Boyle M.H., Jamieson E., et al. Childhood abuse and lifetime psychopathology in a community sample. Am J Psychiatry 2001, 158:1878-1883.
9. Vigod S.N., Stewart D.E. Emergent research in the cause of mental illness in women across the lifespan. Curr Opin Psychiatry 2009, 22:396-400.
10. Bremner J.D., Vythilingam M., Anderson G., Vermetten E., McGlashan T., Heninger G., et al. Assessment of the hypothalamic-pituitary-adrenal axis over a 24-hour diurnal period and in response to neuroendocrine challenges in women with and without childhood sexual abuse and posttraumatic stress disorder. Biol Psychiatry 2003, 54:710-718.
11. Cicchetti D., Rogosch F.A. The impact of child maltreatment and psychopathology on neuroendocrine functioning. Dev Psychopathol 2002, 13:783-804.
12. Rind B., Tromovitch P., Bauserman R. A meta-analytic examination of assumed properties of child sexual abuse using college samples. Psychol Bull 1998, 124:22.
13. McClellan D., Farabee D., Crouch B. Early victimization, drug use, and criminality: a comparison of male and female prisoners. Crim Justice Behav 1997, 24:455-476.
14. Weathington J.M., Arnold A.R., Cooke B.M. Juvenile social subjugation induces a sex-specific pattern of anxiety and depression-like behaviors in adult rats. Horm Behav 2012, 61:91-99.
15. Bourke C.H., Neigh G.N. Behavioral effects of chronic adolescent stress are sustained and sexually dimorphic. Horm Behav 2011, 60:112-120.
16. Weathington J.M., Strahan J.A., Cooke B.M. Social experience induces sex-specific fos expression in the amygdala of the juvenile rat. Horm Behav 2012, 62:154-161.
17. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:1201-1213.
18. Lebow M., Neufeld-Cohen A., Kuperman Y., Tsoory M., Gil S., Chen A. Susceptibility to PTSD-like behavior is mediated by corticotropin-releasing factor receptor type 2 levels in the bed nucleus of the stria terminalis. J Neurosci 2012, 32:6906-6916.
19. Walker D.L., Miles L.A., Davis M. Selective participation of the bed nucleus of the stria terminalis and CRF in sustained anxiety-like versus phasic fear-like responses. Prog Neuropsychopharmacol Biol Psychiatry 2009, 33:1291-1308.
20. Sigurdsson T., Doyere V., Cain C.K., LeDoux J.E. Long-term potentiation in the amygdala: a cellular mechanism of fear learning and memory. Neuropharmacology 2007, 52:215-227.
21. Choi D.C., Furay A.R., Evanson N.K., Ulrich-Lai Y.M., Nguyen M.M.N., Ostrander M.M., et al. The role of the posterior medial bed nucleus of the stria terminalis in modulating hypothalamic-pituitary-adrenocortical axis responsiveness to acute and chronic stress. Psychoneuroendocrinology 2008, 33:659-669.
22. Swanson L.W. Brain maps structure of the rat brain 1992, Elsevier, New York.
23. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, Orlando. 4th ed.
24. Harris G., Levine J.E. Pubertal acceleration of pulsatile gonadotropin-releasing hormone release in male rats as revealed by microdialysis. Endocrinology 2003, 144:163-171.
25. Sisk C.L., Richardson H.N., Chappell P.E., Levine J.E. In vivo gonadotropin-releasing hormone secretion in female rats during peripubertal development and on proestrus. Endocrinology 2001, 142:2929-2936.
26. Cooke B.M., Woolley C.S. Sexually dimorphic organization of synapses in the medial amygdala. J Neurosci 2005, 25:10759-10767.
27. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 2003, 24:151-180.
28. Sawchenko P.E., Li H.Y., Ericsson A. Circuits and mechanisms governing hypothalamic responses to stress: a tale of two paradigms. Prog Brain Res 2000, 122:61-78.
29. Sterrenburg L., Gaszner B., Boerrigter J., Santbergen L., Bramini M., Roubos E.W., et al. Sex-dependent and differential responses to acute restraint stress of corticotropin-releasing factor-producing neurons in the rat paraventricular nucleus, central amygdala, and bed nucleus of the stria terminalis. J Neurosci Res 2012, 90:179-192.
30. Dalla C., Antoniou K., Kokras N., Drossopoulou G., Papathanasiou G., Bekris S., et al. Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiol Behav 2008, 93:595-605.
31. Goel N., Bale T.L. Sex differences in the serotonergic influence on the hypothalamic-pituitary-adrenal stress axis. Endocrinology 2010, 151:1784-1794.
32. Iwasaki-Sekino A., Mano-Otagiri A., Ohata H., Yamauchi N., Shibasaki T. Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats. Psychoneuroendocrinology 2009, 34:226-237.
33. Figueiredo H.F., Dolgas C.M., Herman J.P. Stress activation of cortex and hippocampus is modulated by sex and stage of estrus. Endocrinology 2002, 143:2534-2540.
34. Sagar S.M., Sharp F.R., Curran T. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 1988, 240:1328-1331.
35. Loughlin S.E., Islas M.I., Cheng M.Y., Lee A.G., Villegier A.S., Leslie F.M. Nicotine modulation of stress-related peptide neurons. J Comp Neurol 2006, 497:575-588.
36. van den Berg C.L., Hol T., Van Ree J.M., Spruijt B.M., Everts H., Koolhaas J.M. Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol 1999, 34:129-138.
37. Hermes G.L., Rosenthal L., Montag A., McClintock M.K. Social isolation and the inflammatory response: sex differences in the enduring effects of a prior stressor. Am J Physiol Regul Integr Comp Physiol 2006, 290:R273-R282.
38. Reyes B.A., Valentino R.J., Xu G., Van Bockstaele E.J. Hypothalamic projections to locus coeruleus neurons in rat brain. Eur J Neurosci 2005, 22:93-106.
39. Condes-Lara M. Different direct pathways of locus coeruleus to medial prefrontal cortex and centrolateral thalamic nucleus: electrical stimulation effects on the evoked responses to nociceptive peripheral stimulation. Eur J Pain 1998, 2:15-23.
40. McDonald A.J. Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 1991, 44:1-14.
41. Figueiredo H.F., Bruestle A., Bodie B., Dolgas C.M., Herman J.P. The medial prefrontal cortex differentially regulates stress-induced c-fos expression in the forebrain depending on type of stressor. Eur J Neurosci 2003, 18:2357-2364.
42. Davis M., Whalen P.J. The amygdala: vigilance and emotion. Mol Psychiatry 2001, 6:13-34.
43. Rubinow M.J., Juraska J.M. Neuron and glia numbers in the basolateral nucleus of the amygdala from preweaning through old age in male and female rats: a stereological study. J Comp Neurol 2009, 512:717-725.
44. Sullivan R.M., Duchesne A., Hussain D., Waldron J., Laplante F. Effects of unilateral amygdala dopamine depletion on behaviour in the elevated plus maze: role of sex, hemisphere and retesting. Behav Brain Res 2009, 205:115-122.
45. Giedd J.N., Vaituzis A.C., Hamburger S.D., Lange N., Rajapakse J.C., Kaysen D., et al. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. J Comp Neurol 1996, 366:223-230.
46. Cahill L., Haier R.J., White N.S., Fallon J., Kilpatrick L., Lawrence C., et al. Sex-related difference in amygdala activity during emotionally influenced memory storage. Neurobiol Learn Mem 2001, 75:1-9.
47. Geschwind N., Galaburda A.M. Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Arch Neurol 1985, 42:428-459.
48. Darlington C.L. The female brain. Conceptual advances in brain research 2002, vol. 6. Taylor & Francis, London; New York, p. 1 online resource (xii, 211 p.).
49. Roof R.L. The dentate gyrus is sexually dimorphic in prepubescent rats: testosterone plays a significant role. Brain Res 1993, 610:148-151.
50. Tabibnia G., Cooke B.M., Breedlove S.M. Sex difference and laterality in the volume of mouse dentate gyrus granule cell layer. Brain Res 1999, 827:41-45.
51. Holman S., Collado P. Postnatal cell proliferation and death in a lateralized, gender-related, asymmetric nucleus. J Neurobiol 2001, 47:150-158.
52. Gerendai I., Csaba Z., Vokó Z., Csernus V. Involvement of a direct neural mechanism in the control of gonadal functions. J Steroid Biochem Mol Biol 1995, 53:299-305.
53. Cooke B.M., Stokas M.R., Woolley C.S. Morphological sex differences and laterality in the prepubertal medial amygdala. J Comp Neurol 2007, 501:904-915.
54. Johnson R.T., Breedlove S.M., Jordan C.L. Sex differences and laterality in astrocyte number and complexity in the adult rat medial amygdala. J Comp Neurol 2008, 511:599-609.
55. Kolber B.J., Montana M.C., Carrasquillo Y., Xu J., Heinemann S.F., Muglia L.J., et al. Activation of metabotropic glutamate receptor 5 in the amygdala modulates pain-like behavior. J Neurosci 2010, 30:8203-8213.
56. Adamec R., Blundell J., Burton P. Role of NMDA receptors in the lateralized potentiation of amygdala afferent and efferent neural transmission produced by predator stress. Physiol Behav 2005, 86:75-91.
57. Baker K.B., Kim J.J. Amygdalar lateralization in fear conditioning: evidence for greater involvement of the right amygdala. Behav Neurosci 2004, 118:15-23.
58. Been L.E., Petrulis A. Dissociated functional pathways for appetitive and consummatory reproductive behaviors in male Syrian hamsters. Horm Behav 2012, 61:204-211.
59. Liu Y.C., Salamone J.D., Sachs B.D. Lesions in medial preoptic area and bed nucleus of stria terminalis: differential effects on copulatory behavior and noncontact erection in male rats. J Neurosci 1997, 17:5245-5253.
60. Martinez L.A., Petrulis A. The bed nucleus of the stria terminalis is critical for sexual solicitation, but not for opposite-sex odor preference, in female Syrian hamsters. Horm Behav 2011, 60:651-659.
61. Choi D.C., Furay A.R., Evanson N.K., Ostrander M.M., Ulrich-Lai Y.M., Herman J.P. Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J Neurosci 2007, 27:2025-2034.
62. Forger N.G., Rosen G.J., Waters E.M., Jacob D., Simerly R.B., de Vries G.J. Deletion of Bax eliminates sex differences in the mouse forebrain. Proc Natl Acad Sci USA 2004, 101:13666-13671.
63. Simerly R.B., Chang C., Muramatsu M., Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol 1990, 294:76-95.
64. Hines M., Allen L.S., Gorski R.A. Sex differences in subregions of the medial nucleus of the amygdala and the bed nucleus of the stria terminalis in the rat. Brain Res 1992, 579:321-326.
65. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, dorsomedial nucleus: implications for cerebral hemisphere integration of neuroendocrine, autonomic, and drinking responses. J Comp Neurol 2006, 494:75-107.
66. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, anteromedial area: cerebral hemisphere integration of neuroendocrine, autonomic, and behavioral aspects of energy balance. J Comp Neurol 2006, 494:142-178.
67. Heimer L., de Olmos J., Alheid G.F., Zaborszky L. "Perestroika" in the basal forebrain: opening the border between neurology and psychiatry. Prog Brain Res 1991, 87:109-165.
68. Alheid G.F., Heimer L. Theories of basal forebrain organization and the emotional motor system. Prog Brain Res 1996, 107:461-550.
69. Canteras N.S., Simerly R.B., Swanson L.W. Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 1995, 360:213-245.
70. Dong H.W., Swanson L.W. Projections from bed nuclei of the stria terminalis, posterior division: Implications for cerebral hemisphere regulation of defensive and reproductive behaviors. J Comp Neurol 2004, 471:396-433.
71. Bayless D.W., Darling J.S., Stout W.J., Daniel J.M. Sex differences in attentional processes in adult rats as measured by performance on the 5-choice serial reaction time task. Behav Brain Res 2012, 235:48-54.
72. Risbrough V.B., Hauger R.L., Roberts A.L., Vale W.W., Geyer M.A. Corticotropin-releasing factor receptors CRF1 and CRF2 exert both additive and opposing influences on defensive startle behavior. J Neurosci 2004, 24:6545-6552.