Maternal separation and lesion of adtn alters anxiety and adrenal activity in male rats

International Journal of Neuroscience

Volumn 119, Issue 9, 2009, Pages 1319-1336

  Esquivel, Brbara Brcena ^a   Levin, Gloria ^b   Rivarola, Mara Anglica ^a   Surez, Marta Magdalena ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b Centro de Investigaciones Endocrinologicas   (Argentina)

Author keywords

ACTH; ADTN; Anxiety; Catecholamines; Corticosterone; Maternal separation

Indexed keywords

CATECHOLAMINE; CORTICOSTERONE; CORTICOTROPIN; NORADRENALIN;

ADRENAL GLAND; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN DAMAGE; CATECHOLAMINE BLOOD LEVEL; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; FEMALE; HISTOPATHOLOGY; MALE; MATERNAL DEPRIVATION; NONHUMAN; NORADRENALIN BLOOD LEVEL; RAT; THALAMUS NUCLEUS;

ADRENAL GLANDS; ADRENOCORTICOTROPIC HORMONE; ANIMALS; ANIMALS, NEWBORN; ANTERIOR THALAMIC NUCLEI; ANXIETY; BEHAVIOR, ANIMAL; EPINEPHRINE; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; MATERNAL DEPRIVATION; MEDULLA OBLONGATA; NOREPINEPHRINE; RATS; SYMPATHETIC NERVOUS SYSTEM;

EID: 70350455922     PISSN: 00207454     EISSN: 15635279     Source Type: Journal    
DOI: 10.1080/00207450902931847     Document Type: Article

References (53)

1. Aguilera, G., Hauger, R. L., Pharwood, J. P., Millan, M., & Catt, K. J. (1989). CRF receptors in the pituitary and nervous system: Effects of Stress. In G. Van Loon, R. Kvetnasky, R. Mc Carty, and J. Axelrod (eds.), Stress: neurochemical and humoral mechanisms (Vol. 1) (pp 223-236). New York: Gordon and Breach Science Publishing.
2. Boccia, M. I., & Pedersen, C. A. (2001). Brief vs. long maternal separation in infancy: contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety. Psychoneuroendocrinology, 26, 657-672.
3. Cahill, L. (2006). Why sex matters for neuroscience. Nature Reviews Neuroscience, 7, 477-484.
4. Caldji, C., Francis, D., Sharma, S., Plotsky, P. M., & Meaney, M. J. (2000). The effects of early rearing environment on the development of GABAA and central benzodiacepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology, 22, 219-229.
5. Cirulli, F., Santucci, D., Laviola, G., Alleva, E., & Levine, S. (1994). Behavioral and hormonal responses to stress in the newborn mouse: effects ofmaternal deprivation and chlordiazepoxide. Developmental Psychobiology, 27, 301-316.
6. Eisenhofer, G., Goldstein, D. S., Stull, R., Keiser, H. R. Sunderland, T. Murphy, D. L., et al. (1986). Simultaneous liquid chromatographic determination of 3,4-dihydroxyphenylglycol, catecholamines and 3,4-dihydroxy-phenylalanine in plasma, and their responses to inhibition of monoamine oxidase. Clinical Chemistry, 32, 2030-2032.
7. Ellenbroek, B. A., & Riva, M. A. (2003). Early maternal deprivation as an animal model for schizophrenia. Clinical Neuroscience Research, 3, 297-302.
8. Faure, J., Uys, J. D., Marais, L., Stein, D. J., & Daniels, W. M. (2007). Early maternal separation alters the response to traumatization: resulting in increased levels of hippocampal neurotrophic factors. Metabolic Brain Disease, 22, 183-195.
9. Francis, D., Caldji, C., Champagne, F., Plotsky, P., & Meaney, M. (1999). The role of corticotropin releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Biological Psychology, 46, 1153-1166.
10. Handa, R. T., Burgess, L. H., Kerr, J. E., & O'Keefe, J. A. (1994). Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Hormones and Behavior, 28, 464-476.
11. Heim, C.,&Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biological Psychiatry, 49, 1023-1039.
12. Holzwarth, M. A.,Cunningham, L. A.,&Kleitman,N. (1987). The role of adrenal nerves in the regulation of adrenocortical function. Annals of the New York Academy of Sciences, 512, 449-464.
13. Huot, R. L., Gonzalez, M. E., Ladd, C. O., Thrivikraman, K. V., & Plotsky, P.M. (2004). Foster litters prevent hypothalamic-pituitary-adrenal axis sensitization mediated by neonatal maternal separation. Psychoneuroendocrinology, 29, 279-289.
14. Huot, R. L., Thrivikraman, K. V., Meaney, M. J., & Plotsky, P. M. (2001). Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long-Evans rats and reversal with antidepresive treatment. Psychopharmacology, 158, 366-373.
15. Kalinichev, M., Easterling, K. W., & Holtzman, S. G. (2001). Repeated neonatal maternal separation alters morphine-induced anticonception in male rats. Brain Research Bulletin, 54, 649-654.
16. Kalinichev, M., Easterling, K.W., Plotsky, P.M.,&Holtzman, S. G. (2002). Long-lasting changes in stress-induced carticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats. Pharmacology, Biochemistry and Behavior, 73, 131-140.
17. König, J. F. R.,&Klippel, R. A. (1963). The Rat Brain. Baltimore:Williams andWilkins Company.
18. Labrie, F., Giguere, V., Meunier, H., Simard, J., Grossard, F., & Raymond, V. (1987). Multiple factors controlling ACTH secretion at the anterior pituitary levels. Annals of the New York Academy of Sciences, 512, 97-114.
19. Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J., & Plotsky P. M. (2000). Long-term behavioral and neuroendocrine adaptations to adverse early experience. Progress in Brain Research, 122, 81-103.
20. Ladd, C. O., Owens, M. J.,&Nemeroff, C. B. (1996). Persistent changes in corticotropinreleasing factor neuronal systems induced by maternal deprivation. Endocrinology, 137, 1212-1218.
21. Lehmann, I., Stöhr, T., & Feldon, J. (2000). Long-term effect of prenatal stress experience and postnatal maternal separation on emotional and attentional processes. Behavioral Brain Research, 107, 133-144.
22. Liebsch, G., Landgraf, R., Gestberger, R., Probst, J. Ch.,Wotjak, C. T., Engelmann, M., et al. (1995). Chronic infusion of a CRH1 receptor antisense oligodeoxynucleotide into the central nucleus of the amygdala reduced anxiety-related behavior in socially defeated rats. Regulatory Peptides, 59, 229-239.
23. Liu, D., Caldji, C., Sharma, S., Plotsky, P. M., & Meaney, M. J. (2000). Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinephrine release in the hypothalamic paraventricular nucleus. Journal of Neuroendocrinology, 12, 5-12.
24. Loyber, I., Perassi, N., Leucona, F. A., & Peralta, M. E. (1977). Effects of handling normal and bulbectomized rats at adrenal and plasma corticosterone levels. Experientia, 33, 1393-1394.
25. Marmendal, M., Roman, E., Eriksson, C. J., Nylander, I., Fahlke, C. (2004). Maternal separation alters maternal care, but has minor effects on behavior and brain opioid peptides in adult offspring. Developmental Psychobiology, 45, 140-152.
26. McIntosh, J., Anisman, H., & Merali, Z. (1999). Short-and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Developmental Brain Research, 113, 97-106.
27. Ogawa, T., Mikuni, M., Kuroda, M. Y., Muneoka, K., Mori, K. J., & Takahashi, K. (1994). Periodic maternal deprivation alters stress response in adult offspring: potentiates the negative feedback regulation of restraint stress-induced adrenocortical response and reduces the frequencies of open field-induced behaviors. Pharmacology, Biochemistry and Behavior, 49, 961-967.
28. Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985). Validation of open:closed arm entries in an elevated plus maze as a measure of anxiety in the rat. Journal of Neuroscience Methods, 14, 149-167.
29. Pellow, S., & File, S. E. (1986). Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus maze: a novel test of anxiety in the rat. Pharmacology, Biochemistry and Behavior, 24, 525-529.
30. Pfaff, D. W. (2002). Hormones, Brain and Behavior. San Diego, CA: Academic Press.
31. Ploj, K., Roman, E., & Nylander, I. (2002). Effects of maternal separation on brain nociceptin/orphanin FQ peptide levels in male Wistar rats. Pharmacology, Biochemistry and Behavior, 73, 123-129.
32. Plotsky, P. M., Cunningham, E. T., & Widmaier, E. P. (1989). Catecholaminergic modulation of corticotropin-releasing factor and adrenocorticotropin secretion. Endocrine Reviews, 10, 437-458.
33. Plotsky, P. M., & Meaney, M. J. (1993). Early postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Molecular Brain Research, 18, 195-200.
34. Pryce, C. R., & Feldom, J. (2003). Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neuroscience and Behavioral Reviews, 27, 57-71.
35. Ratka, A., Sutanto, W., Bloemers, M., & De Kloet, E. R. (1989). On the role of brain type I and type II corticosteroid receptors in neuroendocrine regulation. Neuroendocrinology, 50, 117-123.
36. Renard, G. M., Súarez, M. M., Levin, G. M., & Rivarola, M. A. (2005). Sex differences in rats: effects of chronic stress on sympathetic system and anxiety. Physiology and Behavior, 85, 363-369.
37. Rhees, R.W., Lephart, E.D.,&Eliason, D. (2001). Effects ofmaternal separation during early postnatal development on male sexual behavior and female reproductive function. Behavioral Brain Research, 123, 1-10.
38. Russell, D. R., Mueller, A., Sisti, H. M., Ogawa, S., McEwen, B. S., & Brake, W. G. (2003). Anxiety and fear behaviors in adult male and female C57BL/6 mice are modulated by maternal separation. Hormones and Behavior, 43, 561-567.
39. Shalev, U., & Kafkafi, N. (2002). Repeated maternal separation does not alter sucrosereinforced and open-field behaviors. Pharmacology, Biochemistry and Behavior, 73, 115-122.
40. Slotten, H. A., Kalinichev, M., Hagan, J. J., Marsden, C. A.,&Fone,K. C. (2006). Longlasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects. Brain Research, 1097, 123-132.
41. Súarez, M. M.,&Perassi, N. I. (1988). Plasma responses to lesions or stimulations of the limbic thalami nuclei, medial mammillary nucleus and cingulate cortex. Archives Internationales de Physiologie et de Biochimie, 96, 69-74.
42. Súarez, M. M., & Perassi, N. I. (1990). Interaction of some limbic structures which exert inhibitory effect on corticosterone secretion. Archives Internationales de Physiologie et de de Biochimie, 98, 325-330.
43. Súarez, M. M., & Perassi, N. I. (1993). Adrenal response to acute stress in mammillary medial nuclei lesioned rats. Archives Internationales de Physiologie, de Biochimie et de Biophysique, 101, 275-277.
44. Súarez, M. M., & Perassi, N. I. (1997). Influence of anterodorsal thalami nuclei on ACTH release under basal and stressful conditions. Physiology and Behavior, 62, 373-377.
45. Súarez, M. M., Perassi, N. I., & Loyber, I. (1987). Effects of anterodorsalis thalami nucleus lesion on adrenal function in rats. Acta Physiologica et Pharmacologica Latinoamericana, 37, 403-407.
46. Súarez, M. M., Rivarola, M. A., Molina, S. M., Levin, G. M., Ender, J., & Paglini, P. (2004). The role of the anterodorsal thalami nuclei in the regulation of adrenal medullary function, beta-adrenergic cardiac receptors and anxiety responses in maternal deprived rats under stressful conditions. Stress, 7, 195-203.
47. Súarez, M. M., Rivarola, M., Molina, S., Perassi, N., Levin, G., & Cabrera, R. (2001). Periodic maternal deprivation and lesion of anterodorsal thalami nuclei induce alteration on hypophyso-adrenal system activity in adult rats. Life Sciences, 69, 803-813.
48. Suomi, S. J., Collins, M. I., Harlow, H. F., & Ruppenthal, G. C. (1976). Effects of maternal and peer separations on young monkeys. Journal of Child Psychology and Psychiatry and Allied Disciplines, 17, 101-112.
49. Viau, V.,&Meaney,M. J. (1996). The inhibitory effect of testosterone on hypothalamicpituitary- adrenal responses to stress is mediated by the medial preoptic area. Journal of Neuroscience, 16, 1866-1876.
50. Wigger, A., & Neumann, I. D. (1999). Periodic maternal deprivation induces genderdependent alteration in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiology and Behavior, 66, 293-302.
51. Williamson, M., Bingham, B., & Viau, V. (2005). Central organization of androgensensitive pathways to the hypothalamic-pituitary-adrenal axis: implications for individual differences in responses to homeostatic threat and predisposition to disease. Progress in Neuro-psychopharmacology and Biological Psychiatry, 29, 1239-1248.
52. Zeman, W., & Innes, J. M. P. (1963). Cragie's Neuroanatomy of the Rat. New York: Academic Press.
53. Zimmerberg, B., & Kajunski, E. W. (2004). Sexually dimorphic effects of postnatal allopregnanolone on the development of anxiety behavior after early deprivation. Pharmacology, Biochemistry and Behavior, 78, 465-471.