Dendritic morphology of Hippocampal and Amygdalar neurons in adolescent mice is resilient to genetic differences in stress reactivity

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Pillai, Anup G ^a,c   de Jong, Danielle ^c   Kanatsou, Sofia ^a,c   Krugers, Harm ^c   Knapman, Alana ^b   Heinzmann, Jan Michael ^b   Holsboer, Florian ^b   Landgraf, Rainer ^b   Joëls, Marian ^a,c   Touma, Chadi ^b  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CORTICOSTERONE;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BASOLATERAL AMYGDALA; BLOOD SAMPLING; BRAIN CELL; CELL STRUCTURE; COGNITION; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DENDRITIC CELL; EMOTION; GENETIC DIFFERENCE; GENETIC PREDISPOSITION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HISTOPATHOLOGY; HYPOPHYSIS ADRENAL SYSTEM; MALE; MOUSE; NERVE CELL PLASTICITY; NEUROENDOCRINE SYSTEM; NONHUMAN; PERIKARYON; PHENOTYPE; PYRAMIDAL NERVE CELL; SLEEP PARAMETERS; STRATUM RADIATUM; STRESS; ANALYSIS OF VARIANCE; ANIMAL; BLOOD; CYTOLOGY; DENDRITE; DENDRITIC SPINE; GENETICS; MOUSE STRAIN; NERVE CELL; PHYSIOLOGICAL STRESS; PHYSIOLOGY; ULTRASTRUCTURE;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; CORTICOSTERONE; DENDRITES; DENDRITIC SPINES; HIPPOCAMPUS; MALE; MICE; MICE, INBRED STRAINS; NEURONS; PHENOTYPE; STRESS, PHYSIOLOGICAL;

EID: 84862224261     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0038971     Document Type: Article

References (69)

1. de Kloet ER, Joels M, Holsboer F, (2005) Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6: 463-475.
2. Holsboer F, (2000) The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23: 477-501.
3. Holsboer F, Lauer CJ, Schreiber W, Krieg JC, (1995) Altered hypothalamic-pituitary-adrenocortical regulation in healthy subjects at high familial risk for affective disorders. Neuroendocrinology 62: 340-347.
4. Ising M, Kunzel HE, Binder EB, Nickel T, Modell S, et al. (2005) The combined dexamethasone/CRH test as a potential surrogate marker in depression. Prog Neuropsychopharmacol Biol Psychiatry 29: 1085-1093.
5. Lauer CJ, Schreiber W, Modell S, Holsboer F, Krieg JC, (1998) The Munich vulnerability study on affective disorders: overview of the cross-sectional observations at index investigation. J Psychiatr Res 32: 393-401.
6. Modell S, Lauer CJ, Schreiber W, Huber J, Krieg JC, et al. (1998) Hormonal response pattern in the combined DEX-CRH test is stable over time in subjects at high familial risk for affective disorders. Neuropsychopharmacology 18: 253-262.
7. Deuschle M, Schweiger U, Weber B, Gotthardt U, Korner A, et al. (1997) Diurnal activity and pulsatility of the hypothalamus-pituitary-adrenal system in male depressed patients and healthy controls. J Clin Endocrinol Metab 82: 234-238.
8. Keller J, Flores B, Gomez RG, Solvason HB, Kenna H, et al. (2006) Cortisol circadian rhythm alterations in psychotic major depression. Biol Psychiatry 60: 275-281.
9. Wong ML, Kling MA, Munson PJ, Listwak S, Licinio J, et al. (2000) Pronounced and sustained central hypernoradrenergic function in major depression with melancholic features: relation to hypercortisolism and corticotropin-releasing hormone. Proc Natl Acad Sci U S A 97: 325-330.
10. Modell S, Yassouridis A, Huber J, Holsboer F, (1997) Corticosteroid receptor function is decreased in depressed patients. Neuroendocrinology 65: 216-222.
11. Rubin RT, Poland RE, Lesser IM, Winston RA, Blodgett AL, (1987) Neuroendocrine aspects of primary endogenous depression. I. Cortisol secretory dynamics in patients and matched controls. Arch Gen Psychiatry 44: 328-336.
12. Holsboer F, Barden N, (1996) Antidepressants and hypothalamic-pituitary-adrenocortical regulation. Endocr Rev 17: 187-205.
13. De Bellis MD, Gold PW, Geracioti TD Jr, Listwak SJ, Kling MA, (1993) Association of fluoxetine treatment with reductions in CSF concentrations of corticotropin-releasing hormone and arginine vasopressin in patients with major depression. Am J Psychiatry 150: 656-657.
14. Holsboer F, von Bardeleben U, Wiedemann K, Muller OA, Stalla GK, (1987) Serial assessment of corticotropin-releasing hormone response after dexamethasone in depression. Implications for pathophysiology of DST nonsuppression. Biol Psychiatry 22: 228-234.
15. Holsboer-Trachsler E, Hemmeter U, Hatzinger M, Seifritz E, Gerhard U, et al. (1994) Sleep deprivation and bright light as potential augmenters of antidepressant drug treatment-neurobiological and psychometric assessment of course. J Psychiatr Res 28: 381-399.
16. Heuser IJ, Schweiger U, Gotthardt U, Schmider J, Lammers CH, et al. (1996) Pituitary-adrenal-system regulation and psychopathology during amitriptyline treatment in elderly depressed patients and normal comparison subjects. Am J Psychiatry 153: 93-99.
17. Zobel AW, Yassouridis A, Frieboes RM, Holsboer F, (1999) Prediction of medium-term outcome by cortisol response to the combined dexamethasone-CRH test in patients with remitted depression. Am J Psychiatry 156: 949-951.
18. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, et al. (2000) Hippocampal volume reduction in major depression. Am J Psychiatry 157: 115-118.
19. Sheline YI, Sanghavi M, Mintun MA, Gado MH, (1999) Depression duration but not age predicts hippocampal volume loss in medically healthy women with recurrent major depression. J Neurosci 19: 5034-5043.
20. Sheline YI, Gado MH, Price JL, (1998) Amygdala core nuclei volumes are decreased in recurrent major depression. Neuroreport 9: 2023-2028.
21. Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW, (1996) Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci U S A 93: 3908-3913.
22. Lupien SJ, de Leon M, de Santi S, Convit A, Tarshish C, et al. (1998) Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat Neurosci 1: 69-73.
23. Coplan JD, Andrews MW, Rosenblum LA, Owens MJ, Friedman S, et al. (1996) Persistent elevations of cerebrospinal fluid concentrations of corticotropin-releasing factor in adult nonhuman primates exposed to early-life stressors: implications for the pathophysiology of mood and anxiety disorders. Proc Natl Acad Sci U S A 93: 1619-1623.
24. Checkley S, (1996) The neuroendocrinology of depression and chronic stress. Br Med Bull 52: 597-617.
25. De Bellis MD, Chrousos GP, Dorn LD, Burke L, Helmers K, et al. (1994) Hypothalamic-pituitary-adrenal axis dysregulation in sexually abused girls. J Clin Endocrinol Metab 78: 249-255.
26. Frodl T, Reinhold E, Koutsouleris N, Reiser M, Meisenzahl EM, (2010) Interaction of childhood stress with hippocampus and prefrontal cortex volume reduction in major depression. J Psychiatr Res 44: 799-807.
27. Touma C, Bunck M, Glasl L, Nussbaumer M, Palme R, et al. (2008) Mice selected for high versus low stress reactivity: a new animal model for affective disorders. Psychoneuroendocrinology 33: 839-862.
28. Knapman A, Heinzmann JM, Hellweg R, Holsboer F, Landgraf R, et al. (2010) Increased stress reactivity is associated with cognitive deficits and decreased hippocampal brain-derived neurotrophic factor in a mouse model of affective disorders. J Psychiatr Res 44: 566-575.
29. Touma C, Fenzl T, Ruschel J, Palme R, Holsboer F, et al. (2009) Rhythmicity in mice selected for extremes in stress reactivity: behavioural, endocrine and sleep changes resembling endophenotypes of major depression. PLoS One 4: e4325-.
30. Fenzl T, Touma C, Romanowski CP, Ruschel J, Holsboer F, et al. (2011) Sleep disturbances in highly stress reactive mice: modeling endophenotypes of major depression. BMC Neurosci 12: 29-.
31. Knapman A, Heinzmann JM, Holsboer F, Landgraf R, Touma C, (2010) Modeling psychotic and cognitive symptoms of affective disorders: Disrupted latent inhibition and reversal learning deficits in highly stress reactive mice. Neurobiol Learn Mem 94: 145-152.
32. Magarinos AM, McEwen BS, Flugge G, Fuchs E, (1996) Chronic psychosocial stress causes apical dendritic atrophy of hippocampal CA3 pyramidal neurons in subordinate tree shrews. J Neurosci 16: 3534-3540.
33. McEwen BS, (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22: 105-122.
34. Watanabe Y, Gould E, McEwen BS, (1992) Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 588: 341-345.
35. Alfarez DN, De Simoni A, Velzing EH, Bracey E, Joels M, et al. (2009) Corticosterone reduces dendritic complexity in developing hippocampal CA1 neurons. Hippocampus 19: 828-836.
36. Morales-Medina JC, Sanchez F, Flores G, Dumont Y, Quirion R, (2009) Morphological reorganization after repeated corticosterone administration in the hippocampus, nucleus accumbens and amygdala in the rat. J Chem Neuroanat 38: 266-272.
37. Sousa N, Lukoyanov NV, Madeira MD, Almeida OF, Paula-Barbosa MM, (2000) Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97: 253-266.
38. Vyas A, Mitra R, Shankaranarayana Rao BS, Chattarji S, (2002) Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 22: 6810-6818.
39. Mitra R, Sapolsky RM, (2008) Acute corticosterone treatment is sufficient to induce anxiety and amygdaloid dendritic hypertrophy. Proc Natl Acad Sci U S A 105: 5573-5578.
40. Johnson SA, Wang JF, Sun X, McEwen BS, Chattarji S, et al. (2009) Lithium treatment prevents stress-induced dendritic remodeling in the rodent amygdala. Neuroscience 163: 34-39.
41. Manji HK, Quiroz JA, Sporn J, Payne JL, Denicoff K, et al. (2003) Enhancing neuronal plasticity and cellular resilience to develop novel, improved therapeutics for difficult-to-treat depression. Biol Psychiatry 53: 707-742.
42. Ohl F, Michaelis T, Vollmann-Honsdorf GK, Kirschbaum C, Fuchs E, (2000) Effect of chronic psychosocial stress and long-term cortisol treatment on hippocampus-mediated memory and hippocampal volume: a pilot-study in tree shrews. Psychoneuroendocrinology 25: 357-363.
43. Sheline YI, (2003) Neuroimaging studies of mood disorder effects on the brain. Biol Psychiatry 54: 338-352.
44. Sheline YI, (2000) 3D MRI studies of neuroanatomic changes in unipolar major depression: the role of stress and medical comorbidity. Biol Psychiatry 48: 791-800.
45. Dallmann R, Touma C, Palme R, Albrecht U, Steinlechner S, (2006) Impaired daily glucocorticoid rhythm in Per1 (Brd) mice. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 192: 769-775.
46. Engeland WC, Arnhold MM, (2005) Neural circuitry in the regulation of adrenal corticosterone rhythmicity. Endocrine 28: 325-332.
47. HALBERG F, ALBRECHT PG, BITTNER JJ, (1959) Corticosterone rhythm of mouse adrenal in relation to serum corticosterone and sampling. Am J Physiol 197: 1083-1085.
48. Horner CH, Arbuthnott E, (1991) Methods of estimation of spine density-are spines evenly distributed throughout the dendritic field? J Anat 177: 179-184.
49. Vyas A, Pillai AG, Chattarji S, (2004) Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 128: 667-673.
50. Donohue HS, Gabbott PL, Davies HA, Rodriguez JJ, Cordero MI, et al. (2006) Chronic restraint stress induces changes in synapse morphology in stratum lacunosum-moleculare CA1 rat hippocampus: a stereological and three-dimensional ultrastructural study. Neuroscience 140: 597-606.
51. Pawlak R, Rao BS, Melchor JP, Chattarji S, McEwen B, et al. (2005) Tissue plasminogen activator and plasminogen mediate stress-induced decline of neuronal and cognitive functions in the mouse hippocampus. Proc Natl Acad Sci U S A 102: 18201-18206.
52. Mervaala E, Fohr J, Kononen M, Valkonen-Korhonen M, Vainio P, et al. (2000) Quantitative MRI of the hippocampus and amygdala in severe depression. Psychol Med 30: 117-125.
53. Keller J, Shen L, Gomez RG, Garrett A, Solvason HB, et al. (2008) Hippocampal and amygdalar volumes in psychotic and nonpsychotic unipolar depression. Am J Psychiatry 165: 872-880.
54. Frodl T, Meisenzahl E, Zetzsche T, Bottlender R, Born C, et al. (2002) Enlargement of the amygdala in patients with a first episode of major depression. Biol Psychiatry 51: 708-714.
55. Heinzmann JM, Thoeringer CK, Knapman A, Palme R, Holsboer F, et al. (2010) Intrahippocampal corticosterone response in mice selectively bred for extremes in stress reactivity: a microdialysis study. J Neuroendocrinol 22: 1187-1197.
56. Adam EK, Sutton JM, Doane LD, Mineka S, (2008) Incorporating hypothalamic-pituitary-adrenal axis measures into preventive interventions for adolescent depression: are we there yet? Dev Psychopathol 20: 975-1001.
57. Adam EK, Doane LD, Zinbarg RE, Mineka S, Craske MG, et al. (2010) Prospective prediction of major depressive disorder from cortisol awakening responses in adolescence. Psychoneuroendocrinology 35: 921-931.
58. Bersani G, Liberati D, Rasa A, Polli E, Ciuffa M, et al. (2010) Premorbid sleep, appetite, energy, and cognitive circadian profile in patients with depressive disorders. Eur Psychiatry 25: 461-464.
59. Friess E, Modell S, Brunner H, Tagaya H, Lauer CJ, et al. (2008) The Munich vulnerability study on affective disorders: microstructure of sleep in high-risk subjects. Eur Arch Psychiatry Clin Neurosci 258: 285-291.
60. Ising M, Lauer CJ, Holsboer F, Modell S, (2005) The Munich vulnerability study on affective disorders: premorbid neuroendocrine profile of affected high-risk probands. J Psychiatr Res 39: 21-28.
61. Choi S, Weisberg SN, Kellogg CK, (1997) Control of endogenous norepinephrine release in the hypothalamus of male rats changes over adolescent development. Brain Res Dev Brain Res 98: 134-141.
62. Vazquez DM, (1998) Stress and the developing limbic-hypothalamic-pituitary-adrenal axis. Psychoneuroendocrinology 23: 663-700.
63. Peleg-Raibstein D, Feldon J, (2011) Differential effects of post-weaning juvenile stress on the behaviour of C57BL/6 mice in adolescence and adulthood. Psychopharmacology (Berl) 214: 339-351.
64. Kellogg CK, Awatramani GB, Piekut DT, (1998) Adolescent development alters stressor-induced Fos immunoreactivity in rat brain. Neuroscience 83: 681-689.
65. Avital A, Richter-Levin G, (2005) Exposure to juvenile stress exacerbates the behavioural consequences of exposure to stress in the adult rat. Int J Neuropsychopharmacol 8: 163-173.
66. Tsoory M, Cohen H, Richter-Levin G, (2007) Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol 17: 245-256.
67. Lenze SN, Xiong C, Sheline YI, (2008) Childhood adversity predicts earlier onset of major depression but not reduced hippocampal volume. Psychiatry Res 162: 39-49.
68. Heim C, Newport DJ, Mletzko T, Miller AH, Nemeroff CB, (2008) The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33: 693-710.
69. Rao U, Chen LA, Bidesi AS, Shad MU, Thomas MA, et al. (2010) Hippocampal changes associated with early-life adversity and vulnerability to depression. Biol Psychiatry 67: 357-364.