Mechanisms of late-onset cognitive decline after early-life stress

Journal of Neuroscience

Volumn 25, Issue 41, 2005, Pages 9328-9338

  Brunson, Kristen L ^a   Kramár, Enikö ^a   Lin, Bin ^a   Chen, Yuncai ^a   Colgin, Laura Lee ^a   Yanagihara, Theodore K ^a   Lynch, Gary ^a   Baram, Tallie Z ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aging; Dendritic atrophy; Hippocampus; Long term potentiation; Memory; Stress

Indexed keywords

AGING; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; COGNITIVE DEFECT; CONTROLLED STUDY; DENDRITIC CELL; HIPPOCAMPUS; HISTOCHEMISTRY; LONG TERM POTENTIATION; MALE; MAZE TEST; MEMORY; MOSSY FIBER; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; STRESS; SYNAPTIC TRANSMISSION;

AGE FACTORS; AGE OF ONSET; ANIMALS; COGNITION DISORDERS; FEMALE; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MATERNAL BEHAVIOR; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 26844446451     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2281-05.2005     Document Type: Article

References (75)

1. Alfarez D, Joels M, Krugers H (2003) Chronic unpredictable stress impairs long-term potentiation in rat hippocampal CA1 area and dentate gyrus in vitro. Eur J Neurosci 17:1928-1934.
2. Amaral D, Dent J (1981) Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopy study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
3. Amaral DG, Ishizuka N, Claiborne B (1990) Neurons, numbers and the hippocampal network. Prog Brain Res 83:1-11.
4. Ammerman R, Cassisi J, Hersen M, Rasselt W (1986) Consequences of physical abuse and neglect in children. Clin Psychol Rev 6:291-310.
5. Andersen P, Silfvenius H, Sundberg SH, Sveen O, Wigstrom H (1978) Functional characteristics of unmyelinated fibres in the hippocampal cortex. Brain Res 144:11-18.
6. Arai A, Lynch G (1992) Factors regulating the magnitude of long-term potentiation induced by theta pattern stimulation. Brain Res 598:173-184.
7. Avishai-Eliner S, Gilles E, Eghbal-Ahmadi M, Bar-El Y, Baram T (2001) Altered regulation of gene and protein expression of hypothalamic-pituitary- adrenal axis components in an immature rat model of chronic stress. J Neuroendocrinol 13:799-807.
8. Avishai-Eliner S, Brunson K, Sandman C, Baram T (2002) Stressed-out, or in (utero)? Trends Neurosci 25:518-524.
9. Bi X, Yong AP, Zhou J, Ribak CE, Lynch G (2001) Rapid induction of intra-neuronal neurofibrillary tangles in apolipoprotein E-deficient mice. Proc Natl Acad Sci USA 98:8832-8837.
10. Blank T, Nijholt I, Spiess J (2004) Molecular determinants mediating effects of acute stress on hippocampus-dependent synaptic plasticity and learning. Mol Neurobiol 29:131-138.
11. Bliss T, Collingridge G (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
12. Bodnoff SR, Humphreys AG, Lehman JC, Diamond DM, Rose GM, Meaney MJ (1995) Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. J Neurosci 15:61-69.
13. Bremner JD, Randall P, Vermetten E, Staib L, Bronen RA, Mazure C, Capelli S, McCarthy G, Innis RB, Charney DS (1997) Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse-a preliminary report. Biol Psychiatry 41:23-32.
14. Broadbent NJ, Squire LR, Clark RE (2004) Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci USA 101:14515-14520.
15. Brunson K, Eghbal-Ahmadi M, Bender R, Chen Y, Baram T (2001) Long-term, progressive hippocampal cell loss and dysfunction induced by early-life administration of corticotropin-releasing hormone reproduce the effects of early-life stress. Proc Natl Acad Sci USA 98:8856-8861.
16. Brunson K, Chen Y, Avishai-Eliner S, Baram TZ (2003) Stress and the developing hippocampus a double-edged sword? Mol Neurobiol 27:121-136.
17. Buzsaki G (1986) Hippocampal sharp waves: their origins and significance. Brain Res 398:242-252.
18. Buzsaki G, Bayardo F, Miles R, Wong RK, Gage FH (1989) The grafted hippocampus: an epileptic focus. Exp Neurol 105:10-22.
19. Chang FL, Greenough WT (1984) Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res 309:35-46.
20. Chen Y, Bender RA, Brunson KL, Pomper JL, Grigoriadis DE, Wurst W, Baram TZ (2004) Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc Natl Acad Sci USA 101:15782-157827.
21. Clark R, Zola S, Squire L (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853-8860.
22. Dachir S, Kadar T, Robinzon B, Levy A (1993) Cognitive deficits induced in young rats by long-term corticosterone administration. Behav Neural Biol 60:103-109.
23. Desmond NL, Levy WB (1986) Changes in the postsynaptic density with long-term potentiation in the dentate gyrus. J Comp Neurol 253:476-482.
24. Forwood SE, Winters BD, Bussey TJ (2005) Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 hours. Hippocampus 15:347-355.
25. Heim C, Plotsky PM, Nemeroff CB (2004) Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 29:641-648.
26. Henze D, Urban N, Barrionuevo G (2000) The multifarious hippocampal mossy fiber pathway: a review. Neuroscience 98:407-427.
27. Hibberd C, Yau JL, Seckl JR (2000) Glucocorticoids and the ageing hippocampus. J Anat 197:553-562.
28. Hollup S, Kjelstrup K, Hoff J, Moser M, Moser E (2001) Impaired recognition of the goal location during spatial navigation in rats with hippocampal lesions. J Neurosci 21:4505-4513.
29. Holmes G, Ben-Ari Y (1998) Seizures in the developing brain perhaps not so benign after all. Neuron 21:1231-1234.
30. Holmes GL, Sarkisian M, Ben-Ari Y, Chevassus-Au-Louis N (1999) Mossy fiber sprouting after recurrent seizures during early development in rats. J Comp Neurol 404:537-553.
31. Horikawa K, Armstrong WE (1988) A versatile means of intracellular labeling injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25:1-11.
32. Huot R, Plotsky P, Lenox R, McNamara R (2002) Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res 950:52-63.
33. Isgor C, Kabbaj M, Akil H, Watson SJ (2004) Delayed effects of chronic variable stress during peripubertal-juvenile period on hippocampal morphology and on cognitive and stress axis functions in rats. Hippocampus 14:636-648.
34. Joels M, Verkuyl J, Riel EV (2003) Hippocampal and hypothalamic function after chronic stress. Ann NY Acad Sci 1007:367-378,
35. Kamiya H, Shinozaki H, Yamamoto C (1996) Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fiber synapses. J Physiol (Lond) 493:447-455.
36. Kaplan Z, Iancu I, Bodner E (2001) A review of psychological debriefing after extreme stress. Psychiatr Serv 52:824-827.
37. Kerr DS, Campbell LW, Applegate MD, Brodish A, Landfield PW (1991) Chronic stress-induced acceleration of electrophysiologic and morphometric biomarkers of hippocampal aging. J Neurosci 11:1316-1324.
38. Khalilov I, Holmes G, Ben-Ari Y (2003) In vitro formation of a secondary epileptogenic mirror focus by interhippocampal propagation of seizures. Nat Neurosci 6:1079-1085.
39. Kim J, Diamond D (2002) The stressed hippocampus, synaptic plasticity and lost memories. Nat Rev Neurosci 3:453-462,
40. Kramár EA, Lynch G (2003) Developmental and regional differences in the consolidation of long-term potentiation, Neuroscience 118:387-398,
41. Kramár EA, Lin B, Lin C, Arai A, Gall C, Lynch G (2004) A novel mechanism for the facilitation of theta-induced long-term potentiation by brain-derived neurotrophic factor. J Neurosci 24:5151-5161.
42. Kubota D, Colgin L, Casale M, Brucher F, Lynch G (2003) Endogenous waves in hippocampal slices. J Neurophysiol 89:81-89.
43. Landfield PW, Waymire JC, Lynch G (1978) Hippocampal aging and adrenocorticoids: quantitative correlations. Science 202:1098-1102.
44. Lee KS, Schottler F, Oliver M, Lynch G (1980) Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. J Neurophysiol 44:247-258.
45. Lin B, Kramár EA, Bi X, Brucher FA, Gall CM, Lynch G (2005) Theta stimulation polymerizes actin in dendritic spines of hippocampus. J Neurosci 25:2062-2069.
46. Luine V, Villegas M, Martinez C, McEwen B (1994) Repeated stress causes reversible impairments of spatial memory performance. Brain Res 639:167-170.
47. Luscher C, Nicoll RA, Malenka RC, Muller D (2000) Synaptic plasticity and dynamic modulation of the postsynaptic membrane. Nat Neurosci 3:545-550.
48. Magarinos A, McEwen B (1995a) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons comparison of stressors. Neuroscience 69:83-88.
49. Magarinos A, McEwen B (1995b) Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69:89-98.
50. Malenka R, Nicoll R (1999) Long-term potentiation-a decade of progress? Science 285:1870-1874.
51. Mattson MP, Chan SL (2001) Dysregulation of cellular calcium homeostasis in Alzheimer's disease: bad genes and bad habits. J Mol Neurosci 17:205-224.
52. McEwen B (1999) Stress and hippocampal plasticity. Annu Rev Neurosci 22:105-122.
53. Meaney M, Aitken D, Berkel CV, Bhatnager S, Sapolsky R (1988) Effect of neonatal handling on age-related impairments associated with the hippocampus. Science 239:766-768.
54. Morris R (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
55. Mumby DG, Glenn MJ, Nesbitt C, Kyriazis DA (2002) Dissociation in retrograde memory for object discriminations and object recognition in rats with perirhinal cortex damage. Behav Brain Res 132:215-226.
56. Patchev VK, Montkowski A, Rouskova D, Koranyi L, Holsboer F, Almeida OF (1997) Neonatal treatment of rats with the neuroactive steroid tetrahydrodeoxycorticosterone (THDOC) abolishes the behavioral and neuroendocrine consequences of adverse early life events. J Clin Invest 99:962-996.
57. Pavlides C, Nivon L, McEwen B (2002) Effects of chronic stress on hippocampal long-term potentiation. Hippocampus 12:245-257.
58. Poeggel G, Helmeke C, Abraham A, Schwabe T, Friedrich P, Braun K (2003) Juvenile emotional experience alters synaptic composition in the rodent cortex, hippocampus, and lateral amygdala. Proc Natl Acad Sci USA 100:16137-16142.
59. Popov VI, Davies HA, Rogachevsky W, Patrushev IV, Errington ML, Gabbott PL, Bliss TV, Stewart MG (2004) Remodelling of synaptic morphology but unchanged synaptic density during late phase long-term potentiation (LTP): a serial section electron micrograph study in the dentate gyrus in the anaesthetised rat. Neuroscience 128:251-262.
60. Rex CS, Kramár EA, Colgin LL, Lin B, Gall CM, Lynch G (2005) Long-term potentiation is impaired in middle-aged rats: Regional specificity and reversal by adenosine receptor antagonists. J Neurosci 25:5956-5966.
61. Roman F, Staubli U, Lynch G (1987) Evidence for synaptic potentiation in a cortical network during learning. Brain Res 418:221-226.
62. Sah P, Bekkers JM (1996) Apical dendritic location of slow afterhyperpolarization current in hippocampal pyramidal neurons: implications for the integration of long-term potentiation. J Neurosci 16:4537-4542.
63. Sanchez M, Ladd C, Plotsky P (2001) Early adverse experience as a developmental risk factor for later psychopathology evidence from rodent and primate models. Dev Psychopathol 13:419-449.
64. Sapolsky RM (2002) Chickens, eggs and hippocampal atrophy. Nat Neurosci 5:1111-1113.
65. Scharfman HE, Goodman JH, Du F, Schwarcz R (1998) Chronic changes in synaptic responses of entorhinal and hippocampal neurons after amino-oxyacetic acid (AOAA)-induced entorhinal cortical neuron loss. J Neurophysiol 80:3031-3046.
66. Segal M (2005) Dendritic spines and long-term plasticity. Nat Rev Neurosci 6:277-284.
67. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S, Mizuno N (1997) Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17:7503-7522.
68. Silva A (2003) Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. J Neurobiol 54:224-237.
69. Spehlmann R, Chang CM, Daniels JC (1970) Excitability of partially deafferented cortex. I. Macroelectrode studies. Arch Neurol 22:504-509.
70. + channels modulate synaptic plasticity and memory encoding. J Neurosci 22:10163-10171.
71. St George-Hyslop PH, Petit A (2005) Molecular biology and genetics of Alzheimer's disease. C R Biol 328:119-130.
72. Tanzi RE, Bertram L (2005) Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 120:545-555.
73. van Oers HJ, de Kloet ER, Levine S (1999) Persistent effects of maternal deprivation on HPA regulation can be reversed by feeding and stroking, but not by dexamethasone. J Neuroendocrinol 11:581-588.
74. Yau J, Noble J, Hibberd C, Rowe W, Meaney M, Morris R (2002) Chronic treatment with the antidepressant amitriptyline prevents impairments in water maze learning in aging rats. J Neurosci 22:1436-1442.
75. Yeckel MF, Kapur A, Johnston D (1999) Multiple forms of LTP in hippocampal CA3 neurons use a common postsynaptic mechanism. Nat Neurosci 2:625-633.