Disconnection and reconnection: The morphological basis of (mal)adaptation to stress

Trends in Neurosciences

Volumn 35, Issue 12, 2012, Pages 742-751

  Sousa, Nuno ^a   Almeida, Osborne F X ^a,b  

^a UNIVERSITY OF MINHO   (Portugal)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

Author keywords

Cognition; Emotion; Glucocorticoids; Plasticity; Stress

Indexed keywords

ANTIDEPRESSANT AGENT;

ANXIETY; BEHAVIOR; BRAIN STEM; CELL FATE; CELL STRESS; CELL STRUCTURE; CHRONIC STRESS; CLINICAL DECISION MAKING; DENDRITIC CELL; GLIA CELL; HUMAN; MALADJUSTMENT; MENTAL STRESS; NERVE CELL PLASTICITY; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPTIC TRANSMISSION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BRAIN; HUMANS; MENTAL DISORDERS; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84869868062     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2012.08.006     Document Type: Review

References (115)

1. Selye H. A syndrome produced by diverse nocuous agents. Nature 1936, 138:32.
2. McEwen B.S., Giannaros P.J. Stress- and allostasis-induced brain plasticity. Annu. Rev. Med. 2011, 62:431-445.
3. Sapolsky R.M., et al. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
4. de Kloet R., et al. Corticosteroid hormones in the central stress response: quick-and-slow. Front. Neuroendocrinol. 2008, 29:268-272.
5. Sapolsky R.M., et al. The neuroendocrinology of stress and aging, the glucocorticoid cascade hypothesis. Endocr. Rev. 1986, 7:284-301.
6. Sapolsky R.M. A mechanism for glucocorticoid toxicity in the hippocampus, increased neuronal vulnerability to metabolic insults. J. Neurosci. 1985, 5:1228-1232.
7. Chrochemore C., et al. Direct targeting of hippocampal neurons for apoptosis by glucocorticoids is reversible by mineralocorticoid receptor activation. Mol. Psychiatry 2005, 10:790-798.
8. Landfield P.W., et al. Mechanisms of neuronal death in brain aging and Alzheimer's disease: role of endocrine-mediated calcium dyshomeostasis. J. Neurobiol. 1992, 23:1247-1260.
9. Stein-Behrens B., et al. Stress exacerbates neuron loss and cytoskeletal pathology in the hippocampus. J. Neurosci. 1994, 14:5373-5380.
10. Lu J., et al. Ionotropic and metabotropic glutamate receptor mediation of glucocorticoid-induced apoptosis in hippocampal cells and the neuroprotective role of synaptic N-methyl-D-aspartate receptors. Neuroscience 2003, 121:123-131.
11. Behl C., et al. Protection against oxidative stress-induced neuronal cell death - a novel role for RU486. Eur. J. Neurosci. 1997, 9:912-920.
12. Starkman M.N., et al. Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol. Psychiatry 1992, 32:756-765.
13. Sheline Y.I., et al. Hippocampal atrophy in recurrent major depression. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:3908-3913.
14. Starkman M.N., et al. Decrease in cortisol reverses human hippocampal atrophy following treatment of Cushing's disease. Biol. Psychiatry 1999, 46:1595-1602.
15. Frodl T., et al. Effect of hippocampal and amygdala volumes on clinical outcomes in major depression: a 3-year prospective magnetic resonance imaging study. J. Psychiatry Neurosci. 2007, 33:423-430.
16. Colla M., et al. Hippocampal volume reduction and HPA-system activity in major depression. J. Psychiatr. Res. 2007, 41:553-560.
17. Sousa N., et al. Maintenance of hippocampal cell numbers in young and aged rats submitted to chronic unpredictable stress. Comparison with the effects of corticosterone treatment. Stress 1998, 2:237-249.
18. Dranovsky A., et al. Experience dictates stem cell fate in the adult hippocampus. Neuron 2011, 70:908-923.
19. Sahay A., et al. Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 2011, 70:582-588.
20. Kitamura T., et al. Adult neurogenesis modulates the hippocampus-dependent period of associative fear memory. Cell 2009, 139:814-827.
21. Bessa J.M., et al. The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol. Psychiatry 2009, 14:764-773. 739.
22. David D.J., et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 2009, 62:479-493.
23. Pham K., et al. Repeated restraint stress suppresses neurogenesis and induces biphasic PSA-NCAM expression in the adult rat dentate gyrus. Eur. J. Neurosci. 2003, 17:879-886.
24. Tichomirowa M.A., et al. Endocrine disturbances in depression. J. Endocrinol. Invest. 2005, 28:89-99.
25. Holsboer F., et al. Diagnostic value of dexamethasone suppression test in depression. Lancet 1980, 2:706.
26. Snyder J.S., et al. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 2011, 476:458-461.
27. Surget A., et al. Antidepressants recruit new neurons to improve stress response regulation. Mol. Psychiatry 2011, 16:11177-11188.
28. Airan R.D., et al. High-speed imaging reveals neurophysiological links to behavior in an animal model of depression. Science 2007, 317:819-823.
29. Aimone J.B., et al. Resolving new memories: a critical look at the dentate gyrus, adult neurogenesis, and pattern separation. Neuron 2011, 70:589-596.
30. Silva A.J., et al. Molecular and cellular approaches to memory allocation in neural circuits. Science 2009, 326:391-395.
31. Yu S., et al. Depletion of the neural precursor cell pool by glucocorticoids. Ann. Neurol. 2010, 67:21-30.
32. Yu S., et al. Glucocorticoid regulation of astrocytic fate and function. PLoS ONE 2011, 6:e22419.
33. Banasr M., et al. Chronic unpredictable stress decreases cell proliferation in the cerebral cortex of the adult rat. Biol. Psychiatry 2007, 62:496-504.
34. Banasr M., et al. Glial pathology in an animal model of depression: reversal of stress-induced cellular, metabolic and behavioral deficits by the glutamate-modulating drug riluzole. Mol. Psychiatry 2010, 15:501-511.
35. Halassa M.M., Haydon P.G. Integrated brain circuits: astrocytic networks modulate neuronal activity and behavior. Annu. Rev. Physiol. 2010, 17:335-355.
36. Chalifoux J.R., Carter A.G. Glutamate spillover promotes the generation of NMDA spikes. J. Neurosci. 2011, 31:16435-16446.
37. Rajkowska G. Postmortem studies in mood disorders indicate altered numbers of neurons and glial cells. Biol. Psychiatry 2000, 48:766-777.
38. Woolley C.S., et al. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res. 1990, 531:225-231.
39. Sousa N., et al. Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 2000, 97:253-266.
40. van Eekelen J.A., et al. Postnatal ontogeny of mineralocorticoid and glucocorticoid receptor gene expression in regions of the rat tel- and diencephalon. Dev. Brain Res. 1991, 61:33-43.
41. Patel P.D., et al. Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex. Psychoneuroendocrinology 2008, 33:360-367.
42. Groeneweg F.L., et al. Mineralocorticoid and glucocorticoid receptors at the neuronal membrane, regulators of nongenomic corticosteroid signalling. Mol. Cell. Endocrinol. 2012, 350:299-309.
43. Pacak K., Palkovits M. Stressor specificity of central neuroendocrine responses: implications for stress-related disorders. Endocr. Rev. 2001, 22:502-548.
44. Joels M., Baram T. The neuro-symphony of stress. Nat. Rev. Neurosci. 2009, 10:459-466.
45. Ulrich-Lai Y.M., Herman J.P. Neural regulation of endocrine and autonomic stress responses. Nat. Rev. Neurosci. 2009, 10:397-409.
46. Bessa J.M., et al. A trans-dimensional approach to the behavioral aspects of depression. Front. Behav. Neurosci. 2009, 3:1.
47. Pêgo J.M., et al. Dissociation of the morphological correlates of stress-induced anxiety and fear. Eur. J. Neurosci. 2008, 27:1503-1516.
48. Dalley J.W., et al. Prefrontal executive and cognitive functions in rodents, neural and neurochemical substrates. Neurosci. Biobehav. Rev. 2004, 28:771-784.
49. Popoli M., et al. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat. Rev. Neurosci. 2011, 13:22-37.
50. 3H]dexamethasone binding in the limbic brain of the fetal rat. Brain Res. 1985, 355:179-185.
51. Figueiredo H.F., et al. 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.
52. Sullivan R.M., Gratton A. Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology, side matters. Psychoneuroendocrinology 2002, 27:99-114.
53. Sapolsky R.M., et al. The development of the glucocorticoid receptor system in the rat limbic brain. III. Negative-feedback regulation. Brain Res. 1985, 350:169-173.
54. Mizoguchi K., et al. Chronic stress attenuates glucocorticoid negative feedback, involvement of the prefrontal cortex and hippocampus. Neuroscience 2003, 119:887-897.
55. Radley J.J., et al. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 2004, 125:1-6.
56. Cerqueira J.J., et al. Corticosteroid status influences the volume of the rat cingulate cortex - a magnetic resonance imaging study. J. Psychiatr. Res. 2005, 39:451-460.
57. Wellman C.L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J. Neurobiol. 2001, 49:245-253.
58. Cook C.S., Wellman C.L. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J. Neurobiol. 2004, 60:236-248.
59. Radley J.J., et al. Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb. Cortex 2006, 16:313-320.
60. Cerqueira J.J., et al. Specific configuration of dendritic degeneration in pyramidal neurons of the medial prefrontal cortex induced by differing corticosteroid regimens. Cereb. Cortex 2007, 17:1998-2006.
61. Radley J.J., et al. Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. J. Comp. Neurol. 2008, 507:1141-1150.
62. Shansky R.M., et al. Stress-induced dendritic remodeling in the prefrontal cortex is circuit specific. Cereb. Cortex 2009, 19:2479-2484.
63. Shansky R.M., et al. Estrogen promotes stress sensitivity in a prefrontal cortex-amygdala pathway. Cereb. Cortex 2010, 20:2560-2567.
64. Golwater D.S. Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery. Neuroscience 2009, 164:798-808.
65. Perez-Cruz C., et al. Morphology of pyramidal neurons in the rat prefrontal cortex: lateralized dendritic remodeling by chronic stress. Neural Plast. 2007, 2007:46276.
66. Perez-Cruz C., et al. Hemispheric differences in basilar dendrites and spines of pyramidal neurons in the rat prelimbic cortex: activity- and stress-induced changes. Eur. J. Neurosci. 2009, 29:738-747.
67. MacLullich A.M., et al. Smaller left anterior cingulate cortex volumes are associated with impaired hypothalamic-pituitary-adrenal axis regulation in healthy elderly men. J. Clin. Endocrinol. Metab. 2006, 91:1591-1594.
68. Goel V., Dolan R.J. Differential involvement of left prefrontal cortex in inductive and deductive reasoning. Cognition 2004, 93:B109-B121.
69. Reverberi C., et al. Specific impairments of rule induction in different frontal lobe subgroups. Neuropsychologia 2005, 43:460-472.
70. Corballis P.M. Visuospatial processing and the right-hemisphere interpreter. Brain Cogn. 2003, 53:171-176.
71. Goel V., et al. Dissociation of mechanisms underlying syllogistic reasoning. Neuroimage 2000, 12:504-514.
72. Drevets W.C., et al. Functional anatomical correlates of antidepressant drug treatment assessed using PET measures of regional glucose metabolism. Eur. Neuropsychopharmacol. 2002, 12:527-544.
73. Goldapple K., et al. Modulation of cortical-limbic pathways in major depression: treatment-specific effects of cognitive behavior therapy. Arch. Gen. Psychiatry 2004, 61:34-41.
74. Cerqueira J.J., et al. The prefrontal cortex as a key target of the maladaptive response to stress. J. Neurosci. 2007, 27:2781-2787.
75. Brown S.M., et al. Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb. Cortex 2005, 15:1714-1722.
76. Izquierdo A., et al. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J. Neurosci. 2006, 26:5733-5738.
77. Sotiropoulos I., et al. Stress acts cumulatively to precipitate Alzheimer's disease-like tau pathology and cognitive deficits. J. Neurosci. 2011, 31:7840-7847.
78. Lee Y.A., et al. Dorsal-ventral distinction of chronic stress-induced electrophysiological alterations in the rat medial prefrontal cortex. Neuroscience 2011, 183:108-120.
79. Benchenanne K., et al. Coherent theta oscillations and reorganization of spike timing in the hippocampal-prefrontal network upon learning. Neuron 2010, 66:921-936.
80. Jones M.W., Wilson M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol. 2005, 3:e402.
81. Wilber A.A., et al. Chronic stress alters neural activity in medial prefrontal cortex during retrieval of extinction. Neuroscience 2011, 174:115-131.
82. Radley J.J., et al. Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress. Exp. Neurol. 2005, 196:199-203.
83. Bloss E.B., et al. Interactive effects of stress and aging on structural plasticity in the prefrontal cortex. J. Neurosci. 2010, 30:6726-6731.
84. Castrén E. Is mood chemistry?. Nat. Rev. Neurosci. 2005, 6:241-246.
85. Krugers H.J., et al. Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nat. Rev. Neurosci. 2010, 11:675-681.
86. Sandi C. Glucocorticoids act on glutamatergic pathways to affect memory processes. Trends Neurosci. 2011, 34:165-176.
87. Martin K.P., Wellman C.L. NMDA receptor blockade alters stress-induced dendritic remodeling in medial prefrontal cortex. Cereb. Cortex 2011, 21:2366-2373.
88. Yin H.H., Knowlton B.J. The role of the basal ganglia in habit formation. Nat. Rev. Neurosci. 2006, 7:464-476.
89. Dias-Ferreira E., et al. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 2009, 325:621-625.
90. Schwabe L., Wolf O.T. Stress prompts habit behavior in humans. J. Neurosci. 2009, 29:7191-7198.
91. Soares J.M., et al. Stress-induced changes in human decision-making are reversible. Transl. Psychiatry 2012, 2:e131.
92. Schwabe L., et al. Corticosteroids operate as a switch between memory systems. J. Cogn. Neurosci. 2010, 22:1362-1372.
93. Ottersen O.P. Connections of the amygdala of the rat. IV: corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase. J. Comp. Neurol. 1982, 205:30-48.
94. French S.J., Totterdell S. Hippocampal and prefrontal cortical inputs monosynaptically converge with individual projection neurons of the nucleus accumbens. J. Comp. Neurol. 2002, 446:151-165.
95. French S.J., Totterdell S. Individual nucleus accumbens-projection neurons receive both basolateral amygdala and ventral subicular afferents in rats. Neuroscience 2003, 119:19-31.
96. Ressler K.J., Mayberg H.S. Targeting abnormal neural circuits in mood and anxiety disorders, from the laboratory to the clinic. Nat. Neurosci. 2007, 10:1116-1124.
97. McGaugh J.L. Make mild moments memorable, add a little arousal. Trends Cogn. Sci. 2006, 10:345-347.
98. Scheurich A., et al. Experimental evidence for a motivational origin of cognitive impairment in major depression. Psychol. Med. 2008, 38:237-246.
99. Locke H.S., Braver T.S. Motivational influences on cognitive control, behavior, brain activation, and individual differences. Cogn. Affect. Behav. Neurosci. 2008, 8:99-112.
100. Bechara A., et al. Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 2000, 123:2189-2202.
101. Mitra R., et al. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9371-9376.
102. Martin E.I., et al. The neurobiology of anxiety disorders: brain imaging, genetics, and psychoneuroendocrinology. Psychiatr. Clin. North Am. 2009, 32:549-575.
103. Davis M., et al. Roles of the amygdala and bed nucleus of the stria terminalis in fear and anxiety measured with the acoustic startle reflex. Possible relevance to PTSD. Ann. N. Y. Acad. Sci. 1997, 821:305-331.
104. Kavushansky A., Richter-Levin G. Effects of stress and corticosterone on activity and plasticity in the amygdala. J. Neurosci. Res. 2006, 84:1580-1587.
105. Rodriguez Manzanares P.A., et al. Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J. Neurosci. 2005, 25:8725-8734.
106. Maroun M., Richter-Levin G. Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J. Neurosci. 2003, 23:4406-4409.
107. O'Donnell P., Grace A.A. Synaptic interactions among excitatory afferents to nucleus accumbens neurons, hippocampal gating of prefrontal cortical input. J. Neurosci. 1995, 15:3622-3639.
108. Maggio N., Segal M. Differential modulation of long-term depression by acute stress in the rat dorsal and ventral hippocampus. J. Neurosci. 2009, 29:8633-8638.
109. Adhikari A., et al. Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 2010, 65:257-269.
110. Bhatnagar S., et al. Regulation of chronic stress-induced changes in hypothalamic-pituitary-adrenal activity by the basolateral amygdala. Ann. N. Y. Acad. Sci. 2004, 1032:315-319.
111. Sapolsky R.M. Why stress is bad for your brain. Science 1996, 273:749-750.
112. Liston C., et al. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J. Neurosci. 2006, 26:7870-7874.
113. Di S., et al. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J. Neurosci. 2003, 23:4850-4857.
114. Karst H., et al. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:19204-19207.
115. Riedemann T., et al. Corticosteroids: way upstream. Mol. Brain 2010, 3:2.