Stress, synaptic plasticity, and psychopathology

Reviews in the Neurosciences

Volumn 13, Issue 3, 2002, Pages 195-208

  Garcia, René ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Animal models of affective disorders; Depression; Hippocampus; Lateral septum; Medial prefrontal cortex; Post traumatic stress disorder; Stress; Synaptic plasticity

Indexed keywords

AFFECTIVE NEUROSIS; ANIMAL MODEL; CONDITIONING; DEPRESSION; DISEASE MODEL; EMOTION; EXCITABILITY; FORCED SWIMMING TEST; HIPPOCAMPUS; HUMAN; LEARNED HELPLESSNESS; LONG TERM POTENTIATION; MENTAL DISEASE; NERVE CELL PLASTICITY; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; PREFRONTAL CORTEX; PRIORITY JOURNAL; REINFORCEMENT; REVIEW; SEPTUM PELLUCIDUM; STRESS;

EID: 0036397762     PISSN: 03341763     EISSN: None     Source Type: Journal    
DOI: 10.1515/REVNEURO.2002.13.3.195     Document Type: Review

References (115)

1. Begic D, Hotujac L, Jokic-Begic N. Electroencephalographic comparison of veterans with combat-related post-traumatic stress disorder and healthy subjects. Int J Psychophysiol 2001; 40: 167-172.
2. Benjaminsen S. Stressful life events preceding the onset of neurotic depression. Psychol Med 1981; 11: 369-378.
3. Bliss TVP, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993; 361: 31-39.
4. Bonne O, Brandes D, Gilboa A, Gomori JM, Shenton ME, Pitman RK, Shalev AY. Longitudinal MRI study of hippocampal volume in trauma survivors with PTSD. Am J Psychiatry 2001; 158: 1248-1251.
5. Bremner JD, Randall P, Scott TM, Bronen RA, Seibyl JP, Southwick SM, Delaney RC, McCarthy G, Charney DS, Innis RB. MRI-based measurement of hippocampal volume in patients with combat-related posttraumatic stress disorder. Am J Psychiatry 1995; 152: 973-981.
6. Bremner JD, Randall P, Vermetten E, Staib L, Bronen RA, Mazure C, Capelli S, McCarthy G, Innis RB, Charney DS. Magnetic resonance imaging-based measurement of hippocampal volume in posttraumatic stress disorder related to childhood physical and sexual abuse - a preliminary report. Biol Psychiatry 1997; 41: 23-32.
7. Bremner JD, Innis RB, Ng CK, Staib LH, Salomon RM, Bronen RA, Duncan J, Southwick SM, Krystal JH, Rich D, Zubal G, Dey H, Soufer R, Charney DS. Positron emission tomography measurement of cerebral metabolic correlates of yohimbine administration in combat-related posttraumatic stress disorder. Arch Gen Psychiatry 1997; 54: 246-254.
8. Bremner JD, Narayan M, Staib LH, Southwick SM, McGlashan T, Charney DS. Neural correlates of memories of childhood sexual abuse in women with and without posttraumatic stress disorder. Am J Psychiatry 1999; 156: 1787-1795.
9. Bremner JD, Staib LH, Kaloupek D, Southwick SM, Sooufer R, Charney DS. Neural correlates of exposure to traumatic pictures and sound in Vietnam combat veterans with and without posttraumatic stress disorder: a positron emission tomography study. Biol Psychiatry 1999; 45: 806-816.
10. Bremner JD, Innis RB, Southwick SM, Staib L, Zoghbi S, Charney DS. Decreased benzodiazepine receptor binding in prefrontal cortex in combat-related posttraumatic stress disorder. Am J Psychiatry 2000; 157: 1120-1126.
11. Brewin CR. A cognitive neuroscience account of posttraumatic stress disorder and its treatment. Behav Res Ther 2001; 39: 373-393.
12. Casada JH, Amdur R, Larsen R, Liberzon I. Psychophysiologic responsivity in posttraumatic stress disorder: generalized hyperresponsiveness versus trauma specificity. Biol Psychiatry 1998; 44: 1037-1044.
13. Chen B, Dowlatshahi D, MacQueen GM, Wang JF, Young LT. Increased hippocampal BDNF immunoreactivity in subjects treated with antidepressant medication. Biol Psychiatry 2001; 50: 260-265.
14. Clugnet MC, LeDoux JE. Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body. J Neurosci 1990; 10: 2818-2824.
15. Contreras CM, Lara-Morales H, Molina-Hernandez M, Saavedra M, Arrellin-Rosas G. An early lesion of the lateral septal nuclei produces changes in the forced swim test depending on gender. Prog Neuropsychopharmacol Biol Psychiatry 1995; 19: 1277-1284.
16. Contreras CM, Rodriguez-Landa JF, Gutierrez-Garcia AG, Bernal-Morales B. The lowest effective dose of fluoxetine in the forced swim test significantly affects the firing rate of lateral septal nucleus neurones in the rat. J Psychopharmacol 2001; 15: 231-236.
17. Desmedt A, Garcia R, Jaffard R. Differential modulation of changes in hippocampal-septal synaptic excitability by the amygdala as a function of either elemental or contextual fear conditioning in mice. J Neurosci 1998; 18: 480-487.
18. Dias R, Aggleton JP. Effects of selective excitotoxic prefrontal lesions on acquisition of nonmatching- and matching-to-place in the T-maze in the rat: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility. Eur J Neurosci 2000; 12: 4457-4466.
19. Dunnett SB, Nathwani F, Brasted PJ. Medial prefrontal and neostriatal lesions disrupt performance in an operant delayed alternation task in rats. Behav Brain Res 1999; 106: 13-28.
20. Ebner K, Wotjak CT, Holsboer F, Landgraf R, Engelmann M. Vasopressin released within the septal brain area during swim stress modulates the behavioural stress response in rats. Eur J Neurosci 1999; 11: 997-1002.
21. Eichenbaum H, Clegg RA, Feeley A. Reexamination of functional subdivisions of the rodent prefrontal cortex. Exp Neurol 1983; 79: 434-451.
22. Ettedgui E, Bridges M. Posttraumatic stress disorder. Psychiatr Clin N Am 1985; 8: 89-103.
23. Fernandez, M, Pissiota A, Frans O, Knorring LV, Fischer H, Fredrikson M. Brain function in patient with torture related post-traumatic stress disorder before and after fluoxetine treatment: a positron emission tomography provocation study. Neurosci Lett 2001; 297: 101-104.
24. Figurov A, Pozzo-Miller LD, Olafsson P, Wang T, Lu B. Regulation of synaptic responses to high-frequency stimulation and LTP by neurotrophins in the hippocampus. Nature 1996; 381: 706-709.
25. Finlay-Jones R, Brown GW. Types of stressful life event and the onset of anxiety and depressive disorders. Psychol Med 1981; 11: 803-815.
26. Fletcher PC, Frith CD, Rugg MD. The functional neuroanatomy of episodic memory. Trends Neurosci 1997; 20: 213-218.
27. Fliers E, Guldenaar SE, van de Wal N, Swaab DF. Extrahypothalamic vasopressin and oxytocin in the human brain; presence of vasopressin cells in the bed nucleus of the stria terminalis. Brain Res 1986; 375: 363-367.
28. Foa EB, Zinbarg R, Rothbaum BO. Uncontrollability and unpredictability in post-traumatic stress disorder: an animal model. Psychol Bull 1992; 112: 218-238.
29. Foy MR, Stanton ME, Levine S, Thompson RF. Behavioral stress impairs long-term potentiation in rodent hippocampus. Behav Neural Biol 1987; 48: 138-149.
30. Frith C, Dolan R. The role of the prefrontal cortex in higher cognitive functions. Brain Res Cogn Brain Res 1996; 5: 175-181.
31. Garcia R. Stress, hippocampal plasticity, and spatial learning. Synapse 2001; 40: 180-183.
32. Garcia R, Jaffard R. The hippocampo-septal projection in mice: long-term potentiation in the lateral septum. NeuroReport 1992; 3: 193-196.
33. Garcia R, Jaffard R. Changes in synaptic excitability in the lateral septum associated with contextual and auditory fear conditioning in mice. Eur J Neurosci 1996; 8: 809-815.
34. Garcia R, Tocco G, Baudry M, Thompson R. Polysynaptic potentiation in the lateral septum following stimulation of the fimbria in anesthetized rats. Brain Res 1996; 737: 169-174.
35. Garcia R, Musleh W, Tocco G, Baudry M, Thompson RF. Time-dependent blockade of STP and LTP in hippocampal slices following acute stress in mice. Neurosci Lett 1997; 233: 41-44.
36. Garcia R, Vouimba RM, Jaffard R. Contextual conditioned fear blocks the induction but not the maintenance of lateral septal LTP in behaving mice. J Neurophysiol 1997; 78: 76-81.
37. Garcia R, Paquereau J, Vouimba RM, Jaffard R. Footshock stress but not contextual fear conditioning induces long-term enhancement of auditory-evoked potentials in the basolateral amygdala of the freely behaving rat. Eur J Neurosci 1998; 10: 457-463.
38. Garcia R, Tocco G, Baudry M, Thompson RF. Exposure to a conditioned aversive environment interferes with long-term potentiation induction in the fimbria-CA3 pathway. Neuroscience 1998; 82: 139-145.
39. Garcia R, Vouimba RM, Baudry M, Thompson RF. The amygdala modulates prefrontal cortex activity relative to conditioned fear. Nature 1999; 402: 294-296.
40. Gemmell C, O'Mara SM. Medial prefrontal cortex lesions cause deficits in a variable-goal location task but not in object exploration. Behav Neurosci 1999; 113: 465-474.
41. Glass RM, Uhlenhuth EH, Hartel FW, Matuzas W, Fischman MW. Cognitive dysfunction and imipramine in outpatient depressive. Arch Gen Psychiatry 1981; 38: 1048-1051.
42. Gurvits TV, Shenton ME, Hokama H, Ohta H, Lasko NB, Gilbertson MW, Orr SP, Kikinis R, Jolesz FA, McCarley RW, Pitman RK. Magnetic resonance imaging study of hippocampal volume in chronic, combat-related posttraumatic stress disorder. Biol Psychiatry 1996; 40: 1091-1099.
43. Hauser MD. Perseveration, inhibition and the prefrontal cortex: a new look. Curr Opin Neurobiol 1999; 9: 214-222.
44. Herry C, Garcia R. Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. J Neurosci 2002; 22: 577-583.
45. Herry C, Vouimba RM, Garcia R. Plasticity in the thalamo-prefrontal cortical transmission in behaving mice. J Neurophysiol 1999; 82: 2827-2832.
46. Joëls M, Urban IJ. Arginine-vasopressin enhances the responses of lateral septal neurons in the rat to excitatory amino acids and fimbria-fornix stimuli. Brain Res 1984; 311: 201-209.
47. Joëls M, de Kloet ER. Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. Science 1989; 245: 1502-1505.
48. Kang H, Schuman EM. Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 1995; 267: 1658-1662.
49. Khanna S, Sinclair JG. Noxious stimuli produce prolonged changes in the CA1 region of the rat hippocampus. Pain 1989; 39: 337-343.
50. Khanna S, Sinclair JG. Responses in the CA1 region of the rat hippocampus to a noxious stimulus. Exp Neurol 1992; 117: 28-35.
51. Kim JJ, Fanselow MS. Modality-specific retrograde amnesia of fear. Science 1992; 256: 675-677.
52. Kim JJ, Foy MR, Thompson RF. Behavioral stress modifies hippocampal plasticity through N-methyl-D-aspartate receptor activation. Proc Natl Acad Sci USA 1996; 93: 4750-4753.
53. Klein SB. Learning. Principles and Applications, 3rd Ed. New York: McGraw-Hill, 1996.
54. Kollack-Walker S, Don C, Watson SJ, Akil H. Differential expression of c-fos mRNA within neurocircuits of male hamsters exposed to acute or chronic defeat. J Neuroendocrinol 1999; 11: 547-559.
55. Koopman C, Classen C, Cardena E, Spiegel D. When disaster strikes, acute stress disorder may follow. J Trauma Stress 1995; 8: 29-46.
56. Korte SM, De Kloet ER, Buwalda B, Bouman SD, Bohus B. Antisense to the glucocorticoid receptor in hippocampal dentate gyrus reduces immobility in forced swim test. Eur J Pharmacol 1996; 301: 19-25.
57. LeDoux, JE. Emotional memory systems in the brain. Behav Brain Res 1993; 58: 69-79.
58. LeDoux, JE. Emotion: clues from brain. Annu Rev Psychol 1995; 46: 209-235.
59. LeDoux JE. Emotion circuits in the brain. Annu Rev Neurosci 2000; 23: 155-184.
60. Ledoux JE, Muller J. Emotional memory and psychopathology. Philos Trans R Soc Lond B Biol Sci 1997; 352: 1719-1726.
61. Lipska BK, Weinberger DR. To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 2000; 23: 223-239.
62. Loup F, Tribollet E, Dubois-Dauphin M, Dreifuss JJ. Localization of high-affinity binding sites for oxytocin and vasopressin in the human brain. An autoradiographic study. Brain Res 1991; 555: 220-232.
63. Lynch G, Baudry M. The biochemistry of memory: a new and specific hypothesis. Science 1984; 224: 1057-1063.
64. Ma YL, Wang HL, Wu HC, Wei CL, Lee EH. Brain-derived neurotrophic factor antisense oligonucleotide impairs memory retention and inhibits long-term potentiation in rats. Neuroscience 1998; 82: 957-967.
65. Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 1995; 69: 83-88.
66. Maren S. Synaptic transmission and plasticity in the amygdala. An emerging physiology of fear conditioning circuits. Mol Neurobiol 1996; 13: 1-22.
67. Maren S. Neurobiology of Pavlovian fear conditioning. Annu Rev Neurosci 2001; 24: 897-931.
68. Maren S, Fanselow, MS. Synaptic plasticity in the basolateral amygdala induced by hippocampal formation stimulation in vivo. J Neurosci 1995; 15: 7548-c4 7564.
69. Medina JF, Christopher Repa J, Mauk MD, LeDoux JE. Parallels between cerebellum- and amygdala-dependent conditioning. Nat Rev Neurosci 2002; 3: 122-131.
70. Miyata S, Itoh T, Matsushima O, Nakashima T, Kiyohara T. Not only osmotic stress but also repeated restraint stress causes structural plasticity in the supraoptic nucleus of the rat hypothalamus. Brain Res Bull 1994; 33: 669-675.
71. Morgan MA, LeDoux JE. Differential contribution of dorsal and ventral medial prefrontal cortex to acquisition and extinction of conditioned fear in rats. Behav Neurosci 1995; 109: 681-688.
72. Morgan MA, Romanski LM, LeDoux JE. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 1993; 163: 109-113.
73. Müller MB, Toschi N, Kresse AE, Post A, Keck ME. Long-term repetitive transcranial magnetic stimulation increases the expression of brain-derived neurotrophic factor and cholecystokinin mRNA, but not neuropeptide tyrosine mRNA in specific areas of rat brain. Neuropsychopharmacology 2000; 23: 205-215.
74. Nail-Boucherie K, Garcia R, Jaffard R. Influences of the bed nucleus of the stria terminalis and of the paraventricular nucleus of the hypothalamus on the excitability of hippocampal-lateral septal synapses in mice. Neurosci Lett 1998; 246: 112-116.
75. Nibuya M, Morinobu S, Duman RS. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 1995; 15: 7539-7547.
76. Overmier JB, Seligman ME. Effects of inescapable shock upon subsequent escape and avoidance responding. J Comp Physiol Psychol 1967; 63: 28-33.
77. Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, Kandel ER. Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 1996; 16: 1137-1145.
78. Phillips RG, LeDoux JE. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992; 106: 274-285.
79. Pitman RK, Shin LM, Rauch SL. Investigating the pathogenesis of posttraumatic stress disorder with neuroimaging. J Clin Psychiatry 2001; 62 (Suppl 17): 47-54.
80. Porsolt RD, Bertin A, Jalfre M. "Behavioural despair" in rats and mice: strain differences and the effects of imipramine. Eur J Pharmacol 1978; 51: 291-294.
81. Porsolt RD, Anton G, Blavet N, Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 1978; 47: 379-391.
82. Quirk GJ, Russo GK, Barron JL, Lebron, K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 2000; 20: 6225-6231.
83. Reiman EM, Lane RD, Ahern GL, Schwartz GE, Davidson RJ, Friston KJ, Yuri LS, Chen K. Neuroanatomical correlates of externally and internally generated human emotion. Am J Psychiatry 1997; 154: 918-925.
84. Rogan MT, Stäubli UV, LeDoux JE. Fear conditioning induces associative long-term potentiation in the amygdala. Nature, 1997; 390: 604-607.
85. Rosenkranz JA, Grace AA. Modulation of basolateral amygdala neuronal firing and afferent drive by dopamine receptor activation in vivo. J Neurosci 1999; 19: 11027-11039.
86. Rosenkranz JA, Grace AA. Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. J Neurosci 2001; 21: 4090-4103.
87. Rosenkranz JA, Grace AA. Cellular mechanisms of infralimbic and prelimbic prefrontal cortical inhibition and dopaminergic modulation of basolateral amygdala neurons in vivo. J Neurosci 2002; 22: 324-337.
88. Sanchez-Toscano F, Sanchez MM, Garzon J. Changes in the number of dendritic spines in the medial preoptic area during a premature long-term social isolation in rats. Neurosci Lett 1991; 122: 1-3.
89. Sapolsky RM. The possibility of neurotoxicity in the hippocampus in major depression: a primer on neuron death. Biol Psychiatry 2000; 48: 755-765.
90. Scharfman HE, Goodman JH, Sollas AL. Actions of brain-derived neurotrophic factor in slices from rats with spontaneous seizures and mossy fiber sprouting in the dentate gyrus. J Neurosci 1999; 19: 5619-5631.
91. Schulz D, Canbeyli RS. Lesion of the bed nucleus of the stria terminalis enhances learned despair. Brain Res Bull 2000; 52: 83-87.
92. Seligman ME, Maier SF. Failure to escape traumatic shock. J Exp Psychol 1967; 74: 1-9.
93. Sherman AD, Sacquitne JL, Petty F. Specificity of the learned helplessness model of depression. Pharmacol Biochem Behav 1982; 16: 449-454.
94. Shirayama Y, Chen AC, Nakagawa S, Russell DS, Duman RS. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J Neurosci 2002; 22: 3251-3261.
95. Shors TL, Thompson RF. Acute stress impairs (or induces) synaptic long-term potentiation (LTP) but does not affect paired-pulse facilitation in the stratum radiatum of the rat hippocampus. Synapse 1992; 11: 262-265.
96. Shors TL, Seib TB, Levine S, Thompson RF. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 1989; 244: 224-226.
97. Siuciak JA, Lewis DR, Wiegand SJ, Lindsay RM. Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol Biochem Behav 1997; 56: 131-137.
98. Smith MA, Makino S, Kvetnansky R, Post RM. Stress and glucocorticoids affect the expression of brain-derived neurotrophic factor and neurotrophin-3 mRNAs in the hippocampus. J Neurosci 1995; 15: 1768-1777.
99. Stevens DR, Cotman CW. Long-term potentiation of excitatory and inhibitory synaptic potentials in the hippocampal-septal projection of the rat. Brain Res 1991; 558: 120-122.
100. Surtees PG, Barkley C. Future imperfect: the long-term outcome of depression. Br J Psychiatry 1994; 164: 327-341.
101. Swanson LW, Cowan WM. The connections of the septal region in the rat. J Comp Neurol 1979; 186: 621-656.
102. Tarrier N, Sommerfield C, Pilgrim H, Humphreys L. Cognitive therapy or imaginal exposure in the treatment of post-traumatic stress disorder. Twelve-month follow-up. Br J Psychiatry 1999; 175: 571-575.
103. Theios J, Lynch AD, Lowe WF Jr. Differential effects of shock intensity on one-way and shuttle avoidance conditioning. J Exp Psychol 1966; 72: 294-299.
104. Thiebot MH, Martin P, Puech AJ. Animal behavioural studies in the evaluation of antidepressant drugs. Br J Psychiatry 1992; Suppl 15: 44-50.
105. Urban IJA, Ontskul A, Croiset G, Cheng Y, De Wied DA. Long-lasting increase and decrease in synaptic excitability in the rat lateral septum are associated with high and low shuttle box performance, respectively. Brain Behav Res 1995; 68: 173-183.
106. Van den Hooff P, Urban IJA, De Wied D. Vasopressin maintains long-term potentiation in rat lateral septum slices. Brain Res 1989; 505: 181-186.
107. Von Frijtag JC, Kamal A, Reijmers LG, Schrama LH, van den Bos R, Spruijt BM. Chronic imipramine treatment partially reverses the long-term changes of hippocampal synaptic plasticity in socially stressed rats. Neurosci Lett 2001; 309: 153-156.
108. Vouimba RM, Garcia R, Jaffard R. Opposite effects of lateral septal LTP and lateral septal lesions on contextual fear conditioning in mice. Behav Neurosci 1998; 112: 875-884.
109. Vouimba RM, Garcia R, Jaffard R. Pretraining tetanic fimbrial stimulation impairs the expression but not the acquisition of contextual fear conditioning in mice. Neuroscience 1999; 93: 869-876.
110. Wanatabe Y, Gould E, McEwen. Stress induces atrophy of apical dendrites of hippocampal CA3 pyramidal neurons. Brain Res 1992; 588: 341-345.
111. Wieland S, Lucki I. Antidepressant-like activity of 5-HT1A agonists measured with the forced swim test. Psychopharmacology (Berl) 1990; 101: 497-504.
112. Yehuda R, McFarlane AC, Shalev AY. Predicting the development of posttraumatic stress disorder from the acute response to a traumatic event. Biol Psychiatry 1998; 44: 1305-1313.
113. Zaczek R, Hedreen JC, Coyle JT. Evidence for a hippocampal-septal glutamatergic pathway in the rat. Exp Neurol 1979; 65: 145-156.
114. Zetterstrom TS, Pei Q, Grahame-Smith DG. Repeated electroconvulsive shock extends the duration of enhanced gene expression for BDNF in rat brain compared with a single administration. Brain Res Mol Brain Res 1998; 57: 106-110.
115. Zubieta JK, Chinitz JA, Lombardi U, Fig LM, Cameron OG, Liberzon I. Medial frontal cortex involvement in PTSD symptoms: a SPECT study. J Psychiatr Res 1999; 33: 259-264.