Effects of chronic stress in adolescence on learned fear, anxiety, and synaptic transmission in the rat prelimbic cortex

Behavioural Brain Research

Volumn 259, Issue , 2014, Pages 342-353

  Negrón Oyarzo, Ignacio ^a   Pérez, Miguel Ángel ^a   Terreros, Gonzalo ^a   Muñoz, Pablo ^a   Dagnino Subiabre, Alexies ^a  

^a UNIVERSIDAD DE VALPARAÍSO   (Chile)

Author keywords

Adolescence; Anxiety; Learned fear; Prelimbic cortex; Stress; Synaptic transmission

Indexed keywords

ACUTE STRESS; ADOLESCENCE; ADULTHOOD; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN CORTEX; BRAIN SLICE; CHRONIC STRESS; CONDITIONING; CONTROLLED STUDY; DARK LIGHT BOX TEST; ELEVATED PLUS MAZE TEST; EXPERIMENTAL TEST; FEAR; IMMOBILIZATION STRESS; LEARNING; MALE; NEUROBIOLOGY; NONHUMAN; PERINATAL PERIOD; POSTSYNAPTIC POTENTIAL; PRELIMBIC CORTEX; PRIORITY JOURNAL; RAT; REINFORCEMENT; SYNAPTIC TRANSMISSION;

ADOLESCENCE; ANXIETY; LEARNED FEAR; PRELIMBIC CORTEX; STRESS; SYNAPTIC TRANSMISSION;

ADAPTATION, OCULAR; AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; ANXIETY; ELECTRIC STIMULATION; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; MALE; MAZE LEARNING; MOTOR ACTIVITY; PATCH-CLAMP TECHNIQUES; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL; SYNAPTIC TRANSMISSION;

EID: 84889574356     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.11.001     Document Type: Article

References (68)

1. Abush H., Akirav I. Cannabinoids ameliorate impairments induced by chronic stress to synaptic plasticity and short-term memory. Neuropsychopharmacology 2013, 38(8):1521-1534.
2. Avishai-Eliner S., Hatalski C.G., Tabachnik E., Eghbal-Ahmadi M., Baram T.Z. Differential regulation of glucocorticoid receptor messenger RNA (GR-mRNA) by maternal deprivation in immature rat hypothalamus and limbic regions. Brain Res Dev Brain Res 1999, 114(2):265-268.
3. Bagley J., Moghaddam B. Temporal dynamics of glutamate efflux in the prefrontal cortex and in the hippocampus following repeated stress: effects of pretreatment with saline or diazepam. Neuroscience 1997, 77:65-73.
4. Baran S.E., Armstrong C.E., Niren D.C., Hanna J.J., Conrad C.D. Chronic stress and sex differences on the recall of fear conditioning and extinction. Neurobiol Learn Mem 2009, 91:323-332.
5. Brown S.M., Henning S., Wellman C.L. Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex 2005, 15:1714-1722.
6. Burgos-Robles A., Vidal-Gonzalez I., Quirk G.J. Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. J Neurosci 2009, 29(26):8474-8482.
7. Calabrese E.J., Bachmann K.A., Bailer A.J., Bolger P.M., Borak J., Cai L., et al. Biological stress response terminology: Integrating the concepts of adaptive response and preconditioning stress within a hormetic dose-response framework. Toxicol Appl Pharmacol 2007, 222(1):122-128.
8. Chareyron L.J., Lavenex P.B., Lavenex P. Postnatal development of the amygdala: a stereological study in rats. J Comp Neurol 2012, 520(16):3745-3763.
9. Conrad C.D., LeDoux J.E., Magariños A.M., McEwen B.S. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal dendritic atrophy. Behav Neurosci 1999, 113:902-913.
10. Cook S.C., Wellman C.L. Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 2004, 60:236-248.
11. Dahl R.E. Adolescent brain development: a period of vulnerabilities and opportunities. Keynote address. Ann N Y Acad Sci 2004, 1021:1-22.
12. Davis M., Walker D.L., Miles L., Grillon C. Phasic vs sustained fear in rats and humans: role of the extended amygdala in fear vs anxiety. Neuropsychopharmacol Rev 2010, 35:105-135.
13. Davis M. Are different parts of the extended amygdala involved in fear versus anxiety. Biol Psychiatry 1998, 44:1239-1247.
14. Delgado M.R., Nearing K.I., Ledoux J.E., Phelps E.A. Neural circuitry underlying the regulation of conditioned fear and its relation to extinction. Neuron 2008, 59:829-838.
15. Eiland L., Ramroop J., Hill M.N., Manley J., McEwen B.S. Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 2012, 37(1):39-47.
16. Foilb A.R., Lui P., Romeo R.D. The transformation of hormonal stress responses throughout puberty and adolescence. J Endocrinol 2011, 210(3):391-398.
17. Garcia R., Spennato G., Nilsson-Todd L., Moreau J.L., Deschaux O. Hippocampal low-frequency stimulation and chronic mild stress similarly disrupt fear extinction memory in rats. Neurobiol Learn Mem 2008, 89:560-566.
18. Goldwater D.S., Pavlides C., Hunter R.G., Bloss E.B., Hof P.R., McEwen B.S., et al. Structural and functional alterations to rat medial prefrontal cortex following chronic restraint stress and recovery. Neuroscience 2009, 164(2):798-808.
19. Gomez F., Houshyar H., Dallman M.F. Marked regulatory shifts in gonadal, adrenal, and metabolic system responses to repeated restraint stress occur within a 3-week period in pubertal male rats. Endocrinology 2002, 143(8):2852-2862.
20. Gourley S.L., Kedves A.T., Olausson P., Taylor J.R. A history of corticosterone exposure regulates fear extinction and cortical NR2B, GluR2/3, and BDNF. Neuropsychopharmacology 2009, 234(3):707-716.
21. Gourley S.L., Swanson A.M., Koleske A.J. Corticosteroid-induced neural remodeling predicts behavioral vulnerability and resilience. J Neurosci 2013, 33(7):3107-3112.
22. Indovina I., Robbins T.W., Núñez-Elizalde A.O., Dunn B.D., Bishop S.J. Fear-conditioning mechanisms associated with trait vulnerability to anxiety in humans. Neuron 2011, 69:563-571.
23. Kiss J.Z., Troncoso E., Djebbara Z., Vutskits L., Muller D. The role of neural cell adhesion molecules in plasticity and repair. Brain Res Rev 2001, 36(2-3):175-184.
24. Kolb B., Mychasiuk R., Muhammad A., Li Y., Frost D.O., Gibb R. Experience and the developing prefrontal cortex. Proc Natl Acad Sci U S A 2012, 16:109.
25. LeDoux J.E. Emotion circuits in the brain. Annu Rev Neurosci 2000, 23:155-184.
26. Lewis E.M., Barnett J.F., Freshwater L., Hoberman A.M., Christian M.S. Sexual maturation data for Crl Sprague-Dawley rats: criteria and confounding factors. Drug Chem Toxicol 2002, 25(4):437-458.
27. Liston C., McEwen B.S., Casey B.J. Psychosocial stress reversibly disrupts prefrontal processing and attentional control. Proc Natl Acad Sci U S A 2009, 106:912-917.
28. Liu R.J., Aghajanian G.K. Stress blunts serotonin- and hypocretin-evoked EPSCs in prefrontal cortex: role of corticosterone-mediated apical dendritic atrophy. Proc Natl Acad Sci U S A 2008, 105(1):359-364.
29. Lu B., Nagappan G., Guan X., Nathan P.J., Wren P. BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases. Nat Rev Neurosci 2013, 14(6):401-416.
30. Markham J.A., Mullins S.E., Koenig J.I. Periadolescent maturation of the prefrontal cortex is sex-specific and is disrupted by prenatal stress. J Comp Neurol 2013 Jun 1, 521(8):1828-1843.
31. McCormick C.M., Mathews I.Z., Thomas C., Waters P. Investigations of HPA function and the enduring consequences of stressors in adolescence in animal models. Brain Cogn 2010, 72(1):73-85.
32. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 2007, 87(3):873-904.
33. McLaughlin K.J., Gomez J.L., Baran S.E., Conrad C.D. The effects of chronic stress on hippocampal morphology and function: an evaluation of chronic restraint paradigms. Brain Res 2007, 1161:56-64.
34. Michelsen K.A., van den Hove D.L., Schmitz C., Segers O., Prickaerts J., Steinbusch H.W. Prenatal stress and subsequent exposure to chronic mild stress influence dendritic spine density and morphology in the rat medial prefrontal cortex. BMC Neurosci 2007, 8(Dec):107.
35. Milad M.R., Quirk G.J. Fear extinction as a model for translational neuroscience: ten years of progress. Annu Rev Psychol 2012, 63:129-151.
36. Miracle A.D., Brace M.F., Huyck K.D., Singler S.A., Wellman C.L. Chronic stress impairs recall of extinction of conditioned fear. Neurobiol Learn Mem 2006, 85:213-218.
37. Monfils M.H., Cowansage K.K., Klann E., LeDoux J.E. Extinction-reconsolidation boundaries: key to persistent attenuation of fear memories. Science 2009, 324(5929):951-955.
38. Morgan M.A., Romanski L.M., LeDoux J.E. Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci Lett 1993, 163:109-113.
39. Ojeda S.R., Skinner M.K. Puberty in the rat. Physiology of Reproduction 2006, 2061-2126. Elsevier Academic Press, St. Louis, MO. E. Knobil, J.D. Neill (Eds.).
40. Paré D., Quirk G.J., Ledoux J.E. New vistas on amygdala networks in conditioned fear. J Neurophysiol 2004, 92(1):1-9.
41. Pérez M.Á., Pérez-Valenzuela C., Rojas-Thomas F., Ahumada J., Fuenzalida M., Dagnino-Subiabre A. Repeated restraint stress impairs auditory attention and GABAergic synaptic efficacy in the rat auditory cortex. Neuroscience 2013, 246:94-107.
42. Perez-Cruz C., Müller-Keuker J.I., Heilbronner U., Fuchs E., Flügge G. Morphology of pyramidal neurons in the rat prefrontal cortex: lateralized dendritic remodeling by chronic stress. Neural Plast 2007, 2007. article id 46276. 10.1155/2007/46276.
43. Phelps E.A., LeDoux J.E. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 2005, 48:175-187.
44. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 1992, 106:274-285.
45. Pruessner J.C., Baldwin M.W., Dedovic K., Renwick R., Mahani N.K., Lord C., et al. Self-esteem, locus of control, hippocampal volume, and cortisol regulation in young and old adulthood. Neuroimage 2005, 28:815-826.
46. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33(1):56-72.
47. Quirk G.J., Russo G.K., Barron J.L., Lebron K. The role of ventromedial prefrontal cortex in the recovery of extinguished fear. J Neurosci 2000, 20:6225-6231.
48. Radley J.J., Rocher A.B., Janssen W.G., Hof P.R., McEwen B.S., Morrison J.H. Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress. Exp Neurol 2005, 196(1):199-203.
49. Radley J.J., Sisti H.M., Hao J., Rocher A.B., McCall T., Hof P.R., et al. Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 2004, 125:1-6.
50. Reichardt L.F. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 2006, 361(1473):1545-1564.
51. Reznikov L.R., Grillo C.A., Piroli G.G., Pasumarthi R.K., Reagan L.P., Fadel J. Acute stress-mediated increases in extracellular glutamate levels in the rat amygdala: differential effects of antidepressant treatment. Eur J Neurosci 2007, 25:3109-3114.
52. Rodrigues S.M., LeDoux J.E., Sapolsky R.M. The influence of stress hormones on fear circuitry. Annu Rev Neurosci 2009, 32:289-313.
53. Rodrigues S.M., Schafe G.E., LeDoux J.E. Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 2004, 44:75-91.
54. Rogan M.T., Stäubli U.V., LeDoux J.E. Fear conditioning induces associative long-term potentiation in the amygdala. Nature 1997, 390:604-607.
55. Selye H. A syndrome produced by diverse nocuous agents. Nature 1936, 138:32.
56. Sotres-Bayon F., Cain C.K., LeDoux J.E. Brain Mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex. Biol Psychiatry 2006, 60:329-336.
57. Spear L.P. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000, 24(4):417-463.
58. Spear L.P. The psychobiology of adolescence. Authoritative Communities: The Scientific Case for Nurturing the Child (The Search Institute Series on Developmentally Attentive Community and Society) 2007, 263-280. Springer, New York, NY. K. Kline (Ed.).
59. Ulrich-Lai Y.M., Figueiredo H.F., Ostrander M.M., Choi D.C., Engeland W.C., Herman J.P. Chronic stress induces adrenal hyperplasia and hypertrophy in a subregion-specific manner. Am J Physiol Endocrinol Metab 2006, 291:E965-E973.
60. Vidal-Gonzalez I., Vidal-Gonzalez B., Rauch S.L., Quirk G.J. Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 2006, 13(6):728-733.
61. Vyas A., Bernal S., Chattarji S. Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Res 2003, 965:290-294.
62. Vyas A., Chattarji S. Modulation of different states of anxiety-like behavior by chronic stress. Behav Neurosci 2004, 118:1450-1454.
63. Vyas A., Mitra R., Shankaranarayana Rao B.S., Chattarji S. Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons. J Neurosci 2002, 22:6810-6818.
64. Vyas A., Pillai A.G., Chattarji S. Recovery after chronic stress fails to reverse amygdaloid neuronal hypertrophy and enhanced anxiety-like behavior. Neuroscience 2004, 128:667-673.
65. Wall V.L., Fischer E.K., Bland S.T. Isolation rearing attenuates social interaction-induced expression of immediate early gene protein products in the medial prefrontal cortex of male and female rats. Physiol Behav 2012, 107(3):440-450.
66. Wilber A.A., Walker A.G., Southwood C.J., Farrell M.R., Lin G.L., Rebec G.V., et al. Chronic stress alters neural activity in medial prefrontal cortex during retrieval of extinction. Neuroscience 2011, 174:115-131.
67. Yuen E.Y., Wei J., Liu W., Zhong P., Li X., Yan Z. Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron 2012, 873(5):962-977.
68. Zoladz P.R., Park C.R., Halonen J.D., Salim S., Alzoubi K.H., Srivareerat M., et al. Differential expression of molecular markers of synaptic plasticity in the hippocampus, prefrontal cortex, and amygdala in response to spatial learning, predator exposure, and stress-induced amnesia. Hippocampus 2012, 22(3):577-589.