Effects of enrichment predominate over those of chronic stress on fear-related behavior in male rats

References

• Akirav I, Maroun M. The role of the medial prefrontal cortex–amygdala circuit in stress effects on the extinction of fear. Neural Plast 2007; 30873
   Google Scholar
• Berman RF, Hannigan JH, Sperry MA, Zajac CS. Prenatal alcohol exposure and the effects of environmental enrichment on hippocampal dendritic spine density. Alcohol 1996; 13: 209–216
   PubMed Web of Science ®Google Scholar
• Bindu B, Alladi PA, Mansooralikhan BM, Srikumar BN, Raju TR, Kutty BM. Short-term exposure to an enriched environment enhances dendritic branching but not brain-derived neurotrophic factor expression in the hippocampus of rats with ventral subicular lesions. Neuroscience 2007; 144: 412–423
   PubMed Web of Science ®Google Scholar
• Bouton ME. Context and behavioral processes in extinction. Learn Mem 2004; 11: 485–494
   PubMed Web of Science ®Google Scholar
• Bouton ME, Westbrook RF, Corcoran KA, Maren S. Contextual and temporal modulation of extinction: Behavioral and biological mechanisms. Biol Psychiatry 2006; 60: 352–360
   PubMed Web of Science ®Google Scholar
• Bruel-Jungerman E, Laroche S, Rampon C. New neurons in the dentate gyrus are involved in the expression of enhanced long-term memory following environmental enrichment. Eur J Neurosci 2005; 21: 513–521
   PubMed Web of Science ®Google Scholar
• Conrad CD, LeDoux JE, Magarinos AM, McEwen BS. Repeated restraint stress facilitates fear conditioning independently of causing hippocampal CA3 dendritic atrophy. Behav Neurosci 1999; 113: 902–913
   PubMed Web of Science ®Google Scholar
• Corcoran KA, Maren S. Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction. Learn Mem 2004; 11: 598–603
   Google Scholar
• Corcoran KA, Quirk GJ. Recalling safety: cooperative functions of the ventromedial prefrontal cortex and the hippocampus in extinction. CNS Spectr 2007; 12: 200–206
   Google Scholar
• Corcoran KA, Desmond TJ, Frey KA, Maren S. Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J Neurosci 2005; 25: 8978–8987
   PubMed Web of Science ®Google Scholar
• Diamond DM, Fleshner M, Ingersoll N, Rose GM. Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. Behav Neurosci 1996; 110: 661–672
   PubMed Web of Science ®Google Scholar
• Effting M, Kindt M. Contextual control of human fear associations in a renewal paradigm. Behav Res Ther 2007; 45: 2002–2018
   PubMed Web of Science ®Google Scholar
• Gaulke LJ, Horner PJ, Fink AJ, McNamara CL, Hicks RR. Environmental enrichment increases progenitor cell survival in the dentate gyrus following lateral fluid percussion injury. Brain Res Mol Brain Res 2005; 141: 138–150
   PubMedGoogle Scholar
• Harris JA, Jones ML, Bailey GK, Westbrook RF. Contextual control over conditioned responding in an extinction paradigm. J Exp Psychol Anim Behav Process 2000; 26: 174–185
   PubMed Web of Science ®Google Scholar
• Izquierdo A, Wellman CL, Holmes A. Brief uncontrollable stress causes dendritic retraction in infralimbic cortex and resistance to fear extinction in mice. J Neurosci 2006; 26: 5733–5738
   PubMed Web of Science ®Google Scholar
• Ji J, Maren S. Electrolytic lesions of the dorsal hippocampus disrupt renewal of conditional fear after extinction. Learn Mem 2005; 12: 270–276
   PubMed Web of Science ®Google Scholar
• Ji J, Maren S. Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 2007; 17: 749–758
   PubMed Web of Science ®Google Scholar
• Kim JJ, Lee HJ, Welday AC, Song E, Cho J, Sharp PE, Jung MW, Blair HT. Stress-induced alterations in hippocampal plasticity, place cells, and spatial memory. Proc Natl Acad Sci USA 2007; 104: 18297–18302
   PubMed Web of Science ®Google Scholar
• LeDoux JE, Sakaguchi A, Reis DJ. Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. J Neurosci 1984; 4: 683–698
   PubMed Web of Science ®Google Scholar
• Lee KJ, Kim SJ, Kim SW, Choi SH, Shin YC, Park SH, Moon BH, Cho E, Lee MS, Chun BG, Shin KH. Chronic mild stress decreases survival, but not proliferation, of new-born cells in adult rat hippocampus. Exp Mol Med 2006; 38: 44–54
   Google Scholar
• Leggio MG, Mandolesi L, Federico F, Spirito F, Ricci B, Gelfo F, Petrosini L. Environmental enrichment promotes improved spatial abilities and enhanced dendritic growth in the rat. Behav Brain Res 2005; 163: 78–90
   PubMed Web of Science ®Google Scholar
• Luine V, Villegas M, Martinez C, McEwen BS. Repeated stress causes reversible impairments of spatial memory performance. Brain Res 1994; 639: 167–170
   PubMed Web of Science ®Google Scholar
• Magarinos AM, McEwen BS. Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: Comparison of stressors. Neuroscience 1995; 69: 83–88
   PubMed Web of Science ®Google Scholar
• McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci 1999; 22: 105–122
   PubMed Web of Science ®Google Scholar
• McEwen BS. Plasticity of the hippocampus: Adaptation to chronic stress and allostatic load. Ann NY Acad Sci 2001; 933: 265–277
   PubMed Web of Science ®Google Scholar
• Miracle AD, Brace MF, Huyck KD, Singler SA, Wellman CL. Chronic stress impairs recall of extinction of conditioned fear. Neurobiol Learn Mem 2006; 85: 213–218
   PubMedGoogle Scholar
• Mitra R, Jadhav S, McEwen BS, Vyas A, Chattarji S. Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala. Proc Natl Acad Sci USA 2005; 102: 9371–9376
   PubMed Web of Science ®Google Scholar
• Murmu MS, Salomon S, Biala Y, Weinstock M, Braun K, Bock J. Changes of spine density and dendritic complexity in the prefrontal cortex in offspring of mothers exposed to stress during pregnancy. Eur J Neurosci 2006; 24: 1477–1487
   PubMed Web of Science ®Google Scholar
• Parker LA, Limebeer CL, Slomke J. Renewal effect: context-dependent extinction of a cocaine- and a morphine-induced conditioned floor preference. Psychopharmacology (Berl) 2006; 187: 133–137
   Google Scholar
• Radley JJ, Rocher AB, Miller M, Janssen WG, Liston C, Hof PR, McEwen BS, Morrison JH. Repeated stress induces dendritic spine loss in the rat medial prefrontal cortex. Cereb Cortex 2006; 16: 313–320
   PubMed Web of Science ®Google Scholar
• Rampon C, Tang YP, Goodhouse J, Shimizu E, Kyin M, Tsien JZ. Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1–knockout mice. Nat Neurosci 2000; 3: 238–244
   PubMed Web of Science ®Google Scholar
• Rodriguez Manzanares PA, Isoardi NA, Carrer HF, Molina VA. Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J Neurosci 2005; 25: 8725–8734
   PubMed Web of Science ®Google Scholar
• Rovee-Collier C, Dufault D. Multiple contexts and memory retrieval at three months. Dev Psychobiol 1991; 24: 39–49
   Google Scholar
• Segovia G, Yague AG, Garcia-Verdugo JM, Mora F. Environmental enrichment promotes neurogenesis and changes the extracellular concentrations of glutamate and GABA in the hippocampus of aged rats. Brain Res Bull 2006; 70: 8–14
   PubMed Web of Science ®Google Scholar
• Servatius RJ, Shors TJ. Exposure to inescapable stress persistently facilitates associative and nonassociative learning in rats. Behav Neurosci 1994; 108: 1101–1106
   Google Scholar
• Thomas RM, Hotsenpiller G, Peterson DA. Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J Neurosci 2007; 27: 2734–2743
   PubMed Web of Science ®Google Scholar
• Vyas A, Mitra R, Chattarji S. Enhanced anxiety and hypertrophy in basolateral amygdala neurons following chronic stress in rats. Annals of New York Academy of Sciences 2003; 985: 554–555
   Google Scholar
• Wright RL, Conrad CD. Enriched environment prevents chronic stress-induced spatial learning and memory deficits. Behav Brain Res 2007; 187: 41–47
   Google Scholar
• Yang J, Hou C, Ma N, Liu J, Zhang Y, Zhou J, Xu L, Li L. Enriched environment treatment restores impaired hippocampal synaptic plasticity and cognitive deficits induced by prenatal chronic stress. Neurobiol Learn Mem 2007; 87: 257–263
   PubMed Web of Science ®Google Scholar