Heat exposure in female rats elicits abnormal fear expression and cellular changes in prefrontal cortex and hippocampus

Neurobiology of Learning and Memory

Volumn 115, Issue , 2014, Pages 38-42

  Gruene, Tina M ^a   Lipps, Jennifer ^a   Rey, Colin D ^a   Bouck, Anna ^a   Shansky, Rebecca M ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Dendritic spines; Extinction; Fear conditioning; Females; Hippocampus; Prefrontal cortex

Indexed keywords

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL HOUSING; ARTICLE; BRAIN REGION; CONDITIONING; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; FEAR; FEMALE; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; NERVE CELL; NEUROANATOMY; NONHUMAN; PREFRONTAL CORTEX; RAT; RECALL; REINFORCEMENT; THERMAL EXPOSURE; ADVERSE EFFECTS; ANIMAL; BIOSYNTHESIS; CHEMISTRY; CONDITIONED REFLEX; HEAT; HIPPOCAMPUS; LONG EVANS RAT; METABOLISM; PATHOLOGY; PHYSIOLOGY;

PROTEIN C FOS;

ANIMALS; CA3 REGION, HIPPOCAMPAL; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; HIPPOCAMPUS; HOT TEMPERATURE; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, LONG-EVANS;

EID: 84908321755     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2014.05.004     Document Type: Article

References (33)

1. 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. Neurobiology of Learning and Memory 2009, 91:323-332.
2. Bourne J., Harris K.M. Do thin spines learn to be mushroom spines that remember?. Current Opinion in Neurobiology 2007, 17:381-386.
3. Breslau N., Chilcoat H.D., Kessler R.C., Peterson E.L., Lucia V.C. Vulnerability to assaultive violence: Further specification of the sex difference in post-traumatic stress disorder. Psychological Medicine 1999, 29:813-821.
4. DoD (2014). Active duty military personnel by rank/grade (Women Only).
5. Eiland L., McEwen B.S. Early life stress followed by subsequent adult chronic stress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus 2012, 22:82-91.
6. Galea L.a., McEwen B.S., Tanapat P., Deak T., Spencer R.L., Dhabhar F.S. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 1997, 81:689-697.
7. Giachero M., Calfa G.D., Molina V.A. Hippocampal structural plasticity accompanies the resulting contextual fear memory following stress and fear conditioning. Learning & Memory 2013, 20:611-616.
8. Glover E.M., Jovanovic T., Mercer K.B., Kerley K., Bradley B., Ressler K.J., et al. Estrogen levels are associated with extinction deficits in women with posttraumatic stress disorder. Biological Psychiatry 2012, 72:19-24.
9. Graham B.M., Milad M.R. Blockade of estrogen by hormonal contraceptives impairs fear extinction in female rats and women. Biological Psychiatry 2013, 73:371-378.
10. Haskell S.G., Gordon K.S., Mattocks K., Duggal M., Erdos J., Justice A., et al. Gender differences in rates of depression, PTSD, pain, obesity, and military sexual trauma among Connecticut War Veterans of Iraq and Afghanistan. Journal of Women's Health (Larchmt) 2010, 19:267-271.
11. Hoffman A.N., Armstrong C.E., Hanna J.J., Conrad C.D. Chronic stress, cyclic 17β-estradiol, and daily handling influences on fear conditioning in the female rat. Neurobiology of Learning and Memory 2010, 94:422-433.
12. Ji J., Maren S. Differential roles for hippocampal areas CA1 and CA3 in the contextual encoding and retrieval of extinguished fear. Learning & Memory 2008, 15:244-251.
13. Knox D., Nault T., Henderson C., Liberzon I. Glucocorticoid receptors and extinction retention deficits in the single prolonged stress model. Neuroscience 2012, 223:163-173.
14. Lebron-Milad K., Graham B.M., Milad M.R. Low estradiol levels: A vulnerability factor for the development of posttraumatic stress disorder. Biological Psychiatry 2012, 72:6-7.
15. Lebron-Milad K., Milad M.R. Sex differences, gonadal hormones and the fear extinction network: Implications for anxiety disorders. Biology of Mood and Anxiety Disorders 2012, 2:3.
16. Matsuzaki M., Ellis-Davies G.C., Nemoto T., Miyashita Y., Iino M., Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nature Neuroscience 2001, 4:1086-1092.
17. McCormick C.M., Mongillo D.L., Simone J.J. Age and adolescent social stress effects on fear extinction in female rats. Stress 2013, 16:678-688.
18. Milad M.R., Igoe S.A., Lebron-Milad K., Novales J.E. Estrous cycle phase and gonadal hormones influence conditioned fear extinction. Neuroscience 2009, 164:887-895.
19. Peters J., Dieppa-Perea L.M., Melendez L.M., Quirk G.J. Induction of fear extinction with hippocampal-infralimbic BDNF. Science 2010, 328:1288-1290.
20. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
21. Radley J.J., Rocher A.B., Rodriguez A., Ehlenberger D.B., Dammann M., McEwen B.S., et al. Repeated stress alters dendritic spine morphology in the rat medial prefrontal cortex. Journal of Comparative Neurology 2008, 507:1141-1150.
22. Rey C.D., Lipps J., Shansky R.M. Dopamine D1-receptor activation rescues extinction impairments in low-estrogen female rats and induces cortical layer-specific activation changes in prefrontal-amygdala circuits. Neuropsychopharmacology 2013, 10.1038/npp.2013.338.
23. Santos M., D'Amico D., Spadoni O., Amador-Arjona A., Stork O., Dierssen M. Hippocampal hyperexcitability underlies enhanced fear memories in TgNTRK3, a panic disorder mouse model. The Journal of Neuroscience 2013, 33:15259-15271.
24. Schafe G.E., Nader K., Blair H.T., LeDoux J.E. Memory consolidation of Pavlovian fear conditioning: A cellular and molecular perspective. Trends in Neurosciences 2001, 24:540-546.
25. Shansky R.M., Hamo C., Hof P.R., Lou W., McEwen B.S., Morrison J.H. Estrogen promotes stress sensitivity in a prefrontal cortex-amygdala pathway. Cerebral Cortex 2010, 20:2560-2567.
26. Shansky R.M., Hamo C., Hof P.R., McEwen B.S., Morrison J.H. Stress-induced dendritic remodeling in the prefrontal cortex is circuit specific. Cerebral Cortex 2009, 19:2479-2484.
27. Shansky R.M., Morrison J.H. Stress-induced dendritic remodeling in the medial prefrontal cortex: Effects of circuit, hormones and rest. Brain Research 2009, 1293:108-113.
28. Sierra-Mercado D., Padilla-Coreano N., Quirk G.J. Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 2011, 36:529-538.
29. Sotres-Bayon F., Bush D.E., LeDoux J.E. Acquisition of fear extinction requires activation of NR2B-containing NMDA receptors in the lateral amygdala. Neuropsychopharmacology 2007, 32:1929-1940.
30. 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. Learning & Memory 2006, 13:728-733.
31. Yano E.M., Hayes P., Wright S., Schnurr P.P., Lipson L., Bean-Mayberry B., et al. Integration of women veterans into VA quality improvement research efforts: What researchers need to know. Journal of General Internal Medicine 2010, 25(Suppl. 1):56-61.
32. Zeidan M.a., Igoe S.a., Linnman C., Vitalo A., Levine J.B., Klibanski A., et al. Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biological Psychiatry 2011, 0-7. 10.1016/j.biopsych.2011.05.016.
33. Zhang W., Rosenkranz J.A. Repeated restraint stress enhances cue-elicited conditioned freezing and impairs acquisition of extinction in an age-dependent manner. Behavioural Brain Research 2013, 248:12-24.