Sex differences in learned fear expression and extinction involve altered gamma oscillations in medial prefrontal cortex

Neurobiology of Learning and Memory

Volumn 135, Issue , 2016, Pages 66-72

  Fenton, Georgina E ^a   Halliday, David M ^b   Mason, Rob ^a   Bredy, Timothy W ^c,d   Stevenson, Carl W ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

^c UNIVERSITY OF QUEENSLAND   (Australia)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Extinction; Fear conditioning; Gamma oscillations; Infralimbic; Prelimbic; Sex differences

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BRAIN DYSFUNCTION; CONTROLLED STUDY; ELECTRICAL POTENTIAL PARAMETERS; ELECTROPHYSIOLOGY PARAMETERS; FEAR CONDITIONING TEST; FEMALE; FOOTSHOCK; GAMMA RHYTHM; IN VIVO STUDY; LOCAL FIELD POTENTIAL; MALE; MEDIAL PREFRONTAL CORTEX; NEUROPATHOLOGY; NONHUMAN; POSTTRAUMATIC STRESS DISORDER; RAT; RECALL; REINFORCEMENT; SEX DIFFERENCE; YOUNG ADULT; ANIMAL; ANIMAL BEHAVIOR; CONDITIONED REFLEX; FEAR; PHYSIOLOGY; PREFRONTAL CORTEX; SEXUAL CHARACTERISTICS;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; EXTINCTION, PSYCHOLOGICAL; FEAR; FEMALE; GAMMA RHYTHM; MALE; PREFRONTAL CORTEX; RATS; SEX CHARACTERISTICS;

EID: 84991474975     PISSN: 10747427     EISSN: 10959564     Source Type: Journal    
DOI: 10.1016/j.nlm.2016.06.019     Document Type: Article

References (40)

1. Baker-Andresen, D., Flavell, C.R., Li, X., Bredy, T.W., Activation of BDNF signaling prevents the return of fear in female mice. Learning & Memory 20 (2013), 237–240.
2. Baran, S.E., Armstrong, C.E., Niren, D.C., Conrad, C.D., Prefrontal cortex lesions and sex differences in fear extinction and perseveration. Learning & Memory 17 (2010), 267–278.
3. 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 91 (2009), 323–332.
4. Benchenane, K., Tiesinga, P.H., Battaglia, F.P., Oscillations in the prefrontal cortex: A gateway to memory and attention. Current Opinion in Neurobiology 21 (2011), 475–485.
5. Blume, S. R., Hetzel, A., Rosenkranz, J. A. (2013). Sex differences in the basolateral amygdala. SFN abstract 673.01.
6. Cholanian, M., Lobzova, A., Das, B., Yelleswarapu, C., Donaldson, S.T., Digital holographic microscopy discriminates sex differences in medial prefrontal cortex GABA neurons following amphetamine sensitization. Pharmacology, Biochemistry and Behavior 124 (2014), 326–332.
7. Courtin, J., Chaudun, F., Rozeske, R.R., Karalis, N., Gonzalez-Campo, C., Wurtz, H., Herry, C., Prefrontal parvalbumin interneurons shape neuronal activity to drive fear expression. Nature 505 (2014), 92–96.
8. Courtin, J., Karalis, N., Gonzalez-Campo, C., Wurtz, H., Herry, C., Persistence of amygdala gamma oscillations during extinction learning predicts spontaneous fear recovery. Neurobiology of Learning and Memory 113 (2014), 82–89.
9. Diggle, P.J., Spectral analysis. Diggle, P.J., (eds.) Time series. A biostatistical introduction, 1990, Oxford University Press, New York, 94–133.
10. Fenton, G.E., Pollard, A.K., Halliday, D.M., Mason, R., Bredy, T.W., Stevenson, C.W., Persistent prelimbic cortex activity contributes to enhanced learned fear expression in females. Learning & Memory 21 (2014), 55–60.
11. Fenton, G.E., Spicer, C.H., Halliday, D.M., Mason, R., Stevenson, C.W., Basolateral amygdala activity during the retrieval of associative learning under anesthesia. Neuroscience 13 (2013), 146–156.
12. Fitzgerald, P.J., Whittle, N., Flynn, S.M., Graybeal, C., Pinard, C.R., Gunduz-Cinar, O., Holmes, A., Prefrontal single-unit firing associated with deficient extinction in mice. Neurobiology of Learning and Memory 113 (2014), 69–81.
13. Glover, E.M., Jovanovic, T., Norrholm, S.D., Estrogen and extinction of fear memories: Implications for posttraumatic stress disorder treatment. Biological Psychiatry 78 (2015), 178–185.
14. Glykos, V., Whittington, M.A., LeBeau, F.E., Subregional differences in the generation of fast network oscillations in the rat medial prefrontal cortex (mPFC) in vitro. Journal of Physiology 593 (2015), 3597–3615.
15. Gupta, R.R., Sen, S., Diepenhorst, L.L., Rudick, C.N., Maren, S., Estrogen modulates sexually dimorphic contextual fear conditioning and hippocampal long-term potentiation (LTP) in rats. Brain Research 888 (2001), 356–365.
16. Harris, A.Z., Gordon, J.A., Long-range neural synchrony in behavior. Annual Review of Neuroscience 38 (2015), 171–194.
17. Herry, C., Ferraguti, F., Singewald, N., Letzkus, J.J., Ehrlich, I., Lüthi, A., Neuronal circuits of fear extinction. European Journal of Neuroscience 31 (2010), 599–612.
18. Jovanovic, T., Norrholm, S.D., Neural mechanisms of impaired fear inhibition in posttraumatic stress disorder. Frontiers in Behavioral Neuroscience, 5, 2011, 44.
19. Lesting, J., Narayanan, R.T., Kluge, C., Sangha, S., Seidenbecher, T., Pape, H.C., Patterns of coupled theta activity in amygdala-hippocampal-prefrontal cortical circuits during fear extinction. PLoS ONE, 6, 2011, e21714.
20. Linnman, C., Zeidan, M.A., Furtak, S.C., Pitman, R.K., Quirk, G.J., Milad, M.R., Resting amygdala and medial prefrontal metabolism predicts functional activation of the fear extinction circuit. American Journal of Psychiatry 169 (2012), 415–423.
21. MacKenzie, G., Maguire, J., The role of ovarian hormone-derived neurosteroids on the regulation of GABAA receptors in affective disorders. Psychopharmacology 231 (2014), 3333–3342.
22. Maeng, L.Y., Milad, M.R., Sex differences in anxiety disorders: Interactions between fear, stress, and gonadal hormones. Hormones and Behavior 76 (2015), 106–117.
23. Maren, S., De Oca, B., Fanselow, M.S., Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: Positive correlation between LTP and contextual learning. Brain Research 661 (1994), 25–34.
24. Marron Fernandez de Velasco, E., Hearing, M., Xia, Z., Victoria, N.C., Luján, R., Wickman, K., Sex differences in GABABR-GIRK signaling in layer 5/6 pyramidal neurons of the mouse prelimbic cortex. Neuropharmacology 95 (2015), 353–360.
25. Merz, C.J., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R., Wolf, O.T., Neuronal correlates of extinction learning are modulated by sex hormones. Social Cognitive and Affective Neuroscience 7 (2012), 819–830.
26. Milad, M.R., Pitman, R.K., Ellis, C.B., Gold, A.L., Shin, L.M., Lasko, N.B., Rauch, S.L., Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biological Psychiatry 66 (2009), 1075–1082.
27. Mueller, E.M., Panitz, C., Hermann, C., Pizzagalli, D.A., Prefrontal oscillations during recall of conditioned and extinguished fear in humans. Journal of Neuroscience 34 (2014), 7059–7066.
28. Orsini, C.A., Kim, J.H., Knapska, E., Maren, S., Hippocampal and prefrontal projections to the basal amygdala mediate contextual regulation of fear after extinction. Journal of Neuroscience 31 (2011), 17269–17277.
29. 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 39 (2014), 1282–1289.
30. Sangha, S., Ilenseer, J., Sosulina, L., Lesting, J., Pape, H.C., Differential regulation of glutamic acid decarboxylase gene expression after extinction of a recent memory vs. intermediate memory. Learning & Memory 19 (2012), 194–200.
31. Sharpe, M., Killcross, S., The prelimbic cortex uses contextual cues to modulate responding towards predictive stimuli during fear renewal. Neurobiology of Learning and Memory 118 (2015), 20–29.
32. Shin, L.M., Lasko, N.B., Macklin, M.L., Karpf, R.D., Milad, M.R., Orr, S.P., Pitman, R.K., Resting metabolic activity in the cingulate cortex and vulnerability to posttraumatic stress disorder. Archives of General Psychiatry 66 (2009), 1099–1107.
33. 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 36 (2011), 529–538.
34. Stevenson, C.W., Spicer, C.H., Mason, R., Marsden, C.A., Early life programming of fear conditioning and extinction in adult male rats. Behavioural Brain Research 205 (2009), 505–510.
35. Stevenson, C.W., Halliday, D.M., Marsden, C.A., Mason, R., Early life programming of hemispheric lateralization and synchronization in the adult medial prefrontal cortex. Neuroscience 155 (2008), 852–863.
36. Stevenson, C.W., Halliday, D.M., Marsden, C.A., Mason, R., Systemic administration of the benzodiazepine receptor partial inverse agonist FG-7142 disrupts corticolimbic network interactions. Synapse 61 (2007), 646–663.
37. Stujenske, J.M., Likhtik, E., Topiwala, M.A., Gordon, J.A., Fear and safety engage competing patterns of theta-gamma coupling in the basolateral amygdala. Neuron 83 (2014), 919–933.
38. 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 13 (2006), 728–733.
39. Wang, M.E., Yuan, R.K., Keinath, A.T., Ramos Álvarez, M.M., Muzzio, I.A., Extinction of learned fear induces hippocampal place cell remapping. Journal of Neuroscience 35 (2015), 9122–9136.
40. Zeidan, M.A., Igoe, S.A., Linnman, C., Vitalo, A., Levine, J.B., Klibanski, A., Milad, M.R., Estradiol modulates medial prefrontal cortex and amygdala activity during fear extinction in women and female rats. Biological Psychiatry 70 (2011), 920–927.