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Mohammadi-Farani, Ahmad, Fakhri, Sajad, Jalili, Cyrus, Samimi, Zahra. (1401). Intra-mPFC injection of sodium butyrate promotes BDNF expression and ameliorates extinction recall impairment in an experimental paradigm of post-traumatic stress disorder. , 25(9), 1150-1158. doi: 10.22038/ijbms.2022.65000.14312
Ahmad Mohammadi-Farani; Sajad Fakhri; Cyrus Jalili; Zahra Samimi. "Intra-mPFC injection of sodium butyrate promotes BDNF expression and ameliorates extinction recall impairment in an experimental paradigm of post-traumatic stress disorder". , 25, 9, 1401, 1150-1158. doi: 10.22038/ijbms.2022.65000.14312
Mohammadi-Farani, Ahmad, Fakhri, Sajad, Jalili, Cyrus, Samimi, Zahra. (1401). 'Intra-mPFC injection of sodium butyrate promotes BDNF expression and ameliorates extinction recall impairment in an experimental paradigm of post-traumatic stress disorder', , 25(9), pp. 1150-1158. doi: 10.22038/ijbms.2022.65000.14312
Mohammadi-Farani, Ahmad, Fakhri, Sajad, Jalili, Cyrus, Samimi, Zahra. Intra-mPFC injection of sodium butyrate promotes BDNF expression and ameliorates extinction recall impairment in an experimental paradigm of post-traumatic stress disorder. , 1401; 25(9): 1150-1158. doi: 10.22038/ijbms.2022.65000.14312

Intra-mPFC injection of sodium butyrate promotes BDNF expression and ameliorates extinction recall impairment in an experimental paradigm of post-traumatic stress disorder

Iranian Journal of Basic Medical Sciences
مقاله 15، دوره 25، شماره 9، آذر 2022، صفحه 1150-1158    اصل مقاله (466.68 K)
نوع مقاله: Original Article
شناسه دیجیتال (DOI): 10.22038/ijbms.2022.65000.14312
نویسندگان
Ahmad Mohammadi-Farani* 1، 2؛ Sajad Fakhri3؛ Cyrus Jalili4؛ Zahra Samimi5
1Medical Plants Research Center, Basic Health Sciences Institute, Shahrekord University of Medical Sciences, Shahrekord, Iran
2Department of Physiology and Pharmacology, School of medicine, Shahrekord University of Medical Sciences, Shahrekord, Iran
3Pharmaceutical Sciences Research Center, Health Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran
4Medical Biology Research Center, Health Technology Institute, Kermanshah University of Medical Sciences, Kermanshah, Iran
5Department of Immunology, School of medicine, Kermanshah University of Medical Sciences, Kermanshah, Iran
چکیده
Objective(s): Therapeutic strategies that facilitate extinction are promising in the treatment of post-traumatic stress disorder (PTSD). Brain-derived neurotrophic factor (BDNF) has a crucial role in neural plasticity, a process needed for the retention of fear extinction. In this study, we investigated the effects of local administration of a histone deacetylase (HDAC) inhibitor, sodium butyrate (NaBu), on BDNF transcription and behavioral markers of extinction in the single prolonged stress (SPS) model of PTSD. 
Materials and Methods: NaBu was infused into the infralimbic (IL) subregion of the medial prefrontal cortex (mPFC) of male rats. The freezing response was recorded as the criterion to assess fear strength on the day of extinction as well as 24 hr later in the retention test. Other behavioral tests were also measured to evaluate the anxiety level, locomotor activity, and working memory on the retention day. HDAC activity and BDNF mRNA expression were evaluated after the behavioral experiments. 
Results: NaBu facilitated the recall of fear extinction in SPS rats (P<0.0001). SPS rats had higher HDAC activity (P<0.0001) and lower BDNF expression (P<0.05) than non-SPS animals. Also, anxiety was higher in the SPS group (P<0.0001), but locomotor activity (P=0.61) and working memory (P=0.36) were not different between SPS and Non-SPS groups.
Conclusion: Our findings provide evidence that the mechanism of action of NaBu in the improvement of extinction recall is mediated, in part, by enhancing histone acetylation and reviving BDNF expression in IL.
کلیدواژه‌ها
Brain-derived neurotrophic factor؛ Extinction؛ Prefrontal cortex؛ Post-traumatic stress disorder؛ Sodium butyrate
مراجع
1. Shalev A, Liberzon I, Marmar C. Post-traumatic stress disorder. N Engl J Med 2017; 376: 2459-2469.
2. Deslauriers J, Toth M, Der-Avakian A, Risbrough VB. Current status of animal models of posttraumatic stress disorder: behavioral and biological phenotypes, and future challenges in improving translation. Biol Psychiatry 2018; 83: 895-907.
3. Knox D, George SA, Fitzpatrick CJ, Rabinak CA, Maren S, Liberzon I. Single prolonged stress disrupts retention of extinguished fear in rats. Learn Mem 2012; 19: 43-49.
4. Hofmann SG. Enhancing exposure-based therapy from a translational research perspective. Behav Res Ther 2007; 45: 1987-2001.
5. 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.
6. Milad MR, Orr SP, Lasko NB, Chang Y, Rauch SL, Pitman RK. Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study. J Psychiatr Res 2008; 42: 515-520.
7. Norrholm SD, Jovanovic T. Fear processing, psychophysiology, and PTSD. Harv Rev Psychiatry 2018; 26: 129-141.
8. VanElzakker MB, Dahlgren MK, Davis FC, Dubois S, Shin LM. From Pavlov to PTSD: the extinction of conditioned fear in rodents, humans, and anxiety disorders. Neurobiol Learn Mem 2014; 113: 3-18.
9. Paredes D, Morilak DA. A Rodent Model of Exposure Therapy: The use of fear extinction as a therapeutic intervention for PTSD. Front Behav Neurosci 2019; 13: 1-12.
10.    Zuj DV, Palmer MA, Lommen MJ, Felmingham KL. The centrality of fear extinction in linking risk factors to PTSD: A narrative review. Neurosci Biobehav Rev 2016; 69: 15-35.
11. Marek R, Sah P. Neural circuits mediating fear learning and extinction. Adv Neurobiol 2018; 21: 35-48.
12. Piggott VM, Bosse KE, Lisieski MJ, Strader JA, Stanley JA, Conti AC, et al. Single-prolonged stress impairs prefrontal cortex control of amygdala and striatum in rats. Front Behav Neurosci 2019; 13: 1-9.
13. Quirk GJ, Likhtik E, Pelletier JG, Pare D. Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J Neurosci 2003; 23: 8800-8807.
14. Liu WZ, Zhang WH, Zheng ZH, Zou JX, Liu XX, Huang SH, et al. Identification of a prefrontal cortex-to-amygdala pathway for chronic stress-induced anxiety. Nat Commun 2020; 11: 2221.
15. Hong J, Kim D. Freezing response-independent facilitation of fear extinction memory in the prefrontal cortex. Sci Rep 2017; 7: 1-6.
16. Akirav I, Maroun M. The role of the medial prefrontal cortex-amygdala circuit in stress effects on the extinction of fear. Neural Plast 2007; 2007:30873.
17. Vertes RP. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse. 2004; 51: 32-58.
18.    Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ. Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 2006; 13: 728-33.
19. Burgos-Robles A, Vidal-Gonzalez I, Quirk GJ. Sustained conditioned responses in prelimbic prefrontal neurons are correlated with fear expression and extinction failure. J Neurosci 2009; 29: 8474-8482.
20. Krystal JH, Abdallah CG, Averill LA, Kelmendi B, Harpaz-Rotem I, Sanacora G, et al. Synaptic loss and the pathophysiology of PTSD: Implications for ketamine as a prototype novel therapeutic. Curr Psychiatry Rep 2017; 19: 1-11.
21. Burgos-Robles A, Vidal-Gonzalez I, Santini E, Quirk GJ. Consolidation of fear extinction requires NMDA receptor-dependent bursting in the ventromedial prefrontal cortex. Neuron 2007; 53: 871-880.
22. Lin CH, Yeh SH, Lu HY, Gean PW. The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. J Neurosci 2003; 23: 8310-8317.
23. Goda Y, Stevens CF. Synaptic plasticity: the basis of particular types of learning. Curr Biol 1996; 6: 375-378.
24. Andero R, Ressler KJ. Fear extinction and BDNF: Translating animal models of PTSD to the clinic. Genes Brain Behav 2012; 11:503-512.
25. Bredy TW, Wu H, Crego C, Zellhoefer J, Sun YE, Barad M. Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learn Mem 2007; 14: 268-276.
26. Sun W, Li X, An L. Distinct roles of prelimbic and infralimbic proBDNF in extinction of conditioned fear. Neuropharmacology 2018; 131: 11-9.
27. Bhasin M, Reinherz EL, Reche PA. Recognition and classification of histones using support vector machine. J Comput Biol 2006; 13: 102-12.
28. Bredy TW, Barad M. The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learn Mem. 2008; 15: 39-45.
29. Ganai SA, Ramadoss M, Mahadevan V. Histone deacetylase (HDAC) inhibitors - emerging roles in neuronal memory, learning, synaptic plasticity and neural regeneration. Curr Neuropharmacol 2016; 14: 55-71.
30. Lattal KM, Barrett RM, Wood MA. Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behav Neurosci 2007; 121: 1125-1131.
31. Fuchikami M, Yamamoto S, Morinobu S, Takei S, Yamawaki S. Epigenetic regulation of BDNF gene in response to stress. Psychiatry Investig 2010; 7:251-256.
32. Takei S, Morinobu S, Yamamoto S, Fuchikami M, Matsumoto T, Yamawaki S. Enhanced hippocampal BDNF/TrkB signaling in response to fear conditioning in an animal model of posttraumatic stress disorder. J Psychiatr Res 2011; 45: 460-468.
33. Blank M, Dornelles AS, Werenicz A, Velho LA, Pinto DF, Fedi AC, et al. Basolateral amygdala activity is required for enhancement of memory consolidation produced by histone deacetylase inhibition in the hippocampus. Neurobiol Learn Mem 2014; 111: 1-8.
34. Stafford JM, Raybuck JD, Ryabinin AE, Lattal KM. Increasing histone acetylation in the hippocampus-infralimbic network enhances fear extinction. Biol Psychiatry 2012; 72: 25-33.
35. Mohammadi-Farani A, Pourmotabbed A, Ardeshirizadeh Y. Effects of HDAC inhibitors on spatial memory and memory extinction in SPS-induced PTSD rats. Research in Pharmaceutical Sciences 2020; 15: 241-248.
36.    Mohammadi-Farani A, Tamasoki N, Rahimian R. Intra-prefrontal cyclosporine potentiates ketamine-induced fear extinction in rats. Exp Brain Res 2021; 239: 1401-1415.
37.    Paxinos G, Watson C. Paxino’s and Watson’s The rat brain in stereotaxic coordinates. Seventh edition. ed. Amsterdam ; Boston: Elsevier/AP, Academic Press is an imprint of Elsevier; 2014.
38.    Bashiri H, Rezayof A, Sahebgharani M, Tavangar SM, Zarrindast MR. Modulatory effects of the basolateral amygdala alpha2-adrenoceptors on nicotine-induced anxiogenic-like behaviours of rats in the elevated plus maze. Neuropharmacology 2016; 105: 478-486.
39. Salehabadi S, Abrari K, Elahdadi Salmani M, Nasiri M, Lashkarbolouki T. Investigating the role of the amygdala orexin receptor 1 in memory acquisition and extinction in a rat model of PTSD. Behav Brain Res 2020; 384: 112455.
40. Rafiq S, Batool Z, Liaquat L, Haider S. Blockade of muscarinic receptors impairs reconsolidation of older fear memory by decreasing cholinergic neurotransmission: A study in rat model of PTSD. Life Sci 2020; 256:118014.
41. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
42. Lebois LAM, Seligowski AV, Wolff JD, Hill SB, Ressler KJ. Augmentation of Extinction and Inhibitory Learning in Anxiety and Trauma-Related Disorders. Annu Rev Clin Psychol 2019; 15:257-284.
43. Monsey MS, Ota KT, Akingbade IF, Hong ES, Schafe GE. Epigenetic alterations are critical for fear memory consolidation and synaptic plasticity in the lateral amygdala. PLoS One 2011; 6:e19958.
44. Whittle N, Singewald N. HDAC inhibitors as cognitive enhancers in fear, anxiety and trauma therapy: Where do we stand? Biochem Soc Trans 2014; 42:569-581.
45. Siddiqui SA, Singh S, Ranjan V, Ugale R, Saha S, Prakash A. Enhanced Histone Acetylation in the Infralimbic Prefrontal Cortex is Associated with Fear Extinction. Cell Mol Neurobiol 2017; 37:1287-1301.
46. Whittle N, Schmuckermair C, Gunduz Cinar O, Hauschild M, Ferraguti F, Holmes A, et al. Deep brain stimulation, histone deacetylase inhibitors and glutamatergic drugs rescue resistance to fear extinction in a genetic mouse model. Neuropharmacology 2013; 64:414-423.
47. Fujita Y, Morinobu S, Takei S, Fuchikami M, Matsumoto T, Yamamoto S, et al. Vorinostat, a histone deacetylase inhibitor, facilitates fear extinction and enhances expression of the hippocampal NR2B-containing NMDA receptor gene. J Psychiatr Res 2012; 46: 635-643.
48. Bowers ME, Xia B, Carreiro S, Ressler KJ. The class I HDAC inhibitor RGFP963 enhances consolidation of cued fear extinction. Learn Mem 2015; 22: 225-231.
49. Heldt SA, Stanek L, Chhatwal JP, Ressler KJ. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 2007; 12:656-670.
50. Kozlovsky N, Matar MA, Kaplan Z, Kotler M, Zohar J, Cohen H. Long-term down-regulation of BDNF mRNA in rat hippocampal CA1 subregion correlates with PTSD-like behavioural stress response. Int J Neuropsychopharmacol 2007; 10:741-758.
51. Chhatwal JP, Stanek-Rattiner L, Davis M, Ressler KJ. Amygdala BDNF signaling is required for consolidation but not encoding of extinction. Nat Neurosci 2006; 9: 870-872.
52. Karpova NN, Pickenhagen A, Lindholm J, Tiraboschi E, Kulesskaya N, Agustsdottir A, et al. Fear erasure in mice requires synergy between antidepressant drugs and extinction training. Science 2011; 334: 1731-1734.
53. Young MB, Andero R, Ressler KJ, Howell LL. 3,4-Methylenedioxymethamphetamine facilitates fear extinction learning. Transl Psychiatry 2015; 5: e634.
54. Kataoka T, Fuchikami M, Nojima S, Nagashima N, Araki M, Omura J, et al. Combined brain-derived neurotrophic factor with extinction training alleviate impaired fear extinction in an animal model of post-traumatic stress disorder. Genes Brain Behav 2019; 18: e12520.
55. Peters J, Dieppa-Perea LM, Melendez LM, Quirk GJ. Induction of fear extinction with hippocampal-infralimbic BDNF. Science. 2010; 328: 1288-1290.
56. Rosas-Vidal LE, Lozada-Miranda V, Cantres-Rosario Y, Vega-Medina A, Melendez L, Quirk GJ. Alteration of BDNF in the medial prefrontal cortex and the ventral hippocampus impairs extinction of avoidance. Neuropsychopharmacology 2018; 43: 2636-2644.
57. Zheng F, Zhou X, Moon C, Wang H. Regulation of brain-derived neurotrophic factor expression in neurons. Int J Physiol Pathophysiol Pharmacol 2012; 4: 188-200.
58. Miao YL, Guo WZ, Shi WZ, Fang WW, Liu Y, Liu J, et al. Midazolam ameliorates the behavior deficits of a rat posttraumatic stress disorder model through dual 18 kDa translocator protein and central benzodiazepine receptor and neurosteroidogenesis. PLoS One 2014; 9: e101450.
59. Patki G, Li L, Allam F, Solanki N, Dao AT, Alkadhi K, et al. Moderate treadmill exercise rescues anxiety and depression-like behavior as well as memory impairment in a rat model of posttraumatic stress disorder. Physiol Behav 2014; 130: 47-53.
60. Solanki N, Alkadhi I, Atrooz F, Patki G, Salim S. Grape powder prevents cognitive, behavioral, and biochemical impairments in a rat model of posttraumatic stress disorder. Nutr Res 2015; 35: 65-75.
61. Lee B, Sur B, Cho SG, Yeom M, Shim I, Lee H, et al. Ginsenoside Rb1 rescues anxiety-like responses in a rat model of post-traumatic stress disorder. J Nat Med 2016; 70: 133-144.
62. Lee B, Lee H. Systemic Administration of Curcumin Affect Anxiety-Related Behaviors in a Rat Model of Posttraumatic Stress Disorder via Activation of Serotonergic Systems. Evid Based Complement Alternat Med 2018; 2018: 9041309.
63. Lee B, Shim I, Lee H, Hahm DH. Tetramethylpyrazine reverses anxiety-like behaviors in a rat model of post-traumatic stress disorder. Korean J Physiol Pharmacol 2018; 22: 525-538.
64. Xiao B, Han F, Shi Y. Administration of moclobemide facilitates fear extinction and attenuates anxiety-like behaviors by regulating synaptic-associated proteins in a rat model of post-traumatic stress disorder. Synapse 2020; 74: e22146.
65. Yehuda R, Halligan SL, Bierer LM. Relationship of parental trauma exposure and PTSD to PTSD, depressive and anxiety disorders in offspring. J Psychiatr Res 2001; 35: 261-270.
66. Lisieski MJ, Eagle AL, Conti AC, Liberzon I, Perrine SA. Single-Prolonged Stress: A Review of Two Decades of Progress in a Rodent Model of Post-traumatic Stress Disorder. Front Psychiatry 2018; 9: 196.
67. Yang ST, Shi Y, Wang Q, Peng JY, Li BM. Neuronal representation of working memory in the medial prefrontal cortex of rats. Mol Brain 2014; 7: 61.
68. Collins AG, Frank MJ. How much of reinforcement learning is working memory, not reinforcement learning? A behavioral, computational, and neurogenetic analysis. Eur J Neurosci 2012; 35: 1024-1035.
69. Stout DM, Shackman AJ, Pedersen WS, Miskovich TA, Larson CL. Neural circuitry governing anxious individuals’ mis-allocation of working memory to threat. Sci Rep 2017; 7: 1-11.
70. Stout DM, Acheson DT, Moore TM, Gur RC, Baker DG, Geyer MA, et al. Individual variation in working memory is associated with fear extinction performance. Behav Res Ther 2018; 102: 52-59.

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