Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2017, Article ID 5715816, 10 pages
https://doi.org/10.1155/2017/5715816
Research Article

Effects of Traumatic Stress Induced in the Juvenile Period on the Expression of Gamma-Aminobutyric Acid Receptor Type A Subunits in Adult Rat Brain

1Department of Medical Psychology, Shandong University School of Medicine, Jinan, Shandong 250012, China
2Department of Psychological Medicine, National University of Singapore, Singapore 119228

Correspondence should be addressed to Fang Pan; nc.ude.uds@gnafnap

Received 10 October 2016; Revised 18 January 2017; Accepted 15 February 2017; Published 2 March 2017

Academic Editor: Zygmunt Galdzicki

Copyright © 2017 Cui Yan Lu et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. W. Brown and T. O. Harris, “Aetiology of anxiety and depressive disorders in an inner-city population. 1. Early adversity,” Psychological Medicine, vol. 23, no. 1, pp. 143–154, 1993. View at Publisher · View at Google Scholar · View at Scopus
  2. R. F. Anda, V. J. Felitti, J. D. Bremner et al., “The enduring effects of abuse and related adverse experiences in childhood: a convergence of evidence from neurobiology and epidemiology,” European Archives of Psychiatry and Clinical Neuroscience, vol. 256, no. 3, pp. 174–186, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. E. L. Harrison and B. T. Baune, “Modulation of early stress-induced neurobiological changes: a review of behavioural and pharmacological interventions in animal models,” Translational Psychiatry, vol. 4, article no. e390, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Kaufman, P. M. Plotsky, C. B. Nemeroff, and D. S. Charney, “Effects of early adverse experiences on brain structure and function: clinical implications,” Biological Psychiatry, vol. 48, no. 8, pp. 778–790, 2000. View at Publisher · View at Google Scholar · View at Scopus
  5. R. B. Lydiard, “The role of GABA in anxiety disorders,” Journal of Clinical Psychiatry, vol. 64, supplement 3, pp. 21–27, 2003. View at Google Scholar · View at Scopus
  6. C. B. Nemeroff, “The role of GABA in the pathophysiology and treatment of anxiety disorders,” Psychopharmacology Bulletin, vol. 37, no. 4, pp. 133–146, 2003. View at Google Scholar · View at Scopus
  7. J. D. Bremner, R. B. Innis, S. M. Southwick, L. Staib, S. Zoghbi, and D. S. Charney, “Decreased benzodiazepine receptor binding in prefrontal cortex in combat-related posttraumatic stress disorder,” American Journal of Psychiatry, vol. 157, no. 7, pp. 1120–1126, 2000. View at Publisher · View at Google Scholar · View at Scopus
  8. B. Luscher, Q. Shen, and N. Sahir, “The GABAergic deficit hypothesis of major depressive disorder,” Molecular Psychiatry, vol. 16, no. 4, pp. 383–406, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. B. K. Puri and A. D. Hall, Revision Notes in Psychiatry, Arnold, 2004.
  10. U. Günther, J. Benson, D. Benke et al., “Benzodiazepine-insensitive mice generated by targeted disruption of the γ2 subunit gene of γ-aminobutyric acid type A receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 17, pp. 7749–7753, 1995. View at Publisher · View at Google Scholar · View at Scopus
  11. E. A. Barnard, P. Skolnick, R. W. Olsen et al., “International Union of Pharmacology. XV. Subtypes of gamma-aminobutyric acidA receptors: classification on the basis of subunit structure and receptor function,” Pharmacological Reviews, vol. 50, no. 2, pp. 291–313, 1998. View at Google Scholar
  12. U. Rudolph, F. Crestani, D. Benke et al., “Benzodiazepine actions mediated by specific γ-aminobutyric acid(A) receptor subtypes,” Nature, vol. 401, no. 6755, pp. 796–800, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. R. M. McKernan, T. W. Rosahl, D. S. Reynolds et al., “Sedative but not anxiolytic properties of benzodiazepines are mediated by the GABA(A) receptor α1 subtype,” Nature Neuroscience, vol. 3, no. 6, pp. 587–592, 2000. View at Publisher · View at Google Scholar · View at Scopus
  14. R. Dias, W. F. A. Sheppard, R. L. Fradley et al., “Evidence for a significant role of α3-containing GABAA receptors in mediating the anxiolytic effects of benzodiazepines,” The Journal of Neuroscience, vol. 25, no. 46, pp. 10682–10688, 2005. View at Publisher · View at Google Scholar · View at Scopus
  15. U. Rudolph and H. Möhler, “Analysis of GABAA receptor function and dissection of the pharmacology of benzodiazepines and general anesthetics through mouse genetics,” Annual Review of Pharmacology and Toxicology, vol. 44, pp. 475–498, 2004. View at Publisher · View at Google Scholar · View at Scopus
  16. M. R. Milad and S. L. Rauch, “The role of the orbitofrontal cortex in anxiety disorders,” Annals of the New York Academy of Sciences, vol. 1121, pp. 546–561, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. G. J. Quirk and D. Mueller, “Neural mechanisms of extinction learning and retrieval,” Neuropsychopharmacology, vol. 33, no. 1, pp. 56–72, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Mostert and J. Kesselring, “Effects of a short-term exercise training program on aerobic fitness, fatigue, health perception and activity level of subjects with multiple sclerosis,” Multiple Sclerosis, vol. 8, no. 2, pp. 161–168, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Ströhle, M. Höfler, H. Pfister et al., “Physical activity and prevalence and incidence of mental disorders in adolescents and young adults,” Psychological Medicine, vol. 37, no. 11, pp. 1657–1666, 2007. View at Publisher · View at Google Scholar · View at Scopus
  20. A. A. Vujanovic, S. G. Farris, C. B. Harte, J. A. J. Smits, and M. J. Zvolensky, “Smoking status and exercise in relation to PTSD symptoms: a test among trauma-exposed adults,” Mental Health and Physical Activity, vol. 6, no. 2, pp. 132–138, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. G. Stathopoulou, M. B. Powers, A. C. Berry, J. A. J. Smits, and M. W. Otto, “Exercise interventions for mental health: a quantitative and qualitative review,” Clinical Psychology: Science & Practice, vol. 13, no. 2, pp. 179–193, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. B. Kim and J. Seo, “Treadmill exercise alleviates post-traumatic stress disorder-induced impairment of spatial learning memory in rats,” Journal of Exercise Rehabilitation, vol. 9, no. 4, pp. 413–419, 2013. View at Publisher · View at Google Scholar
  23. T.-Y. Huang and C.-H. Lin, “A comparison between chronic exercise training and desipramine as treatments for the depression-like behavior of early-life maternal deprivation rats,” Neuroscience Letters, vol. 480, no. 3, pp. 201–205, 2010. View at Publisher · View at Google Scholar · View at Scopus
  24. G. Elmesallamy, M. Abass, N. Refat, and A. Atta, “Differential effects of alprazolam and clonazepam on the immune system and blood vessels of non-stressed and stressed adult male albino rats,” Interdisciplinary Toxicology, vol. 4, no. 3, pp. 132–143, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. Y. Li, Y.-J. Ji, H. Jiang et al., “Effects of unpredictable chronic stress on behavior and brain-derived neurotrophic factor expression in CA3 subfield and dentate gyrus of the hippocampus in different aged rats,” Chinese Medical Journal, vol. 122, no. 13, pp. 1564–1569, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Aisa, R. Tordera, B. Lasheras, J. Del Río, and M. J. Ramírez, “Effects of maternal separation on hypothalamic-pituitary-adrenal responses, cognition and vulnerability to stress in adult female rats,” Neuroscience, vol. 154, no. 4, pp. 1218–1226, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. J.-H. Lee, H. J. Kim, J. G. Kim et al., “Depressive behaviors and decreased expression of serotonin reuptake transporter in rats that experienced neonatal maternal separation,” Neuroscience Research, vol. 58, no. 1, pp. 32–39, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Marais, S. J. van Rensburg, J. M. van Zyl, D. J. Stein, and W. M. U. Daniels, “Maternal separation of rat pups increases the risk of developing depressive-like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus,” Neuroscience Research, vol. 61, no. 1, pp. 106–112, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. A. S. Ivy, C. S. Rex, Y. Chen et al., “Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors,” Journal of Neuroscience, vol. 30, no. 39, pp. 13005–13015, 2010. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Lader, “Benzodiazepines revisited-will we ever learn?” Addiction, vol. 106, no. 12, pp. 2086–2109, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. L. G. Miller, S. Woolverton, D. J. Greenblatt, F. Lopez, R. B. Roy, and R. I. Shader, “Chronic benzodiazepine administration. IV. Rapid development of tolerance and receptor downregulation associated with alprazolam administration,” Biochemical Pharmacology, vol. 38, no. 21, pp. 3773–3777, 1989. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Harro, A. Lang, and E. Vasar, “Long-term diazepam treatment produces changes in cholecystokinin receptor binding in rat brain,” European Journal of Pharmacology, vol. 180, no. 1, pp. 77–83, 1990. View at Publisher · View at Google Scholar · View at Scopus
  33. X. Liu, L. J. Yang, S. J. Fan, H. Jiang, and F. Pan, “Swimming exercise effects on the expression of HSP70 and iNOS in hippocampus and prefrontal cortex in combined stress,” Neuroscience Letters, vol. 476, no. 2, pp. 99–103, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. C. Li, Y. Liu, S. Yin et al., “Long-term effects of early adolescent stress: dysregulation of hypothalamic–pituitary–adrenal axis and central corticotropin releasing factor receptor 1 expression in adult male rats,” Behavioural Brain Research, vol. 288, pp. 39–49, 2015. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Steckler and V. Risbrough, “Pharmacological treatment of PTSD—established and new approaches,” Neuropharmacology, vol. 62, no. 2, pp. 617–627, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. C. Caldji, D. Francis, S. Sharma, P. M. Plotsky, and M. J. Meaney, “The effects of early rearing environment on the development of GABA(A) and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat,” Neuropsychopharmacology, vol. 22, no. 3, pp. 219–229, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. F. Crestani, M. Lorez, K. Baer et al., “Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues,” Nature Neuroscience, vol. 2, no. 9, pp. 833–839, 1999. View at Publisher · View at Google Scholar · View at Scopus
  38. Q. Shen, R. Lal, B. A. Luellen, J. C. Earnheart, A. M. Andrews, and B. Luscher, “γ-aminobutyric acid-type A receptor deficits cause hypothalamic-pituitary-adrenal axis hyperactivity and antidepressant drug sensitivity reminiscent of melancholic forms of depression,” Biological Psychiatry, vol. 68, no. 6, pp. 512–520, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. R. J. Davidson, K. M. Putnam, and C. L. Larson, “Dysfunction in the neural circuitry of emotion regulation—a possible prelude to violence,” Science, vol. 289, no. 5479, pp. 591–594, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. H. Möhler, J.-M. Fritschy, F. Crestani, T. Hensch, and U. Rudolph, “Specific GABAA circuits in brain development and therapy,” Biochemical Pharmacology, vol. 68, no. 8, pp. 1685–1690, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. S. Royer, M. Martina, and D. Paré, “An inhibitory interface gates impulse traffic between the input and output stations of the amygdala,” The Journal of Neuroscience, vol. 19, no. 23, pp. 10575–10583, 1999. View at Google Scholar · View at Scopus
  42. A. Wisłowska-Stanek, M. Lehner, A. Skórzewska et al., “Changes in the brain expression of alpha-2 subunits of the GABA-A receptor after chronic restraint stress in low- and high-anxiety rats,” Behavioural Brain Research, vol. 253, pp. 337–345, 2013. View at Publisher · View at Google Scholar · View at Scopus
  43. M. Koenigs and J. Grafman, “Posttraumatic stress disorder: the role of medial prefrontal cortex and amygdala,” Neuroscientist, vol. 15, no. 5, pp. 540–548, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. M. R. Milad, R. K. Pitman, C. B. Ellis et al., “Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder,” Biological Psychiatry, vol. 66, no. 12, pp. 1075–1082, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. R. L. Aupperle, A. J. Melrose, M. B. Stein, and M. P. Paulus, “Executive function and PTSD: disengaging from trauma,” Neuropharmacology, vol. 62, no. 2, pp. 686–694, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Pirker, C. Schwarzer, A. Wieselthaler, W. Sieghart, and G. Sperk, “GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain,” Neuroscience, vol. 101, no. 4, pp. 815–850, 2000. View at Publisher · View at Google Scholar · View at Scopus
  47. G. R. Dawson, “An inverse agonist selective for 5 subunit-containing GABAA receptors enhances cognition,” Journal of Pharmacology and Experimental Therapeutics, vol. 316, no. 3, pp. 1335–1345, 2006. View at Publisher · View at Google Scholar
  48. N. Collinson, J. R. Atack, P. Laughton, G. R. Dawson, and D. N. Stephens, “An inverse agonist selective for α5 subunit-containing GABA A receptors improves encoding and recall but not consolidation in the Morris water maze,” Psychopharmacology, vol. 188, no. 4, pp. 619–628, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. F. Crestani, R. Keist, J.-M. Fritschy et al., “Trace fear conditioning involves hippocampal α5 GABAA receptors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 13, pp. 8980–8985, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. T. M. Ballard, F. Knoflach, E. Prinssen et al., “RO4938581, a novel cognitive enhancer acting at GABAA α5 subunit-containing receptors,” Psychopharmacology, vol. 202, no. 1–3, pp. 207–223, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. R. J. Loewenstein, “Rational Psychopharmacology in the treatment of multiple personality disorder,” Psychiatric Clinics of North America, vol. 14, no. 3, pp. 721–740, 1991. View at Google Scholar · View at Scopus
  52. J. R. T. Davidson, “Use of benzodiazepines in social anxiety disorder, generalized anxiety disorder, and posttraumatic stress disorder,” Journal of Clinical Psychiatry, vol. 65, supplement 5, pp. 29–33, 2004. View at Google Scholar · View at Scopus
  53. E. Gelpin, O. Bonne, T. Peri, D. Brandes, and A. Y. Shalev, “Treatment of recent trauma survivors with benzodiazepines: a prospective study,” The Journal of Clinical Psychiatry, vol. 57, no. 9, pp. 390–394, 1996. View at Google Scholar · View at Scopus
  54. R. A. Sansone, J. Hruschka, A. Vasudevan, and S. N. Miller, “Benzodiazepine exposure and history of trauma,” Psychosomatics, vol. 44, no. 6, pp. 523–524, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. J. Zohar, A. Juven-Wetzler, R. Sonnino, S. Cwikel-Hamzany, E. Balaban, and H. Cohen, “New insights into secondary prevention in post-traumatic stress disorder,” Dialogues in Clinical Neuroscience, vol. 13, no. 3, pp. 301–309, 2011. View at Google Scholar · View at Scopus
  56. S. Chen, X. Huang, X. J. Zeng, W. Sieghart, and E. I. Tietz, “Benzodiazepine-mediated regulation of α1, α2, β1–3 and γ2 GABAA receptor subunit proteins in the rat brain hippocampus and cortex,” Neuroscience, vol. 93, no. 1, pp. 33–44, 1999. View at Publisher · View at Google Scholar
  57. M. Guszkowska, “The effects of exercise on anxiety, depression and mood states,” Psychiatria Polska, vol. 38, no. 4, pp. 611–620, 2004. View at Google Scholar · View at Scopus
  58. R. K. Dishman, A. L. Dunn, S. D. Youngstedt et al., “Increased open field locomotion and decreased striatal GABAA binding after activity wheel running,” Physiology and Behavior, vol. 60, no. 3, pp. 699–705, 1996. View at Publisher · View at Google Scholar · View at Scopus
  59. J. Glykys, E. O. Mann, and I. Mody, “Which GABAA receptor subunits are necessary for tonic inhibition in the hippocampus?” Journal of Neuroscience, vol. 28, no. 6, pp. 1421–1426, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. M. R. Groen, O. Paulsen, E. Pérez-Garci et al., “Development of dendritic tonic GABAergic inhibition regulates excitability and plasticity in CA1 pyramidal neurons,” Journal of Neurophysiology, vol. 112, no. 2, pp. 287–299, 2014. View at Publisher · View at Google Scholar · View at Scopus