Hippocampal GABAergic dysfunction in a rat chronic mild stress model of depression

Hippocampus

Volumn 21, Issue 4, 2011, Pages 422-433

  Holm, Mai Marie ^a   Nieto Gonzalez, Jose Luis ^a   Vardya, Irina ^a   Henningsen, Kim ^b   Jayatissa, Magdalena Niepsuj ^b   Wiborg, Ove ^b   Jensen, Kimmo ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

Anhedonia; Antidepressant; DG; Inhibitory postsynaptic currents; Parvalbumin

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; ESCITALOPRAM; GABOXADOL; PARVALBUMIN;

4 AMINOBUTYRIC ACID RELEASE; ANHEDONIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHRONIC STRESS; CONTROLLED STUDY; DENTATE GYRUS; GABAERGIC SYSTEM; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; MAJOR DEPRESSION; MALE; NONHUMAN; PATCH CLAMP; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RAT; UPREGULATION;

ACTION POTENTIALS; ANIMALS; ANTIDEPRESSIVE AGENTS, SECOND-GENERATION; CITALOPRAM; DENTATE GYRUS; DEPRESSION; DISEASE MODELS, ANIMAL; GABA-A RECEPTOR AGONISTS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; ISOXAZOLES; MALE; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, GABA-A; SEROTONIN UPTAKE INHIBITORS;

EID: 79953041746     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20758     Document Type: Article

References (59)

1. Abidin I, Eysel UT, Lessmann V, Mittmann T. 2008. Impaired GABAergic inhibition in the visual cortex of brain-derived neurotrophic factor heterozygous knockout mice. J Physiol 586: 1885-1901.
2. Aponte Y, Lien CC, Reisinger E, Jonas P. 2006. Hyperpolarization-activated cation channels in fast-spiking interneurons of rat hippocampus. J Physiol 574: 229-243.
3. Bannai H, Levi S, Schweizer C, Inoue T, Launey T, Racine V, Sibarita JB, Mikoshiba K, Triller A. 2009. Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron 62: 670-682.
4. Bartos M, Vida I, Frotscher M, Meyer A, Monyer H, Geiger JR, Jonas P. 2002. Fast synaptic inhibition promotes synchronized gamma oscillations in hippocampal interneuron networks. Proc Natl Acad Sci USA 99: 13222-13227.
5. Bergstrom A, Jayatissa MN, Thykjaer T, Wiborg O. 2007. Molecular pathways associated with stress resilience and drug resistance in the chronic mild stress rat model of depression: A gene expression study. J Mol Neurosci 33: 201-215.
6. Berrettini WH, Nurnberger JIJr, Hare TA, Simmons-Alling S, Gershon ES, Post RM. 1983. Reduced plasma and CSF gamma-aminobutyric acid in affective illness: Effect of lithium carbonate. Biol Psychiatry 18: 185-194.
7. Brambilla P, Perez J, Barale F, Schettini G, Soares JC. 2003. GABAergic dysfunction in mood disorders. Mol Psychiatry 8: 721-737, 715.
8. Bremner JD, Narayan M, Anderson ER, Staib LH, Miller HL, Charney DS. 2000. Hippocampal volume reduction in major depression. Am J Psychiatry 157: 115-118.
9. Chang L, Cloak CC, Ernst T. 2003. Magnetic resonance spectroscopy studies of GABA in neuropsychiatric disorders. J Clin Psychiatry 64 (Suppl 3): 7-14.
10. Czeh B, Simon M, van der Hart MG, Schmelting B, Hesselink MB, Fuchs E. 2005. Chronic stress decreases the number of parvalbumin-immunoreactive interneurons in the hippocampus: Prevention by treatment with a substance P receptor (NK1) antagonist. Neuropsychopharmacology 30: 67-79.
11. Devanand DP, Lisanby S, Lo ES, Fitzsimons L, Cooper TB, Halbreich U, Sackeim HA. 1998. Effects of electroconvulsive therapy on plasma vasopressin and oxytocin. Biol Psychiatry 44: 610-616.
12. Drasbek KR, Jensen K. 2006. THIP, a hypnotic and antinociceptive drug, enhances an extrasynaptic GABAA receptor-mediated conductance in mouse neocortex. Cereb Cortex 16: 1134-1141.
13. Duman RS. 2004. Depression: A case of neuronal life and death? Biol Psychiatry 56: 140-145.
14. Farrant M, Nusser Z. 2005. Variations on an inhibitory theme: Phasic and tonic activation of GABA(A) receptors. Nat Rev Neurosci 6: 215-229.
15. Fernandez-Chacon R, Konigstorfer A, Gerber SH, Garcia J, Matos MF, Stevens CF, Brose N, Rizo J, Rosenmund C, Sudhof TC. 2001. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410: 41-49.
16. Fuchs E, Czeh B, Flugge G. 2004. Examining novel concepts of the pathophysiology of depression in the chronic psychosocial stress paradigm in tree shrews. Behav Pharmacol 15: 315-325.
17. Fuller RW. 1995. Serotonin uptake inhibitors: Uses in clinical therapy and in laboratory research. Prog Drug Res 45: 167-204.
18. Gronli J, Fiske E, Murison R, Bjorvatn B, Sorensen E, Ursin R, Portas CM. 2007. Extracellular levels of serotonin and GABA in the hippocampus after chronic mild stress in rats. A microdialysis study in an animal model of depression. Behav Brain Res 181: 42-51.
19. Guidotti A, Auta J, Davis JM, Di-Giorgi-Gerevini V, Dwivedi Y, Grayson DR, Impagnatiello F, Pandey G, Pesold C, Sharma R, Uzunov D, Costa E. 2000. Decrease in reelin and glutamic acid decarboxylase67 (GAD67) expression in schizophrenia and bipolar disorder: A postmortem brain study. Arch Gen Psychiatry 57: 1061-1069.
20. Gulyas AI, Acsady L, Freund TF. 1999. Structural basis of the cholinergic and serotonergic modulation of GABAergic neurons in the hippocampus. Neurochem Int 34: 359-372.
21. Heninger GR, Delgado PL, Charney DS. 1996. The revised monoamine theory of depression: A modulatory role for monoamines, based on new findings from monoamine depletion experiments in humans. Pharmacopsychiatry 29: 2-11.
22. Henningsen K, Andreasen JT, Bouzinova EV, Jayatissa MN, Jensen MS, Redrobe JP, Wiborg O. 2009. Cognitive deficits in the rat chronic mild stress model for depression: Relation to anhedonic-like responses. Behav Brain Res 198: 136-141.
23. Holderbach R, Clark K, Moreau JL, Bischofberger J, Normann C. 2007. Enhanced long-term synaptic depression in an animal model of depression. Biol Psychiatry 62: 92-100.
24. Holm MM, Nieto-Gonzalez JL, Vardya I, Vaegter CB, Nykjaer A, Jensen K. 2009. Mature BDNF, but not ProBDNF, reduces excitability of fast-spiking interneurons in mouse dentate gyrus. J Neurosci 29: 12412-12418.
25. Jayatissa MN, Bisgaard C, Tingstrom A, Papp M, Wiborg O. 2006. Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology 31: 2395-2404.
26. Jayatissa MN, Bisgaard CF, West MJ, Wiborg O. 2008. The number of granule cells in rat hippocampus is reduced after chronic mild stress and re-established after chronic escitalopram treatment. Neuropharmacology 54: 530-541.
27. Kawa K. 1994. Distribution and functional properties of 5-HT3 receptors in the rat hippocampal dentate gyrus: A patch-clamp study. J Neurophysiol 71: 1935-1947.
28. Kerr AM, Reisinger E, Jonas P. 2008. Differential dependence of phasic transmitter release on synaptotagmin 1 at GABAergic and glutamatergic hippocampal synapses. Proc Natl Acad Sci USA 105: 15581-15586.
29. Kraushaar U, Jonas P. 2000. Efficacy and stability of quantal GABA release at a hippocampal interneuron-principal neuron synapse. J Neurosci 20: 5594-5607.
30. Krishnan V, Nestler EJ. 2008. The molecular neurobiology of depression. Nature 455: 894-902.
31. Lawrence JJ, Saraga F, Churchill JF, Statland JM, Travis KE, Skinner FK, McBain CJ. 2006. Somatodendritic Kv7/KCNQ/M channels control interspike interval in hippocampal interneurons. J Neurosci 26: 12325-12338.
32. Maguire J, Mody I. 2007. Neurosteroid synthesis-mediated regulation of GABA(A) receptors: Relevance to the ovarian cycle and stress. JNeurosci 27: 2155-2162.
33. Maya Vetencourt JF, Sale A, Viegi A, Baroncelli L, De PR, O'Leary OF, Castren E, Maffei L. 2008. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 320: 385-388.
34. McMahon LL, Kauer JA. 1997. Hippocampal interneurons are excited via serotonin-gated ion channels. J Neurophysiol 78: 2493-2502.
35. Morales M, Bloom FE. 1997. The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17: 3157-3167.
36. Nestler EJ, Barrot M, DiLeone RJ, Eisch AJ, Gold SJ, Monteggia LM. 2002. Neurobiology of depression. Neuron 34: 13-25.
37. Northoff G, Steinke R, Czcervenka C, Krause R, Ulrich S, Danos P, Kropf D, Otto H, Bogerts B. 1999. Decreased density of GABA-A receptors in the left sensorimotor cortex in akinetic catatonia: Investigation of in vivo benzodiazepine receptor binding. J Neurol Neurosurg Psychiatry 67: 445-450.
38. Orchinik M, Carroll SS, Li YH, McEwen BS, Weiland NG. 2001. Heterogeneity of hippocampal GABA(A) receptors: Regulation by corticosterone. J Neurosci 21: 330-339.
39. Owens MJ, Nemeroff CB. 1994. Role of serotonin in the pathophysiology of depression: Focus on the serotonin transporter. Clin Chem 40: 288-295.
40. Paxinos G, Watson C. 1998. The Rat Brain in Stereotaxic Coordinates, 4th ed. Orlando, FL: Academic Press.
41. Peng Z, Huang CS, Stell BM, Mody I, Houser CR. 2004. Altered expression of the delta subunit of the GABAA receptor in a mouse model of temporal lobe epilepsy. J Neurosci 24: 8629-8639.
42. Petty F, Trivedi MH, Fulton M, Rush AJ. 1995. Benzodiazepines as antidepressants: Does GABA play a role in depression? Biol Psychiatry 38: 578-591.
43. Pittenger C, Duman RS. 2008. Stress, depression, and neuroplasticity: A convergence of mechanisms. Neuropsychopharmacology 33: 88-109.
44. Robinson RT, Drafts BC, Fisher JL. 2003. Fluoxetine increases GABA(A) receptor activity through a novel modulatory site. J Pharmacol Exp Ther 304: 978-984.
45. Sartorius A, Mahlstedt MM, Vollmayr B, Henn FA, Ende G. 2007. Elevated spectroscopic glutamate/gamma-amino butyric acid in rats bred for learned helplessness. Neuroreport 18: 1469-1473.
46. Schneggenburger R, Sakaba T, Neher E. 2002. Vesicle pools and short-term synaptic depression: Lessons from a large synapse. Trends Neurosci 25: 206-212.
47. Sheline YI. 2003. Neuroimaging studies of mood disorder effects on the brain. Biol Psychiatry 54: 338-352.
48. Smith SS, Shen H, Gong QH, Zhou X. 2007. Neurosteroid regulation of GABA(A) receptors: Focus on the alpha4 and delta subunits. Pharmacol Ther 116: 58-76.
49. Song C, Leonard BE. 2005. The olfactory bulbectomised rat as a model of depression. Neurosci Biobehav Rev 29: 627-647.
50. Steele PM, Mauk MD. 1999. Inhibitory control of LTP and LTD: Stability of synapse strength. J Neurophysiol 81: 1559-1566.
51. Tozuka Y, Fukuda S, Namba T, Seki T, Hisatsune T. 2005. GABAergic excitation promotes neuronal differentiation in adult hippocampal progenitor cells. Neuron 47: 803-815.
52. Videbech P, Ravnkilde B. 2004. Hippocampal volume and depression: A meta-analysis of MRI studies. Am J Psychiatry 161: 1957-1966.
53. Vigo DV, Baldessarini RJ. 2009. Anticonvulsants in the treatment of major depressive disorder: An overview. Harv Rev Psychiatry 17: 231-241.
54. Wang J, Liu S, Haditsch U, Tu W, Cochrane K, Ahmadian G, Tran L, Paw J, Wang Y, Mansuy I, Salter MM, Lu YM. 2003. Interaction of calcineurin and type-A GABA receptor gamma 2 subunits produces long-term depression at CA1 inhibitory synapses. J Neurosci 23: 826-836.
55. Wang XJ, Buzsaki G. 1996. Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16: 6402-6413.
56. Williams SR, Buhl EH, Mody I. 1998. The dynamics of synchronized neurotransmitter release determined from compound spontaneous IPSCs in rat dentate granule neurones in vitro. J Physiol 510: 477-497.
57. Willner P, Muscat R, Papp M. 1992. Chronic mild stress-induced anhedonia: A realistic animal model of depression. Neurosci Biobehav Rev 16: 525-534.
58. Xie M, Li X, Han J, Vogt DL, Wittemann S, Mark MD, Herlitze S. 2007. Facilitation versus depression in cultured hippocampal neurons determined by targeting of Ca2+ channel cavbeta4 versus cavbeta2 subunits to synaptic terminals. J Cell Biol 178: 489-502.
59. Zhang N, Wei W, Mody I, Houser CR. 2007. Altered localization of GABA(A) receptor subunits on dentate granule cell dendrites influences tonic and phasic inhibition in a mouse model of epilepsy. J Neurosci 27: 7520-7531.