Cellular correlates of anxiety in CA1 hippocampal pyramidal cells of 5-HT1A receptor knockout mice

Psychopharmacology

Volumn 213, Issue 2-3, 2011, Pages 453-463

  Freeman Daniels, Emily ^a   Beck, Sheryl G ^b   Kirby, Lynn G ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

5 HT1A receptor; Anxiety; Electrophysiology; Elevated plus maze; Hippocampus; Serotonin

Indexed keywords

4 AMINOBUTYRIC ACID; GLUTAMIC ACID; SEROTONIN 1A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; HIPPOCAMPAL CA1 REGION; INHIBITORY POSTSYNAPTIC POTENTIAL; MALE; MOUSE; NERVE CELL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SYNAPSE; WILD TYPE;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; CARBOLINES; DIAZEPAM; DISEASE MODELS, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MAZE LEARNING; MICE; MICE, KNOCKOUT; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RECEPTOR, SEROTONIN, 5-HT1A;

EID: 79952489527     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-010-2030-5     Document Type: Article

References (68)

1. Adhikari A, Topiwala MA, Gordon JA (2010) Synchronized activity between the ventral hippocampus and the medial prefrontal cortex during anxiety. Neuron 65:257-269
2. Allan AM, Baier LD, Zhang X (1992) Effects of lorazepam tolerance and withdrawal on GABAA receptor-operated chloride channels. J Pharmacol Exp Ther 261:395-402
3. 1A receptors in the median raphe nucleus and dorsal hippocampus may mediate anxiolytic and anxiogenic behaviours respectively. Eur J Pharmacol 264:259-264
4. Appenrodt E, Kroning G, Schwarzberg H (1999) Increased plasma ACTH in rats exposed to the elevated plus-maze is independent of the pineal gland. Psychoneuroendocrinology 24:833-838 (Pubitemid 29461056)
5. Bailey SJ, Toth M (2004) Variability in the benzodiazepine response of serotonin 5-HT1A receptor null mice displaying anxiety-like phenotype: evidence for genetic modifiers in the 5-HT-mediated regulation of GABA(A) receptors. J Neurosci 24:6343-6351 (Pubitemid 38944225)
6. Barbaccia ML, Costa E, Ferrero P, Guidotti A, Roy A, Sunderland T, Pickar D, Paul SM, Goodwin FK (1986) Diazepam-binding inhibitor. A brain neuropeptide present in human spinal fluid: studies in depression, schizophrenia, and Alzheimer's disease. Arch Gen Psychiatry 43:1143-1147
7. Bourin M, Hascoet M (2001) Drug mechanisms in anxiety. Curr Opin Investig Drugs 2:259-265 (Pubitemid 32185953)
8. Britton KT, Lee G, Koob GF (1988) Corticotropin releasing factor and amphetamine exaggerate partial agonist properties of benzodiazepine antagonist Ro 15-1788 in the conflict test. Psychopharmacol (Berl) 94:306-311 (Pubitemid 18074017)
9. Cagetti E, Liang J, Spigelman I, Olsen RW (2003) Withdrawal from chronic intermittent ethanol treatment changes subunit composition reduces synaptic function, and decreases behavioral responses to positive allosteric modulators of GABAA receptors. Mol Pharmacol 63:53-64 (Pubitemid 36043808)
10. Calogero AE, Gallucci WT, Chrousos GP, Gold PW (1988) Interaction between GABAergic neurotransmission and rat hypothalamic corticotropin-releasing hormone secretion in vitro. Brain Res 463:28-36
11. Carli M, Tatarczynska E, Cervo L, Samanin R (1993) Stimulation of hippocampal 5-HT1A receptors causes amnesia and anxiolytic-like but not antidepressant-like effects in the rat. Eur J Pharmacol 234:215-221 (Pubitemid 23103443)
12. Charney DS, Drevets WC (2002) Neurobiological basis of anxiety disorders. In: Davis KL, Charney DS, Coyle J, Nemeroff C (eds) Neuropsychopharmacology: the Fifth Generation of Progress. American College of Neuropsychopharmacology. Lippincott Williams & Wilkins, Baltimore, MD, pp 901-930
13. Cossart R, Epsztein J, Tyzio R, Becq H, Hirsch J, Ben-Ari Y, Crepel V (2002) Quantal release of glutamate generates pure kainate and mixed AMPA/kainate EPSCs in hippocampal neurons. Neuron 35:147-159 (Pubitemid 34804329)
14. Costa E, Guidotti A (1991) Diazepam binding inhibitor (DBI): a peptide with multiple biological actions. Life Sci 49:325-344
15. Crawley JN (1996) Unusual behavioral phenotypes of inbred mouse strains. Trends Neurosci 19:181-182
16. Crawley J (2007) What's wrong with my mouse: behavioral phenotyping of transgenic and knockout mice. John Wiley and Sons, Hoboken
17. Dos SL, De Andrade TG, Zangrossi JH (2008) 5-HT1A receptors in the dorsal hippocampus mediate the anxiogenic effect induced by the stimulation of 5-HT neurons in the median raphe nucleus. Eur Neuropsychopharmacol 18:286-294
18. Fanselow MS, Dong HW (2010) Are the dorsal and ventral hippocampus functionally distinct structures? Neuron 65:7-19
19. File SE (2001) Factors controlling measures of anxiety and responses to novelty in the mouse. Behav Brain Res 125:151-157
20. 1A-receptor ligands in dorsal raphe and ventral hippocampus. Pharmacol Biochem Behav 54:123-128
21. 1A receptor modulation of anxiety in two ethological animal tests. J Neurosci 16:4810-4815
22. File SE, Mabbutt PS, Hitchcott PK (1990) Characterisation of the phenomenon of "one-trial tolerance" to the anxiolytic effect of chlordiazepoxide in the elevated plus-maze. Psychopharmacol (Berl) 102:98-101
23. File SE, Zangrossi H Jr, Sanders FL, Mabbutt PS (1994) Raised corticosterone in the rat after exposure to the elevated plus-maze. Psychopharmacol (Berl) 113:543-546 (Pubitemid 24150508)
24. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470 (Pubitemid 126682925)
25. Gerlai R (2001) Gene targeting: technical confounds and potential solutions in behavioral brain research. Behav Brain Res 125:13-21
26. Gordon JA, Lacefield CO, Kentros CG, Hen R (2005) State-dependent alterations in hippocampal oscillations in serotonin 1A receptor-deficient mice. J Neurosci 25:6509-6519 (Pubitemid 40995283)
27. Graeff FG, Guimaraes FS, De Andrade TG, Deakin JF (1996) Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54:129-141 (Pubitemid 26146666)
28. Gray JA, McNaughton N (2003) The neuropsychology of anxiety: an enquiry into the function of the septo-hippocampal system. Oxford University Press, Oxford
29. Griebel G, Moreau JL, Jenck F, Martin JR, Misslin R (1993) Some critical determinants of the behavior of rats in the elevated plus-maze. Behav Process 29:37-47
30. Gross C, Zhuang X, Stark K, Ramboz S, Oosting R, Kirby L, Santarelli L, Beck S, Hen R (2002) Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature 416:396-400 (Pubitemid 34272867)
31. Heisler LK, Chu HM, Brennan TJ, Danao JA, Bajwa P, Parsons LH, Tecott LH (1998) Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc Natl Acad Sci USA 95:15049-15054 (Pubitemid 29003754)
32. Hogg S (1996) A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Biochem Behav 54:21-30
33. Hogg S, Andrews N, File SE (1994) Contrasting behavioural effects of 8-OH DPAT in the dorsal raphe nucleus and ventral hippocampus. Neuropharmacology 33:343-348
34. Jacobson L, Sapolsky RM (1991) The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118-134
35. Jolas T, Schreiber R, Laporte AM, Chastanet M, De VJ, Glaser T, Adrien J, Hamon M (1995) Are postsynaptic 5-HT1A receptors involved in the anxiolytic effects of 5-HT1A receptor agonists and in their inhibitory effects on the firing of serotonergic neurons in the rat? J Pharmacol Exp Ther 272:920-929
36. Kataoka Y, Shibata K, Miyazaki A, Inoue Y, Tominaga K, Koizumi S, Ueki S, Niwa M (1991) Involvement of the dorsal hippocampus in mediation of the antianxiety action of tandospirone, a 5-hydroxytryptamine1A agonistic anxiolytic. Neuropharmacology 30:475-480
37. Kostowski W, Plaznik A, Stefanski R (1989) Intra-hippocampal buspirone in animal models of anxiety. Eur J Pharmacol 168:393-396 (Pubitemid 19231518)
38. Lacaille JC, Mueller AL, Kunkel DD, Schwartzkroin PA (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7:1979-1993 (Pubitemid 17114922)
39. Lister RG (1987) The use of a plus-maze to measure anxiety in the mouse. Psychopharmacol (Berl) 92:180-185
40. Lo IL, Gross C (2008) Alpha-Ca2+/calmodulin-dependent protein kinase II contributes to the developmental programming of anxiety in serotonin receptor 1A knock-out mice. J Neurosci 28:6250-6257
41. Lucki I (1996) Serotonin receptor specificity in anxiety disorders. J Clin Psychiatry 57 Suppl 6:5-10
42. Maguire JL, Stell BM, Rafizadeh M, Mody I (2005) Ovarian cycle-linked changes in GABA(A) receptors mediating tonic inhibition alter seizure susceptibility and anxiety. Nat Neurosci 8:797-804 (Pubitemid 43085847)
43. Mayorga AJ, Dalvi A, Page ME, Zimov-Levinson S, Hen R, Lucki I (2001) Antidepressant-like behavioral effects in 5-hydroxytryptamine(1A) and 5-hydroxytryptamine(1B) receptor mutant mice. J Pharmacol Exp Ther 298:1101-1107 (Pubitemid 32761926)
44. McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87:873-904
45. McEwen BS, Gould EA, Sakai RR (1992) The vulnerability of the hippocampus to protective and destructive effects of glucocorticoids in relation to stress. Br J Psychiatry 15(Suppl):18-23
46. McEwen BS, Magarinos AM (1997) Stress effects on morphology and function of the hippocampus. Ann NY Acad Sci 821:271-284 (Pubitemid 27343028)
47. Menard J, Treit D (1998) The septum and the hippocampus differentially mediate anxiolytic effects of R(+)-8-OH-DPAT. Behav Pharmacol 9:93-101 (Pubitemid 28186506)
48. Menard J, Treit D (1999) Effects of centrally administered anxiolytic compounds in animal models of anxiety. Neurosci Biobehav Rev 23:591-613 (Pubitemid 29086927)
49. Millan MJ (2003) The neurobiology and control of anxious states. Prog Neurobiol 70:83-244
50. Neumeister A, Bain E, Nugent AC, Carson RE, Bonne O, Luckenbaugh DA, Eckelman W, Herscovitch P, Charney DS, Drevets WC (2004) Reduced serotonin type 1A receptor binding in panic disorder. J Neurosci 24:589-591 (Pubitemid 38166482)
51. Parks CL, Robinson PS, Sibille E, Shenk T, Toth M (1998) Increased anxiety of mice lacking the serotonin1A receptor. Proc Natl Acad Sci USA 95:10734-10739
52. Pattij T, Groenink L, Oosting RS, van der GJ M, RA OB (2002) GABA(A)-benzodiazepine receptor complex sensitivity in 5-HT (1A) receptor knockout mice on a 129/Sv background. Eur J Pharmacol 447:67-74 (Pubitemid 34775222)
53. Pellow S, Chopin P, File SE, Briley M (1985) Validation of open: closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods 14:149-167 (Pubitemid 16239568)
54. Phillips TJ, Hen R, Crabbe JC (1999) Complications associated with genetic background effects in research using knockout mice. Psychopharmacol (Berl) 147:5-7 (Pubitemid 30010010)
55. Ramboz S, Oosting R, Amara DA, Kung HF, Blier P, Mendelsohn M, Mann JJ, Brunner D, Hen R (1998) Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc Natl Acad Sci USA 95:14476-14481 (Pubitemid 28549392)
56. Ravindran LN, Stein MB (2010) The pharmacologic treatment of anxiety disorders: a review of progress. J Clin Psychiatry 71:839-854
57. Rodgers RJ, Haller J, Holmes A, Halasz J, Walton TJ, Brain PF (1999) Corticosterone response to the plus-maze: high correlation with risk assessment in rats and mice. Physiol Behav 68:47-53 (Pubitemid 30009781)
58. Rodgers RJ, Lee C, Shepherd JK (1992) Effects of diazepam on behavioural and antinociceptive responses to the elevated plus-maze in male mice depend upon treatment regimen and prior maze experience. Psychopharmacol (Berl) 106:102-110
59. Rodgers RJ, Shepherd JK (1993) Influence of prior maze experience on behaviour and response to diazepam in the elevated plus-maze and light/dark tests of anxiety in mice. Psychopharmacol (Berl) 113:237-242 (Pubitemid 24001999)
60. Sandford JJ, Argyropoulos SV, Nutt DJ (2000) The psychobiology of anxiolytic drugs. Part 1: Basic neurobiology. Pharmacol Ther 88:197-212
61. Sarnyai Z, Sibille EL, Pavlides C, Fenster RJ, McEwen BS, Toth M (2000) Impaired hippocampal-dependent learning and functional abnormalities in the hippocampus in mice lacking serotonin(1A) receptors. Proc Natl Acad Sci USA 97:14731-14736 (Pubitemid 32016644)
62. Schreiber R, De Vry J (1993) Neuronal circuits involved in the anxiolytic effects of the 5-HT1A receptor agonists 8-OH-DPAT ipsapirone and buspirone in the rat. Eur J Pharmacol 249:341-351 (Pubitemid 23334109)
63. Sibille E, Pavlides C, Benke D, Toth M (2000) Genetic inactivation of the Serotonin(1A) receptor in mice results in downregulation of major GABA(A) receptor alpha subunits, reduction of GABA(A) receptor binding, and benzodiazepine-resistant anxiety. J Neurosci 20:2758-2765 (Pubitemid 30220299)
64. Skelton KH, Nemeroff CB, Knight DL, Owens MJ (2000) Chronic administration of the triazolobenzodiazepine alprazolam produces opposite effects on corticotropin-releasing factor and urocortin neuronal systems. J Neurosci 20:1240-1248 (Pubitemid 30220480)
65. Smith SS, Gong QH, Li X, Moran MH, Bitran D, Frye CA, Hsu FC (1998) Withdrawal from 3alpha-OH-5alpha-pregnan-20-One using a pseudopregnancy model alters the kinetics of hippocampal GABAA-gated current and increases the GABAA receptor alpha4 subunit in association with increased anxiety. J Neurosci 18:5275-5284 (Pubitemid 28311944)
66. Stefanski R, Palejko W, Bidzinski A, Kostowski W, Plaznik A (1993) Serotonergic innervation of the hippocampus and nucleus accumbens septi and the anxiolytic-like action of midazolam and 5-HT1A receptor agonists. Neuropharmacology 32:977-985 (Pubitemid 23316504)
67. Treit D, Menard J, Royan C (1993) Anxiogenic stimuli in the elevated plus-maze. Pharmacol Biochem Behav 44:463-469
68. Van Sickle BJ, Xiang K, Tietz EI (2004) Transient plasticity of hippocampal CA1 neuron glutamate receptors contributes to benzodiazepine withdrawal-anxiety. Neuropsychopharmacology 29:1994-2006 (Pubitemid 39486551)