Glutamatergic and GABAergic modulations of ultrasonic vocalizations during maternal separation distress in mouse pups

Psychopharmacology

Volumn 204, Issue 1, 2009, Pages 61-71

  Takahashi, Aki ^a   Yap, Jasmine J ^a   Bohager, Dawnya Zitzman ^a,c   Faccidomo, Sara ^a,c   Clayton, Terry ^b   Cook, James M ^b   Miczek, Klaus A ^a  

^a TUFTS UNIVERSITY   (United States)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Anxiety; GABAA receptor subtypes; MGluR2 3; Motor activity; Motor incoordination; Mouse pups; NMDA receptor; Ultrasonic vocalizations

Indexed keywords

2 AMINO 2 (2 CARBOXYCYCLOPROPYL) 3 (XANTHEN 9 YL)PROPIONIC ACID; 4 AMINO 2 OXABICYCLO[3.1.0]HEXANE 4,6 DICARBOXYLIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; 7 TERT BUTYL 3 (2,5 DIFLUOROPHENYL) 6 (2 METHYL 2H 1,2,4 TRIAZOL 3 YLMETHOXY) 1,2,4 TRIAZOLO[4,3 B]PYRIDAZINE; BENZODIAZEPINE DERIVATIVE; BROMAZEPAM; CHLORDIAZEPOXIDE; DIZOCILPINE; FLUNITRAZEPAM; GLUTAMATE RECEPTOR; MEMANTINE; METABOTROPIC RECEPTOR AGONIST; METABOTROPIC RECEPTOR ANTAGONIST; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NERAMEXANE; QH II 066; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BODY TEMPERATURE; CONTROLLED STUDY; DOSE RESPONSE; GABAERGIC SYSTEM; LOCOMOTION; MATERNAL DEPRIVATION; MOTOR ACTIVITY; MOTOR COORDINATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SEPARATION ANXIETY; TRANQUILIZING ACTIVITY; VOCALIZATION;

ANIMALS; ANIMALS, NEWBORN; ANTI-ANXIETY AGENTS; ANXIETY; BEHAVIOR, ANIMAL; GABA AGENTS; LOCOMOTION; MATERNAL DEPRIVATION; MICE; MOTOR ACTIVITY; PROTEIN SUBUNITS; RECEPTORS, GABA-A; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, N-METHYL-D-ASPARTATE; SOUND SPECTROGRAPHY; ULTRASONICS; VOCALIZATION, ANIMAL;

EID: 67349156666     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-008-1437-8     Document Type: Article

References (81)

1. A receptors, is a nonsedating anxiolytic in rodents and primates J Pharmacol Exp Ther 316 410 422 (Pubitemid 41832621)
2. C Belzung AM Le Guisquet G Griebel 2000 β-CCT, a selective BZ-ω1 receptor antagonist, blocks the anti-anxiety but not the amnesic action of chlordiazepoxide in mice Behav Pharmacol 11 125 131 (Pubitemid 30315847)
3. D Benton K Nastiti 1988 The influence of psychotropic drugs on the ultrasonic calling of mouse pups Psychopharmacology 95 99 102 (Pubitemid 18111711)
4. V Bergink HJ van Megen HG Westenberg 2004 Glutamate and anxiety Eur Neuropsychopharmacol 14 175 183 (Pubitemid 38410952)
5. MS Blumberg G Sokoloff RF Kirby KJ Kent 2000 Distress vocalizations in infant rats: what's all the fuss about Psychol Sci 11 78 81
6. JD Bremner RB Innis SM Southwick L Staib S Zoghbi DS Charney 2000 Decreased benzodiazepine receptor binding in prefrontal cortex in combat-related posttraumatic stress disorder Am J Psychiatry 157 1120 1126 (Pubitemid 30432494)
7. JD Bremner RB Innis T White M Fujita D Silbersweig AW Goddard L Staib E Stern A Cappiello S Woods R Baldwin DS Charney 2000 SPECT [I-123]iomazenil measurement of the benzodiazepine receptor in panic disorder Biol Psychiatry 47 96 106 (Pubitemid 30069732)
8. I Bresink W Danysz CG Parsons E Mutschler 1995 Different binding affinities of NMDA receptor channel blockers in various brain regions-indication of NMDA receptor heterogeneity Neuropharmacology 34 533 540
9. SA Brunelli HN Shair MA Hofer 1994 Hypothermic vocalizations of rat pups (Rattus norvegicus) elicit and direct maternal search behavior J Comp Psychol 108 298 303
10. B Buisson D Bertrand 1998 Open-channel blockers at the human α4β2 neuronal nicotinic acetylcholine receptor Mol Pharmacol 53 555 563 (Pubitemid 28162880)
11. B Clineschmidt M Williams J Witoslawski P Bunting A Risley J Totaro 1982 Restoration of shock-suppressed behavior by treatment with (+)-5-methyl-10,11- dihydro-5H-dibenzo[a,d]-cyclohepten-5,10-imine (MK-801), a substance with potent anticonvulsant, central sympathomimetic, and apparent anxiolytic properties Drug Dev Res 2 147 163
12. A receptor-ion channels J Med Chem 45 1887 1900 (Pubitemid 34415384)
13. A-receptor clustering results in enhanced anxiety and a bias for threat cues Nat Neurosci 2 833 839 (Pubitemid 30491177)
14. HE Criswell DJ Knapp DH Overstreet GR Breese 1994 Effects of ethanol, chlordiazepoxide, and MK-801 on performance in the elevated-plus maze and on locomotor activity Alcohol Clin Exp Res 18 596 601 (Pubitemid 24189284)
15. 2 in the hypothalamus and limbic system of the rat Brain Res Dev Brain Res 119 127 38 (Pubitemid 30058389)
16. A receptors in mediating the anxiolytic effects of benzodiazepines J Neurosci 25 10682 10688 (Pubitemid 41681916)
17. A Dirks EW Fish T Kikusui J van der Gugten L Groenink B Olivier KA Miczek 2002 Effects of corticotropin-releasing hormone on distress vocalizations and locomotion in maternally separated mouse pups Pharmacol Biochem Behav 72 993 999 (Pubitemid 34621327)
18. BD Drever WG Anderson H Johnson M O'Callaghan S Seo DY Choi G Riedel B Platt 2007 Memantine acts as a cholinergic stimulant in the mouse hippocampus J Alzheimers Dis 12 319 333
19. A receptors Psychopharmacology 149 277 285 (Pubitemid 30262342)
20. EW Fish S Faccidomo S Gupta KA Miczek 2004 Anxiolytic-like effects of escitalopram, citalopram, and R-citalopram in maternally separated mouse pups J Pharmacol Exp Ther 308 474 480 (Pubitemid 38134207)
21. A-receptor subtypes during postnatal development: an immunohistochemical study J Neurosci 14 5302 5324 (Pubitemid 24279052)
22. CR Gardner 1985 Distress vocalization in rat pups a simple screening method for anxiolytic drugs J Pharmacol Meth 14 181 187 (Pubitemid 15241172)
23. A) receptors J Pharmacol Exp Ther 298 753 768 (Pubitemid 32673429)
24. FS Guimarães AP Carobrez JC De Aguiar FG Graeff 1991 Anxiolytic effect in the elevated plus-maze of the NMDA receptor antagonist AP7 microinjected into the dorsal periaqueductal grey Psychopharmacology 103 91 94
25. DR Helton JP Tizzano JA Monn DD Schoepp MJ Kallman 1998 Anxiolytic and side-effect profile of LY354740: a potent, highly selective, orally active agonist for group II metabotropic glutamate receptors J Pharmacol Exp Ther 284 651 660 (Pubitemid 28086655)
26. JP Herman NK Mueller H Figueiredo 2004 Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration Ann N Y Acad Sci 1018 35 45 (Pubitemid 38951388)
27. A/BzR subtypes (α1β3γ2, α5β3γ2, and α6β3γ2) via a comprehensive ligand-mapping approach J Med Chem 43 71 95 (Pubitemid 30055764)
28. TR Insel JL Hill RB Mayor 1986 Rat pup ultrasonic isolation calls: possible mediation by the benzodiazepine receptor complex Pharmacol Biochem Behav 24 1263 1267 (Pubitemid 16067408)
29. JH Kehne TC [tmp] McCloskey BM Baron EM Chi BL Harrison JP Whitten MG Palfreyman 1991 NMDA receptor complex antagonists have potential anxiolytic effects as measured with separation-induced ultrasonic vocalizations Eur J Pharmacol 193 283 292
30. JH Kehne BM Baron BL Harrison TC [tmp] McCloskey MG Palfreyman M Poirot FG Salituro BW Siegel AL Slone PL Van Giersbergen HS White 1995 MDL 100,458 and MDL 102,288: two potent and selective glycine receptor antagonists with different functional profiles Eur J Pharmacol 284 109 118
31. AE Kingston PL Ornstein RA Wright BG Johnson NG Mayne JP Burnett R Belagaje S Wu DD Schoepp 1998 LY341495 is a nanomolar potent and selective antagonist of group II metabotropic glutamate receptors Neuropharmacology 37 1 12 (Pubitemid 28300133)
32. A Kłodzińska E Chojnacka-Wójcik A Pałucha P Brański P Popik A Pilc 1999 Potential anti-anxiety, anti-addictive effects of LY 354740, a selective group II glutamate metabotropic receptors agonist in animal models Neuropharmacology 38 1831 1839 (Pubitemid 29509721)
33. J Kornhuber M Weller 1997 Psychotogenicity and N-methyl-d-aspartate receptor antagonism: implications for neuroprotective pharmacotherapy Biol Psychiatry 41 135 44 (Pubitemid 27062653)
34. A receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development J Neurosci 12 4151 4172
35. A receptor modulator Proc Natl Acad Sci U S A 102 7380 7385 (Pubitemid 40696386)
36. GX Liu GQ Cai YQ Cai ZJ Sheng J Jiang Z Mei ZG Wang L Guo J Fei 2007 Reduced anxiety and depression-like behaviors in mice lacking GABA transporter subtype 1 Neuropsychopharmacology 32 1531 1539 (Pubitemid 46920158)
37. K Löw F Crestani R Keist D Benke I Brünig JA Benson JM Fritschy T Rülicke H Bluethmann H Möhler U Rudolph 2000 Molecular and neuronal substrate for the selective attenuation of anxiety Science 290 131 134
38. C Maldonado O Cauli M Rodríguez-Arias MA Aguilar J Miñarro 2003 Memantine presents different effects from MK-801 in motivational and physical signs of morphine withdrawal Behav Brain Res 144 25 35 (Pubitemid 37011163)
39. A-benzodiazepine receptor binding in panic disorder: preliminary results from a quantitative PET study Arch Gen Psychiatry 55 715 720 (Pubitemid 28364388)
40. L Mathiasen NR Mirza 2005 A comparison of chlordiazepoxide, bretazenil, L838,417 and zolpidem in a validated mouse Vogel conflict test Psychopharmacology 182 475 484 (Pubitemid 41464628)
41. A receptor α1 subtype Nat Neurosci 3 587 592 (Pubitemid 30332078)
42. A and 5-HT anxiolytics Psychopharmacology 121 38 56
43. KA Miczek JJ Yap HE Covington 2008 Social stress, therapeutics and drug abuse: preclinical models of escalated and depressed intake Pharmacol Ther 120 102 128
44. JA Monn MJ Valli SM Massey MM Hansen TJ Kress JP Wepsiec AR Harkness JL Grutsch Jr RA Wright BG Johnson SL Andis A Kingston R Tomlinson R Lewis KR Griffey JP Tizzano DD Schoepp 1999 Synthesis, pharmacological characterization, and molecular modeling of heterobicyclic amino acids related to (+)-2-aminobicyclo[3.1.0] hexane-2,6-dicarboxylic acid (LY354740): Identification of two new potent, selective, and systemically active agonists for group II metabotropic glutamate receptors J Med Chem 42 1027 1040 (Pubitemid 29153432)
45. H Monyer N Burnashev DJ Laurie B Sakmann PH Seeburg 1994 Developmental and regional expression in the rat brain and functional properties of four NMDA receptors Neuron 12 529 540 (Pubitemid 24100885)
46. K Nastiti D Benton PF Brain 1991 The effects of compounds acting at the benzodiazepine receptor complex on the ultrasonic calling of mouse pups Behav Pharmacol 2 121 128
47. E Noirot 1966 Ultrasounds in young rodents. I. Changes with age in albino rats Anim Behav 14 459 462
48. E Noirot 1972 Ultrasounds and maternal behavior in small rodents Develop Psychobiol 5 371 387
49. RE Nordquist T Steckler JG Wettstein C Mackie W Spooren 2008 Metabotropic glutamate receptor modulation, translational methods, and biomarkers: relationships with anxiety Psychopharmacology 199 389 402
50. B Olivier E Molewijk R van Oorschot G van der Poel T Zethof J van der Heyden J Mos 1994 New animal models of anxiety Eur Neuropsychopharmacol 4 93 102 (Pubitemid 24199858)
51. B Olivier E Molewijk R van Oorschot J van der Heyden E Ronken J Mos 1998 Rat pup ultrasonic vocalization: effects of benzodiazepine receptor ligands Eur J Pharmacol 358 117 128 (Pubitemid 28458883)
52. B Olivier E Molewijk JAM van der Heyden R van Oorschot E Ronken J Mos KA Miczek 1998 Ultrasonic vocalization in rat pups: effects of serotonergic ligands Neurosci Biobehav Rev 23 215 227 (Pubitemid 29011623)
53. CG Parsons G Quack I Bresink L Baran E Przegalinski W Kostowski P Krzascik S Hartmann W Danysz 1995 Comparison of the potency, kinetics and voltage-dependency of a series of uncompetitive NMDA receptor antagonists in vitro with anticonvulsive and motor impairment activity in vivo Neuropharmacology 34 1239 1258
54. CG Parsons W Danysz A Bartmann P Spielmanns T Frankiewicz M Hesselink B Eilbacher G Quack 1999 Amino-alkyl-cyclohexanes are novel uncompetitive NMDA receptor antagonists with strong voltage-dependency and fast blocking kinetics: in vitro and in vivo characterization Neuropharmacology 38 85 108 (Pubitemid 29073529)
55. CG Parsons A Stöffler W Danysz 2007 Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system-too little activation is bad, too much is even worse Neuropharmacology 53 699 723 (Pubitemid 47532143)
56. M Pérez de la Mora D Lara-García KX Jacobsen M Vázquez-García M Crespo-Ramírez C Flores-Gracia E Escamilla-Marvan K Fuxe 2006 Anxiolytic-like effects of the selective metabotropic glutamate receptor 5 antagonist MPEP after its intra-amygdaloid microinjection in three different non-conditioned rat models of anxiety Eur J Neurosci 23 2749 2759 (Pubitemid 43801467)
57. PV Plazas J Savino S Kracun ME Gomez-Casati E Katz CG Parsons NS Millar AB Elgoyhen 2007 Inhibition of the α9α10 nicotinic cholinergic receptor by neramexane, an open channel blocker of N-methyl-d-aspartate receptors Eur J Pharmacol 566 11 19 (Pubitemid 46782793)
58. DG Rainnie EK Asprodini P Shinnick-Gallagher 1991 Excitatory transmission in the basolateral amygdala J. Neurophysiol 66 986 998
59. JK Rowlett W Tornatzky JM Cook C Ma KA Miczek 2001 Zolpidem, triazolam, and diazepam decrease distress vocalizations in mouse pups: Differential antagonism by flumazenil and β-Carboline-3-carboxylate-t-butyl ester (β-CCt) J Pharmacol Exp Ther 297 247 253 (Pubitemid 32243489)
60. A receptor subtypes mediate the anxiolytic, abuse-related, and motor effects of benzodiazepine-like drugs in primates Proc Natl Acad Sci U S A 102 915 20 (Pubitemid 40282765)
61. P Roy-Byrne DK Wingerson A Radant DJ Greenblatt DS Cowley 1996 Reduced benzodiazepine sensitivity in patients with panic disorder: comparison with patients with obsessive-compulsive disorder and normal subjects Am J Psychiatry 153 1444 1449 (Pubitemid 26365459)
62. A receptor subtypes Nature 401 796 800 (Pubitemid 129515840)
63. A receptor blockade in the basolateral amygdala of rats J Pharmacol Exp Ther 283 969 977 (Pubitemid 27514662)
64. A Satow S Maehara S Ise H Hikichi M Fukushima G Suzuki T Kimura T Tanak S Ito H Kawamoto H Ohta 2008 Pharmacological effects of the metabotropic glutamate receptor 1 antagonist compared with those of the metabotropic glutamate receptor 5 antagonist and metabotropic glutamate receptor 2/3 agonist in rodents: detailed investigations with a selective allosteric metabotropic glutamate receptor 1 antagonist, FTIDC [4-[1-(2-fluoropyridine-3-yl)-5-methyl- 1H-1,2,3-triazol-4-yl]-N-isopropyl-N-methyl-3,6-dihydropyridine-1(2H) -carboxamide] J Pharmacol Exp Ther 326 577 586
65. A receptors containing α5 subunits contributing to the sedative properties of benzodiazepine site agonists Neuropsychopharmacology 33 332 339 (Pubitemid 350243345)
66. Sales GD, Pye D (1974) Ultrasonic communication by animals. Chapman & Hall, London
67. RI Shader DJ Greenblatt 1993 Use of benzodiazepines in anxiety disorders N Engl J Med 328 1398 1405 (Pubitemid 23131393)
68. M Sheng J Cummings LA Roldan YN Jan LY Jan 1994 Changing subunit composition of heteromeric NMDA receptors during development of rat cortex Nature 368 144 147 (Pubitemid 24101524)
69. A receptors containing alpha-5 subunits J Pharmacol Exp Ther 283 488 493 (Pubitemid 27514602)
70. BN Smith FE Dudek 1996 Amino acid-mediated regulation of spontaneous synaptic patterns in the rat basolateral amygdala J Neurophysiol 76 1958 1967 (Pubitemid 26322631)
71. O Stork FY Ji K Kaneko S Stork Y Yoshinobu T Moriya S Shibata K Obata 2000 Postnatal development of a GABA deficit and disturbance of neural functions in mice lacking GAD65 Brain Res 865 45 58 (Pubitemid 30256206)
72. CJ Swanson M Bures MP Johnson AM Linden JA Monn DD Schoepp 2005 Metabotropic glutamate receptors as novel targets for anxiety and stress disorders Nat Rev Drug Discov 4 131 144 (Pubitemid 40277494)
73. E Tatarczyńska A Kłodzińska B Kroczka E Chojnacka-Wójcik A Pilc 2001 The antianxiety-like effects of antagonists of group I and agonists of group II and III metabotropic glutamate receptors after intrahippocampal administration Psychopharmacology 158 94 99 (Pubitemid 32938318)
74. J Tiihonen J Kuikka P Rasanen U Lepola H Koponen A Liuska A Lehmusvaara P Vainio M Kononen K Bergstrom M Yu I Kinnunen K Akerman J Karhu 1997 Cerebral benzodiazepine receptor binding and distribution in generalized anxiety disorder: a fractal analysis Mol Psychiatry 2 463 471 (Pubitemid 27482948)
75. C van Rijnsoever M Täuber MK Choulli R Keist U Rudolph H Mohler JM Fritschy F Crestani 2004 Requirement of alpha5-GABAA receptors for the development of tolerance to the sedative action of diazepam in mice J Neurosci 24 6785 6790 (Pubitemid 38993900)
76. A receptor complex and the neurosteroid recognition site J Pharmacol Exp Ther 282 318 325 (Pubitemid 27425557)
77. GS Watson JT Roach KJ Sufka 1999 Benzodiazepine receptor function in the chick social separation-stress procedure Exp Clin Psychopharmacol 7 83 89 (Pubitemid 29228294)
78. JL Wiley 1997 Behavioral pharmacology of N-methyl-d-aspartate antagonists: implications for the study and pharmacotherapy of anxiety and schizophrenia Exp Clin Psychopharmacol 5 365 374 (Pubitemid 27490383)
79. JT Winslow TR Insel 1991 Infant rat separation is a sensitive test for novel anxiolytics Progr Neuropsychopharmacol Biol Psychiatry 15 745 757
80. W Zajaczkowski G Quack W Danysz 1996 Infusion of (+)-MK-801 and memantine-contrasting effects on radial maze learning in rats with entorhinal cortex lesion Eur J Pharmacol 296 239 246 (Pubitemid 126334461)
81. PR Zoladz AM Campbell CR Park D Schaefer W Danysz DM Diamond 2006 Enhancement of long-term spatial memory in adult rats by the noncompetitive NMDA receptor antagonists, memantine and neramexane Pharmacol Biochem Behav 85 298 306