Selective effects of benzodiazepines on the acquisition of conditioned taste aversion compared to attenuation of neophobia in C57BL/6 mice

Psychopharmacology

Volumn 206, Issue 3, 2009, Pages 389-401

  Callaerts Vegh, Zsuzsanna ^b   Hoyer, Daniel ^a   Kelly, Peter H ^a  

^a NOVARTIS PHARMA AG   (Switzerland)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Acquisition; Alprazolam; Anxiolytics; Attenuation of neophobia; Benzodiazepines; Chlordiazepoxide; Conditioned taste aversion; Mouse

Indexed keywords

ALPRAZOLAM; ANXIOLYTIC AGENT; CHLORDIAZEPOXIDE; LITHIUM CHLORIDE; SACCHARIN;

ANIMAL EXPERIMENT; ARTICLE; ATTENUATION; C57BL 6 MOUSE; CONDITIONING; CONTROLLED STUDY; DRUG EFFECT; DRUG SELECTIVITY; LEARNING; MALE; MEMORY; MOUSE; NEOPHOBIA; NONHUMAN; PRIORITY JOURNAL; TASTE AVERSION;

ALPRAZOLAM; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BENZODIAZEPINES; CHLORDIAZEPOXIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRINKING BEHAVIOR; EXTINCTION, PSYCHOLOGICAL; HYPNOTICS AND SEDATIVES; MALE; MICE; MICE, INBRED C57BL; SACCHARIN; TASTE;

EID: 70349579042     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-009-1614-4     Document Type: Article

References (76)

1. F Anglade JC Bizot RH Dodd C Baudoin G Chapouthier 1994 Opposite effects of cholinergic agents and benzodiazepine receptor ligands in a passive avoidance task in rats Neurosci Lett 182 2 247 250 7715820 10.1016/0304-3940(94)90808-7 (Pubitemid 24380248)
2. JR Atack 2003 Anxioselective compounds acting at the GABA(A) receptor benzodiazepine binding site Curr Drug Targets CNS Neurol Disord 2 4 213 232 12871032 10.2174/1568007033482841
3. JM Baas C Grillon KB Bocker AA Brack CA Morgan 3rd JL Kenemans MN Verbaten 2002 Benzodiazepines have no effect on fear-potentiated startle in humans Psychopharmacology (Berlin) 161 3 233 247 10.1007/s00213-002-1011-8 (Pubitemid 34591661)
4. M Barad 2005 Fear extinction in rodents: basic insight to clinical promise Curr Opin Neurobiol 15 6 710 715 16260129 10.1016/j.conb.2005.10.005 (Pubitemid 41682313)
5. CH Beck HC Fibiger 1995 Conditioned fear-induced changes in behavior and in the expression of the immediate early gene c-fos: with and without diazepam pretreatment J Neurosci 15 1 Pt 2 709 720 7823174
6. DE Berman Y Dudai 2001 Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex Science 291 5512 2417 2419 11264539 10.1126/science.1058165 (Pubitemid 32231805)
7. F Bermudez-Rattoni 2004 Molecular mechanisms of taste-recognition memory Nat Rev Neurosci 5 3 209 217 14976520 10.1038/nrn1344
8. KC Berridge D Treit 1986 Chlordiazepoxide directly enhances positive ingestive reactions in rats Pharmacol Biochem Behav 24 2 217 221 3952112 10.1016/0091-3057(86)90341-2 (Pubitemid 16185584)
9. DI Boomsma CE van Beijsterveldt JJ Hudziak 2005 Genetic and environmental influences on anxious/depression during childhood: a study from The Netherlands Twin Register Genes Brain Behav 4 8 466 481 16268991 10.1111/j.1601-183X.2005. 00141.x (Pubitemid 41689392)
10. M Bourin M Hascoet 2003 The mouse light/dark box test Eur J Pharmacol 463 1-3 55 65 12600702 10.1016/S0014-2999(03)01274-3 (Pubitemid 36205072)
11. ME Bouton 2002 Context, ambiguity, and unlearning: sources of relapse after behavioral extinction Biol Psychiatry 52 10 976 986 12437938 10.1016/S0006-3223(02)01546-9 (Pubitemid 35356355)
12. ME Bouton FA Kenney C Rosengard 1990 State-dependent fear extinction with two benzodiazepine tranquilizers Behav Neurosci 104 1 44 55 2317285 10.1037/0735-7044.104.1.44
13. CL Broekkamp M Le Pichon KG Lloyd 1984 The comparative effects of benzodiazepines, progabide and PK 9084 on acquisition of passive avoidance in mice Psychopharmacology (Berlin) 83 1 122 125 10.1007/BF00427435
14. Bures J, Bermudez Rattoni F, Yamamoto T (1998) Conditioned taste aversion: memory of a special kind. Oxford University Press, Oxford
15. O Buresova J Bures 1980 Post-ingestion interference with brain function prevents attenuation of neophobia in rats Behav Brain Res 1 4 299 312 7295379 10.1016/0166-4328(80)90023-6 (Pubitemid 10056510)
16. L Burriss E Ayers DA Powell 2007 Combat veterans show normal discrimination during differential trace eyeblink conditioning, but increased responsivity to the conditioned and unconditioned stimulus J Psychiatr Res 41 9 785 794 16716352 10.1016/j.jpsychires.2006.04.004 (Pubitemid 46659718)
17. G Chapouthier D Bondoux B Martin C Desforges JM Launay 1991 Genetic difference in sensitivity to beta-carboline: evidence for the involvement of brain benzodiazepine receptors Brain Res 553 2 342 346 1657284 10.1016/0006-8993(91)90847-O
18. JT Concannon J Freda 1980 Modulation of conditioned taste aversion by sodium pentobarbital Pharmacol Biochem Behav 13 6 761 764 6259666 10.1016/0091-3057(80)90203-8 (Pubitemid 11167891)
19. SJ Cooper 1989 Benzodiazepine receptor-mediated enhancement and inhibition of taste reactivity, food choice, and intake Ann N Y Acad Sci 575 321 336 2561252 10.1111/j.1749-6632.1989.tb53253.x discussion 336-337
20. JC Crabbe EJ Gallaher SJ Cross JK Belknap 1998 Genetic determinants of sensitivity to diazepam in inbred mice Behav Neurosci 112 3 668 677 9676982 10.1037/0735-7044.112.3.668 (Pubitemid 28309157)
21. JN Crawley 1985 Exploratory behavior models of anxiety in mice Neurosci Biobehav Rev 9 1 37 44 2858080 10.1016/0149-7634(85)90030-2 (Pubitemid 15136669)
22. JN Crawley JK Belknap A Collins JC Crabbe W Frankel N Henderson RJ Hitzemann SC Maxson LL Miner AJ Silva JM Wehner A Wynshaw-Boris R Paylor 1997 Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies Psychopharmacology (Berlin) 132 2 107 124 10.1007/s002130050327 (Pubitemid 27338986)
23. JF Cryan PH Kelly F Chaperon C Gentsch C Mombereau K Lingenhoehl W Froestl B Bettler K Kaupmann WP Spooren 2004 Behavioral characterization of the novel GABAB receptor-positive modulator GS39783 (N,N'-dicyclopentyl-2- methylsulfanyl-5-nitro-pyrimidine-4, 6-diamine): anxiolytic-like activity without side effects associated with baclofen or benzodiazepines J Pharmacol Exp Ther 310 3 952 963 15113848 10.1124/jpet.104.066753 (Pubitemid 39108915)
24. P D'Adamo DP Wolfer C Kopp I Tobler D Toniolo HP Lipp 2004 Mice deficient for the synaptic vesicle protein Rab3a show impaired spatial reversal learning and increased explorative activity but none of the behavioral changes shown by mice deficient for the Rab3a regulator Gdi1 Eur J Neurosci 19 7 1895 1905 15078563 10.1111/j.1460-9568.2004.03270.x (Pubitemid 38482577)
25. JR Davidson 2004 Use of benzodiazepines in social anxiety disorder, generalized anxiety disorder, and posttraumatic stress disorder J Clin Psychiatry 65 Suppl 5 29 33 15078116
26. M Davis 1990 Animal models of anxiety based on classical conditioning: the conditioned emotional response (CER) and the fear-potentiated startle effect Pharmacol Ther 47 2 147 165 2203068 10.1016/0163-7258(90)90084-F (Pubitemid 20228577)
27. M Davis 2002 Role of NMDA receptors and MAP kinase in the amygdala in extinction of fear: clinical implications for exposure therapy Eur J Neurosci 16 3 395 398 12193180 10.1046/j.1460-9568.2002.02138.x (Pubitemid 35471855)
28. R de Jongh L Groenink J van Der Gugten B Olivier 2002 The light-enhanced startle paradigm as a putative animal model for anxiety: effects of chlordiazepoxide, flesinoxan and fluvoxamine Psychopharmacology (Berlin) 159 2 176 180 10.1007/s002130100914 (Pubitemid 34146561)
29. MR Delgado A Olsson EA Phelps 2006 Extending animal models of fear conditioning to humans Biol Psychol 73 1 39 48 16472906 10.1016/j.biopsycho. 2006.01.006
30. H Dickinson-Anson JL McGaugh 1993 Midazolam administered into the amygdala impairs retention of an inhibitory avoidance task Behav Neural Biol 60 1 84 87 8105777 10.1016/0163-1047(93)90781-C
31. M Domjan D Gillan 1976 Role of novelty in the aversion for increasingly concentrated saccharin solutions Physiol Behav 16 5 537 542 972943 10.1016/0031-9384(76)90211-0
32. MS Fanselow FJ Helmstetter 1988 Conditional analgesia, defensive freezing, and benzodiazepines Behav Neurosci 102 2 233 243 3365319 10.1037/0735-7044.102.2.233 (Pubitemid 18213269)
33. GM Gafford RG Parsons FJ Helmstetter 2005 Effects of post-training hippocampal injections of midazolam on fear conditioning Learn Mem 12 6 573 578 16322359 10.1101/lm.51305 (Pubitemid 41770080)
34. E Gelpin O Bonne T Peri D Brandes AY Shalev 1996 Treatment of recent trauma survivors with benzodiazepines: a prospective study J Clin Psychiatry 57 9 390 394 9746445 (Pubitemid 26321989)
35. G Griebel C Belzung G Perrault DJ Sanger 2000 Differences in anxiety-related behaviours and in sensitivity to diazepam in inbred and outbred strains of mice Psychopharmacology (Berlin) 148 2 164 170 10.1007/s002130050038
36. C Grillon JM Baas DS Pine S Lissek M Lawley V Ellis J Levine 2006 The benzodiazepine alprazolam dissociates contextual fear from cued fear in humans as assessed by fear-potentiated startle Biol Psychiatry 60 7 760 766 16631127 10.1016/j.biopsych.2005.11.027 (Pubitemid 44427760)
37. R Gutierrez CJ Rodriguez-Ortiz V De La Cruz L Nunez-Jaramillo F Bermudez-Rattoni 2003 Cholinergic dependence of taste memory formation: evidence of two distinct processes Neurobiol Learn Mem 80 3 323 331 14521874 10.1016/S1074-7427(03)00066-2 (Pubitemid 37159359)
38. S Hogg 1996 A review of the validity and variability of the elevated plus-maze as an animal model of anxiety Pharmacol Biochem Behav 54 1 21 30 8728535 10.1016/0091-3057(95)02126-4 (Pubitemid 26146661)
39. S Hogg 1996 A review of the validity and variability of the elevated plus-maze as an animal model of anxiety Pharmacol Biochem Behav 54 1 21 30 8728535 10.1016/0091-3057(95)02126-4 (Pubitemid 26146661)
40. Y Iwamoto S Morinobu T Takahashi S Yamawaki 2007 Single prolonged stress increases contextual freezing and the expression of glycine transporter 1 and vesicle-associated membrane protein 2 mRNA in the hippocampus of rats Prog Neuropsychopharmacol Biol Psychiatry 31 3 642 651 17267088 10.1016/j.pnpbp.2006. 12.010 (Pubitemid 46476821)
41. RA Jensen JL Martinez Jr BJ Vasquez JL McGaugh 1979 Benzodiazepines alter acquisition and retention of an inhibitory avoidance response in mice Psychopharmacology (Berlin) 64 1 125 126 10.1007/BF00427358 (Pubitemid 9224422)
42. Kelly P, Callaerts-Vegh Z, Hoyer D (2005) Contrasting actions of chlordiazepoxide and scopolamine on conditioned taste aversion: implication for anxiolytic action. Prog. No. 416.10. Society of Neuroscience, Washington
43. S Lissek AS Powers EB McClure EA Phelps G Woldehawariat C Grillon DS Pine 2005 Classical fear conditioning in the anxiety disorders: a meta-analysis Behav Res Ther 43 11 1391 1424 15885654 10.1016/j.brat.2004.10.007 (Pubitemid 41282795)
44. L Mathiasen NR Mirza 2005 A comparison of chlordiazepoxide, bretazenil, L838, 417 and zolpidem in a validated mouse Vogel conflict test Psychopharmacology (Berlin) 182 4 475 484 10.1007/s00213-005-0119-z (Pubitemid 41464628)
45. TA Mellman V Bustamante D David AI Fins 2002 Hypnotic medication in the aftermath of trauma J Clin Psychiatry 63 12 1183 1184 12530420
46. KR Merikangas NC Low 2005 Genetic epidemiology of anxiety disorders Handb Exp Pharmacol 169 163 179 16594258 10.1007/3-540-28082-0-6
47. KM Myers M Davis 2002 Behavioral and neural analysis of extinction Neuron 36 4 567 584 12441048 10.1016/S0896-6273(02)01064-4 (Pubitemid 35346753)
48. T Nagatani T Yamamoto 1991 Antagonism by propyl-beta-carboline-3- carboxylate of passive avoidance impairment induced by diazepam Eur J Pharmacol 198 1 109 112 1915575 10.1016/0014-2999(91)90571-7
49. H Oishi S Iwahara KM Yang A Yogi 1972 Effects of chlordiazepoxide on passive avoidance responses in rats Psychopharmacologia 23 4 375 385 5025579 10.1007/BF00406740
50. JB Patel VB Ciofalo LC Iorio 1979 Benzodiazepine blockade of passive-avoidance task in mice: a state-dependent phenomenon Psychopharmacology (Berlin) 61 1 25 28 10.1007/BF00426805 (Pubitemid 9212583)
51. EA Phelps MR Delgado KI Nearing JE LeDoux 2004 Extinction learning in humans: role of the amygdala and vmPFC Neuron 43 6 897 905 15363399 10.1016/j.neuron.2004.08.042 (Pubitemid 39215019)
52. L Prut C Belzung 2003 The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review Eur J Pharmacol 463 1-3 3 33 12600700 10.1016/S0014-2999(03)01272-X (Pubitemid 36205070)
53. L Ramirez-Lugo S Zavala-Vega F Bermudez-Rattoni 2006 NMDA and muscarinic receptors of the nucleus accumbens have differential effects on taste memory formation Learn Mem 13 1 45 51 16452653 10.1101/lm.103206 (Pubitemid 43200818)
54. V Rau JP DeCola MS Fanselow 2005 Stress-induced enhancement of fear learning: an animal model of posttraumatic stress disorder Neurosci Biobehav Rev 29 8 1207 1223 16095698 10.1016/j.neubiorev.2005.04.010 (Pubitemid 41446896)
55. S Reilly MA Bornovalova 2005 Conditioned taste aversion and amygdala lesions in the rat: a critical review Neurosci Biobehav Rev 29 7 1067 1088 15893375 10.1016/j.neubiorev.2005.03.025 (Pubitemid 41242781)
56. RA Rescorla 1996 Preservation of pavlovian associations through extinction The Q J Exp Psychol 49 245
57. KJ Ressler BO Rothbaum L Tannenbaum P Anderson K Graap E Zimand L Hodges M Davis 2004 Cognitive enhancers as adjuncts to psychotherapy: use of d-cycloserine in phobic individuals to facilitate extinction of fear Arch Gen Psychiatry 61 11 1136 1144 15520361 10.1001/archpsyc.61.11.1136 (Pubitemid 39463415)
58. K Rickels R Downing E Schweizer H Hassman 1993 Antidepressants for the treatment of generalized anxiety disorder. A placebo-controlled comparison of imipramine, trazodone, and diazepam Arch Gen Psychiatry 50 11 884 895 8215814
59. N Ripoll BA Nic Dhonnchadha V Sebille M Bourin M Hascoet 2005 The four-plates test-retest paradigm to discriminate anxiolytic effects Psychopharmacology (Berlin) 180 1 73 83 10.1007/s00213-004-2130-1 (Pubitemid 40897073)
60. HA Robertson 1979 Benzodiazepine receptors in "emotional" and "non-emotional" mice; comparison of four strains Eur J Pharmacol 56 1-2 163 166 572777 10.1016/0014-2999(79)90447-3 (Pubitemid 9180912)
61. DJ Sanger D Joly 1985 Anxiolytic drugs and the acquisition of conditioned fear in mice Psychopharmacology (Berlin) 85 3 284 288 10.1007/BF00428188 (Pubitemid 15123100)
62. JC Scaife RW Langley CM Bradshaw E Szabadi 2005 Diazepam suppresses the acquisition but not the expression of 'fear-potentiation' of the acoustic startle response in man J Psychopharmacol 19 4 347 356 15982989 10.1177/0269881105053285 (Pubitemid 41003130)
63. JC Scaife RH Hou ER Samuels F Baqui RW Langley CM Bradshaw E Szabadi 2007 Diazepam-induced disruption of classically-conditioned fear-potentiation of late-latency auditory evoked potentials is prevented by flumazenil given before, but not after, CS/US pairing J Psychopharmacol 21 1 93 101 16533870 10.1177/0269881106063130 (Pubitemid 46012088)
64. A Siegmund CT Wotjak 2006 Toward an animal model of posttraumatic stress disorder Ann N Y Acad Sci 1071 324 334 16891581 10.1196/annals.1364.025 (Pubitemid 44126739)
65. F Sotres-Bayon CK Cain JE LeDoux 2006 Brain mechanisms of fear extinction: historical perspectives on the contribution of prefrontal cortex Biol Psychiatry 60 4 329 336 16412988 10.1016/j.biopsych.2005.10.012 (Pubitemid 44215846)
66. 1A receptor agonists, partial agonists and a silent antagonist on the performance of the conditioned emotional response test in the rat Psychopharmacology (Berlin) 128 3 293 303 10.1007/s002130050137 (Pubitemid 26403125)
67. L Stein BD Berger 1969 Paradoxical fear-increasing effects of tranquilizers: evidence of repression of memory in the rat Science 166 902 253 256 5817764 10.1126/science.166.3902.253
68. ME Stone BS Grimes DB Katz 2005 Hippocampal inactivation enhances taste learning Learn Mem 12 6 579 586 16322360 10.1101/lm.32305 (Pubitemid 41770081)
69. GM Sullivan J Apergis DE Bush LR Johnson M Hou JE Ledoux 2004 Lesions in the bed nucleus of the stria terminalis disrupt corticosterone and freezing responses elicited by a contextual but not by a specific cue-conditioned fear stimulus Neuroscience 128 1 7 14 15450349 10.1016/j.neuroscience.2004.06.015 (Pubitemid 39140675)
70. G Villarreal DA Hamilton H Petropoulos I Driscoll LM Rowland JA Griego PW Kodituwakku BL Hart R Escalona WM Brooks 2002 Reduced hippocampal volume and total white matter volume in posttraumatic stress disorder Biol Psychiatry 52 2 119 125 12114003 10.1016/S0006-3223(02)01359-8 (Pubitemid 34756557)
71. H Welzl P D'Adamo HP Lipp 2001 Conditioned taste aversion as a learning and memory paradigm Behav Brain Res 125 1-2 205 213 11682112 10.1016/S0166-4328(01)00302-3 (Pubitemid 33000459)
72. A Wigger MM Sanchez KC Mathys K Ebner E Frank D Liu A Kresse ID Neumann F Holsboer PM Plotsky R Landgraf 2004 Alterations in central neuropeptide expression, release, and receptor binding in rats bred for high anxiety: critical role of vasopressin Neuropsychopharmacology 29 1 1 14 12942143 10.1038/sj.npp.1300290 (Pubitemid 38068008)
73. EL Wignall JM Dickson P Vaughan TF Farrow ID Wilkinson MD Hunter PW Woodruff 2004 Smaller hippocampal volume in patients with recent-onset posttraumatic stress disorder Biol Psychiatry 56 11 832 836 15576059 10.1016/j.biopsych.2004.09.015 (Pubitemid 39575456)
74. T Yamamoto 2007 Brain regions responsible for the expression of conditioned taste aversion in rats Chem Senses 32 1 105 109 17110526 10.1093/chemse/bjj045 (Pubitemid 46017880)
75. T Yamamoto Y Fujimoto 1991 Brain mechanisms of taste aversion learning in the rat Brain Res Bull 27 3-4 403 406 1683599 10.1016/0361-9230(91)90133-5
76. T Yamamoto T Shimura N Sako Y Yasoshima N Sakai 1994 Neural substrates for conditioned taste aversion in the rat Behav Brain Res 65 2 123 137 7718144 10.1016/0166-4328(94)90097-3