Use of the light/dark test for anxiety in adult and adolescent male rats

Behavioural Brain Research

Volumn 256, Issue , 2013, Pages 119-127

  Arrant, Andrew E ^a   Schramm Sapyta, Nicole L ^a   Kuhn, Cynthia M ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Adolescence; Anxiety; Factor analysis; FG 7142; Light dark test; Yohimbine

Indexed keywords

N METHYL BETA CARBOLINE 3 CARBOXAMIDE; YOHIMBINE; ALPHA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; ANTIDEPRESSANT AGENT; CARBOLINE DERIVATIVE;

ADOLESCENT; ADULT ANIMAL; AGE; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; EXPERIMENTAL TEST; EXPLORATORY BEHAVIOR; FACTORIAL ANALYSIS; GABAERGIC SYSTEM; LIGHT DARK TEST; LOCOMOTION; MALE; MULTIPLE REGRESSION; NEUROMODULATION; NONHUMAN; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; RAT; ANIMAL; DIAGNOSIS; DRUG EFFECTS; DRUG THERAPY; HIGH RISK BEHAVIOR; LIGHT; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TEST; REGRESSION ANALYSIS; SPRAGUE DAWLEY RAT; TIME;

ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; AGE FACTORS; ANIMALS; ANTIDEPRESSIVE AGENTS; ANXIETY; CARBOLINES; EXPLORATORY BEHAVIOR; FACTOR ANALYSIS, STATISTICAL; LIGHT; MALE; MOTOR ACTIVITY; NEUROPSYCHOLOGICAL TESTS; RATS, SPRAGUE-DAWLEY; REGRESSION ANALYSIS; RISK-TAKING; TIME FACTORS; YOHIMBINE;

EID: 84882995229     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.05.035     Document Type: Article

References (72)

1. Crawley J.N. Exploratory behavior models of anxiety in mice. Neuroscience & Biobehavioral Reviews 1985, 9:37-44.
2. Crawley J., Goodwin F.K. Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacology Biochemistry and Behavior 1980, 13:167-170.
3. Crawley J.N. Neuropharmacologic specificity of a simple animal model for the behavioral actions of benzodiazepines. Pharmacology Biochemistry and Behavior 1981, 15:695-699.
4. Bourin M., Hascoet M. The mouse light/dark box test. European Journal of Pharmacology 2003, 463:55-65.
5. Costall B., Jones B.J., Kelly M.E., Naylor R.J., Tomkins D.M. Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacology Biochemistry and Behavior 1989, 32:777-785.
6. Young R., Johnson D.N. A fully automated light/dark apparatus useful for comparing anxiolytic agents. Pharmacology Biochemistry and Behavior 1991, 40:739-743.
7. Milner L.C., Crabbe J.C. Three murine anxiety models: results from multiple inbred strain comparisons. Genes, Brain and Behavior 2008, 7:496-505.
8. Bill D.J., Fletcher A., Glenn B.D., Knight M. Behavioural studies on WAY100289, a novel 5-HT3 receptor antagonist, in two animal models of anxiety. European Journal of Pharmacology 1992, 218:327-334.
9. Merlo Pich E., Samanin R. A two-compartment exploratory model to study anxiolytic/anxiogenic effects of drugs in the rat. Pharmacological Research 1989, 21:595-602.
10. Chaouloff F., Durand M., Mormede P. Anxiety- and activity-related effects of diazepam and chlordiazepoxide in the rat light/dark and dark/light tests. Behavioural Brain Research 1997, 85:27-35.
11. Steinberg L. A social neuroscience perspective on adolescent risk-taking. The Development Review 2008, 28:78-106.
12. Eaton D.K., Kann L., Kinchen S., Shanklin S., Flint K.H., Hawkins J., et al. Youth risk behavior surveillance - United States, 2011. MMWR - MMWR Publications - Surveillance Summaries 2012, 61:1-162.
13. Ernst M., Pine D.S., Hardin M. Triadic model of the neurobiology of motivated behavior in adolescence. Psychological Medicine 2006, 36:299-312.
14. Vasa R.A., Pine D.S., Thorn J.M., Nelson T.E., Spinelli S., Nelson E., et al. Enhanced right amygdala activity in adolescents during encoding of positively valenced pictures. Developmental Cognitive Neuroscience 2011, 1:88-99.
15. Harro J. Long-term partial 5-HT depletion: interference of anxiety and impulsivity?. Psychopharmacology 2002, 164:433-434.
16. Macri S., Adriani A., Chiarotti F., Laviola G. Risk taking during exploration of a plus-maze is greater in adolescent than in juvenile or adult mice. Animal Behavior 2002, 64:541-546.
17. Olausson P., Engel J.A., Soderpalm B. Behavioral sensitization to nicotine is associated with behavioral disinhibition; counteraction by citalopram. Psychopharmacology (Berl) 1999, 142:111-119.
18. Hascoet M., Colombel M.C., Bourin M. Influence of age on behavioural response in the light/dark paradigm. Physiology & Behavior 1999, 66:567-570.
19. Slawecki C.J. Comparison of anxiety-like behavior in adolescent and adult Sprague-Dawley rats. Behavioral Neuroscience 2005, 119:1477-1483.
20. Schramm-Sapyta N.L., Cha Y.M., Chaudhry S., Wilson W.A., Swartzwelder H.S., Kuhn C.M. Differential anxiogenic, aversive, and locomotor effects of THC in adolescent and adult rats. Psychopharmacology (Berl) 2007, 191:867-877.
21. Arrant A.E., Jemal H., Kuhn C.M. Adolescent male rats are less sensitive than adults to the anxiogenic and serotonin-releasing effects of fenfluramine. Neuropharmacology 2013, 65:213-222.
22. Primus R.J., Kellogg C.K. Pubertal-related changes influence the development of environment-related social interaction in the male rat. Developmental Psychobiology 1989, 22:633-643.
23. Andrade M.M., Tome M.F., Santiago E.S., Lucia-Santos A., de Andrade T.G. Longitudinal study of daily variation of rats' behavior in the elevated plus-maze. Physiology & Behavior 2003, 78:125-133.
24. Imhof J.T., Coelho Z.M., Schmitt M.L., Morato G.S., Carobrez A.P. Influence of gender and age on performance of rats in the elevated plus maze apparatus. Behavioural Brain Research 1993, 56:177-180.
25. Doremus T.L., Varlinskaya E.I., Spear L.P. Age-related differences in elevated plus maze behavior between adolescent and adult rats. Annals of the New York Academy of Sciences 2004, 1021:427-430.
26. Adriani W., Chiarotti F., Laviola G. Elevated novelty seeking and peculiar d-amphetamine sensitization in periadolescent mice compared with adult mice. Behavioral Neuroscience 1998, 112:1152-1166.
27. Douglas L.A., Varlinskaya E.I., Spear L.P. Novel-object place conditioning in adolescent and adult male and female rats: effects of social isolation. Physiology & Behavior 2003, 80:317-325.
28. Stansfield K.H., Kirstein C.L. Effects of novelty on behavior in the adolescent and adult rat. Developmental Psychobiology 2006, 48:10-15.
29. Schramm-Sapyta N.L., Cauley M.C., Stangl D.K., Glowacz S., Stepp K.A., Levin E.D., et al. Role of individual and developmental differences in voluntary cocaine intake in rats. Psychopharmacology (Berl) 2011, 215:493-504.
30. Fernandes C., Gonzalez M.I., Wilson C.A., File S.E. Factor analysis shows that female rat behaviour is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacology Biochemistry and Behavior 1999, 64:731-738.
31. Doremus T.L., Varlinskaya E.I., Spear L.P. Factor analysis of elevated plus-maze behavior in adolescent and adult rats. Pharmacology Biochemistry and Behavior 2006, 83:570-577.
32. Ramos A., Berton O., Mormede P., Chaouloff F. A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behavioural Brain Research 1997, 85:57-69.
33. Ramos A. Animal models of anxiety: do I need multiple tests. Trends in Pharmacological Sciences 2008, 29:493-498.
34. Fraser L.M., Brown R.E., Hussin A., Fontana M., Whittaker A., O'Leary T.P., et al. Measuring anxiety- and locomotion-related behaviours in mice: a new way of using old tests. Psychopharmacology (Berl) 2010, 211:99-112.
35. Caster J.M., Walker Q.D., Kuhn C.M. Enhanced behavioral response to repeated-dose cocaine in adolescent rats. Psychopharmacology (Berl) 2005, 183:218-225.
36. Parylak S.L., Caster J.M., Walker Q.D., Kuhn C.M. Gonadal steroids mediate the opposite changes in cocaine-induced locomotion across adolescence in male and female rats. Pharmacology Biochemistry and Behavior 2008, 89:314-323.
37. Van Swearingen A.E., Walker Q.D., Kuhn C.M. Sex differences in novelty- and psychostimulant-induced behaviors of C57BL/6 mice. Psychopharmacology (Berl) 2013, 225:707-718.
38. File S.E., Baldwin H.A. Effects of beta-carbolines in animal models of anxiety. Brain Research Bulletin 1987, 19:293-299.
39. Pellow S., File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacology Biochemistry and Behavior 1986, 24:525-529.
40. Belzung C., Le Pape G. Comparison of different behavioral test situations used in psychopharmacology for measurement of anxiety. Physiology & Behavior 1994, 56:623-628.
41. File S.E., Lippa A.S., Beer B., Lippa M.T. Animal tests of anxiety. Current Protocols in Neuroscience 2004, Chapter 8:Unit 8 3.
42. Cruz A.P., Frei F., Graeff F.G. Ethopharmacological analysis of rat behavior on the elevated plus-maze. Pharmacology Biochemistry and Behavior 1994, 49:171-176.
43. Rodgers R.J., Johnson N.J. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacology Biochemistry and Behavior 1995, 52:297-303.
44. Casey B.J., Jones R.M., Hare T.A. The adolescent brain. Annals of the New York Academy of Sciences 2008, 1124:111-126.
45. Gray J.A., McNaughton N. The Neuropsychology of Anxiety: An Enquiry into the Functions of the Septo-hippocampal System 2000, Oxford University Press, Oxford/New York. 2nd ed.
46. Handley S.L., McBlane J.W., Critchley M.A., Njung'e K. Multiple serotonin mechanisms in animal models of anxiety: environmental, emotional and cognitive factors. Behavioural Brain Research 1993, 58:203-210.
47. Jaskiw G.E., Lipska B.K., Weinberger D.R. The anxiogenic beta-carboline FG-7142 inhibits locomotor exploration similarly in postweanling and adult rats. Neuroscience Letters 2003, 346:5-8.
48. Candy J.M., Martin I.L. The postnatal development of the benzodiazepine receptor in the cerebral cortex and cerebellum of the rat. Journal of Neurochemistry 1979, 32:655-658.
49. Palacios J.M., Niehoff D.L., Kuhar M.J. Ontogeny of GABA and benzodiazepine receptors: effects of Triton X-100, bromide and muscimol. Brain Research 1979, 179:390-395.
50. Lippa A.S., Beer B., Sano M.C., Vogel R.A., Meyerson L.R. Differential ontogeny of type 1 and type 2 benzodiazepine receptors. Life Sciences 1981, 28:2343-2347.
51. Fritschy J.M., Paysan J., Enna A., Mohler H. Switch in the expression of rat GABAA-receptor subtypes during postnatal development: an immunohistochemical study. The Journal of Neuroscience 1994, 14:5302-5324.
52. Primus R.J., Kellogg C.K. Gonadal status and pubertal age influence the responsiveness of the benzodiazepine/GABA receptor complex to environmental challenge in male rats. Brain Research 1991, 561:299-306.
53. Graeff F.G., Viana M.B., Mora P.O. Opposed regulation by dorsal raphe nucleus 5-HT pathways of two types of fear in the elevated T-maze. Pharmacology Biochemistry and Behavior 1996, 53:171-177.
54. Evans A.K., Abrams J.K., Bouwknecht J.A., Knight D.M., Shekhar A., Lowry C.A. The anxiogenic drug FG-7142 increases serotonin metabolism in the rat medial prefrontal cortex. Pharmacology Biochemistry and Behavior 2006, 84:266-274.
55. Hackler E.A., Turner G.H., Gresch P.J., Sengupta S., Deutch A.Y., Avison M.J., et al. 5-Hydroxytryptamine2C receptor contribution to m-chlorophenylpiperazine and N-methyl-beta-carboline-3-carboxamide-induced anxiety-like behavior and limbic brain activation. Journal of Pharmacology and Experimental Therapeutics 2007, 320:1023-1029.
56. Murrin L.C., Sanders J.D., Bylund D.B. Comparison of the maturation of the adrenergic and serotonergic neurotransmitter systems in the brain: implications for differential drug effects on juveniles and adults. Biochemical Pharmacology 2007, 73:1225-1236.
57. Abercrombie E.D., Keller R.W., Zigmond M.J. Characterization of hippocampal norepinephrine release as measured by microdialysis perfusion: pharmacological and behavioral studies. Neuroscience 1988, 27:897-904.
58. Kehne J.H., Davis M. Central noradrenergic involvement in yohimbine excitation of acoustic startle: effects of DSP4 and 6-OHDA. Brain Research 1985, 330:31-41.
59. Fontana D.J., Commissaris R.L. Anxiolytic-like effects of alpha-2-adrenoceptor agonists on conflict behavior in the rat: pre- versus postsynaptic receptor mechanisms. Pharmacology Biochemistry and Behavior 1992, 43:697-704.
60. Happe H.K., Coulter C.L., Gerety M.E., Sanders J.D., O'Rourke M., Bylund D.B., et al. Alpha-2 adrenergic receptor development in rat CNS: an autoradiographic study. Neuroscience 2004, 123:167-178.
61. Infurna R.N., Spear L.P. Developmental changes in amphetamine-induced taste aversions. Pharmacology Biochemistry and Behavior 1979, 11:31-35.
62. Schramm-Sapyta N.L., Morris R.W., Kuhn C.M. Adolescent rats are protected from the conditioned aversive properties of cocaine and lithium chloride. Pharmacology Biochemistry and Behavior 2006, 84:344-352.
63. Shram M.J., Funk D., Li Z., Le A.D. Periadolescent and adult rats respond differently in tests measuring the rewarding and aversive effects of nicotine. Psychopharmacology (Berl) 2006, 186:201-208.
64. Wilmouth C.E., Spear L.P. Adolescent and adult rats' aversion to flavors previously paired with nicotine. Annals of the New York Academy of Sciences 2004, 1021:462-464.
65. Philpot R.M., Badanich K.A., Kirstein C.L. Place conditioning: age-related changes in the rewarding and aversive effects of alcohol. Alcoholism: Clinical and Experimental Research 2003, 27:593-599.
66. Anderson R.I., Varlinskaya E.I., Spear L.P. Ethanol-induced conditioned taste aversion in male sprague-dawley rats: impact of age and stress. Alcoholism: Clinical and Experimental Research 2010, 34:2106-2115.
67. Schramm-Sapyta N.L., DiFeliceantonio A.G., Foscue E., Glowacz S., Haseeb N., Wang N., et al. Aversive effects of ethanol in adolescent versus adult rats: potential causes and implication for future drinking. Alcoholism: Clinical and Experimental Research 2010, 34:2061-2069.
68. Holstein S.E., Spanos M., Hodge C.W. Adolescent C57BL/6J mice show elevated alcohol intake, but reduced taste aversion, as compared to adult mice: a potential behavioral mechanism for binge drinking. Alcoholism: Clinical and Experimental Research 2011, 35:1842-1851.
69. Doremus T.L., Brunell S.C., Varlinskaya E.I., Spear L.P. Anxiogenic effects during withdrawal from acute ethanol in adolescent and adult rats. Pharmacology Biochemistry and Behavior 2003, 75:411-418.
70. Pattwell S.S., Bath K.G., Casey B.J., Ninan I., Lee F.S. Selective early-acquired fear memories undergo temporary suppression during adolescence. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:1182-1187.
71. Rewards Spear L.P. aversions and affect in adolescence: emerging convergences across laboratory animal and human data. Developmental Cognitive Neuroscience 2011, 1:390-403.
72. Chambers R.A., Taylor J.R., Potenza M.N. Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. American Journal of Psychiatry 2003, 160:1041-1052.