Determination of motor activity and anxiety-related behaviour in rodents: Methodological aspects and role of nitric oxide

Interdisciplinary Toxicology

Volumn 6, Issue 3, 2013, Pages 126-135

  Sestakova, Natalia ^a   Puzserova, Angelika ^a   Kluknavsky, Michal ^a   Bernatova, Iveta ^a  

^a INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

anxiety; black and white box; elevated plus maze; nitric oxide; open field; zero maze

Indexed keywords

N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ANXIETY; DECISION MAKING; ELEVATED PLUS MAZE TEST; EMOTIONALITY; EPIGENETICS; EXPLORATORY BEHAVIOR; ILLUMINATION; LOCOMOTION; MAZE TEST; MODULATION; MOTOR ACTIVITY; NONHUMAN; OPEN FIELD TEST; REVIEW; RISK ASSESSMENT;

EID: 84897919848     PISSN: 13376853     EISSN: 13379569     Source Type: Journal    
DOI: 10.2478/intox-2013-0020     Document Type: Review

References (113)

1. Al-Rahbi B, Zakaria R, Othman Z, Hassan A, Muthuraju S and Wan Mohammad WM. (2013). Mood and memory function in ovariectomised rats exposed to social instability stress. Biomed Res Int 2013: Article ID 493643, 10 pages, doi: 10.1155/2013/493643.
2. Archer J. (1973). Test for emotionality in rats and mice: a review. Anim Behav 21: 205-235.
3. Bernatova I, Puzserova A and Dubovicky M. (2010). Sex differences in social stress-induced pressor and behavioral responses in normotensive and prehypertensive rats. Gen Physiol Biophys 29: 346-354.
4. Bernatova I, Puzserova A, Sestakova N and Mach M. (2011). Horiziontal motor activity of hypertensive rats is associated with level of blood pressure. Acta Physiologica: official journal of the Federation of European Physiological Societies. 202, suppl. 685: 84, abstract.
5. Berton O, Ramos A, Chaouloff F and Morméde P. (1997). Behavioral reactivity to social and nonsocial stimulations: a multivariate analysis of six inbred rat strains. Behav Genet 27: 155-166. (Pubitemid 27203931)
6. Bond NW and Di Giusto EL. (1977). Prenatal alcohol consumption and openfield behaviour in rats: effects of age at time of testing. Psychopharmacology (Berl) 52: 311-312. (Pubitemid 8097259)
7. Braun AA, Skelton MR, Vorhees CV and Williams MT. (2011). Comparison of the elevated plus and elevated zero mazes in treated and untreated male Sprague-Dawley rats: effects of anxiolytic and anxiogenic agents. Pharmacol Biochem Behav 97: 406-415.
8. Broadhurst PL. (1969). Psychogenetics of emotionality in the rat. Ann N Y Acad Sci 159: 806-824.
9. Carnevali L, Mastorci F, Graiani G, Razzoli M, Trombini M, Pico-Alfonso MA, Arban R, Grippo AJ, Quaini F and Sgoifo A. (2012). Social defeat and isolation induce clear signs of a depression-like state, but modest cardiac alterations in wild-type rats. Physiol Behav 106: 142-150.
10. Cleck JN, Ecke LE and Blendy JA. (2008). Endocrine and gene expression changes following forced swim stress exposure during cocaine abstinence in mice. Psychopharmacology (Berl) 201: 15-28.
11. Clément Y, Calatayud F and Belzung C. (2002). Genetic basis of anxiety-like behaviour: a critical review. Brain Res Bull 57: 57-71. (Pubitemid 34097771)
12. Cook MN, Crounse M and Flaherty L. (2002). Anxiety in the elevated zeromaze is augmented in mice after repeated daily exposure. Behav Genet 32: 113-118. (Pubitemid 34522419)
13. Costall B, Jones BJ, Kelly ME, Naylor RJ and Tomkins DM. (1989). Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol Biochem Behav 32: 777-785. (Pubitemid 19162403)
14. Crawley J and Goodwin FK. (1980). Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13: 167-170. (Pubitemid 11225713)
15. Crawley JN. (1981). Neuropharmacologic specificity of a simple animal model for the behavioral actions of benzodiazepines. Pharmacol Biochem Behav 15: 695-699. (Pubitemid 12195249)
16. Czech DA, Jacobson EB, LeSueur-Reed KT and Kazel MR. (2003). Putative anxiety-linked effects of the nitric oxide synthase inhibitor L-NAME in three murine exploratory behavior models. Pharmacol Biochem Behav 75: 741-748. (Pubitemid 37289458)
17. da Silva GL, Matteussi AS, dos Santos ARS, Calixto JB and Rodrigues ALS. (2000). Evidence for dual effects of nitric oxide in the forced swimming test and in the tail suspension test in mice. Cognitive Neurosci Neuropsychol 11: 3699-3702.
18. Darnaudéry M and Maccari S. (2008). Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev 57: 571-585.
19. Davis MJ, Duvoisin RM and Raber J. (2013). Related functions of mGlu4 and mGlu8. Pharmacol Biochem Behav. in press.
20. De Oliveira CL, Del Bel EA and Guimarǎes FS. (1997). Effects of L-NOARG on plus-maze performance in rats. Pharmacol Biochem Behav 56: 55-59. (Pubitemid 27016105)
21. Del Bel EA, da Silva CA, Guimaraes FS and Bermúdez-Echeverry M. (2004). Catalepsy induced by intra-striatal administration of nitric oxide synthase inhibitors in rats. Eur J Pharmacol 485: 175-181. (Pubitemid 38134412)
22. Del Bel EA, Souza AS, Guimaraes FS, da Silva CA and Nucci-da-Silva LP. (2002). Motor effects of acute and chronic inhibition of nitric oxide synthesis in mice. Psychopharmacology (Berl) 161: 32-37.
23. Domeney A and Feldon J. (1998). The disruption of prepulse inhibition by social isolation in the Wistar rat: how robust is the effect? Pharmacol Biochem Behav 59: 883-890. (Pubitemid 28237899)
24. Dubovicky M and Jezova D. (2004). Effect of chronic emotional stress on habituation processes in open field in adult rats. Ann NY Acad Sci 1018: 199-206. (Pubitemid 38951407)
25. Dubovicky M, Paton S, Morris M, Mach M and Lucot JB. (2007). Effects of combined exposure to pyridostigmine bromide and shaker stress on acoustic startle response, pre-pulse inhibition and open field behavior in mice. J Appl Toxicol 27: 276-283. (Pubitemid 46663422)
26. Dubovicky M, Skultetyova I and Jezova D. (1999). Neonatal stress alters habituation of exploratory behavior in adult male but not female rats. Pharmacol Biochem Behav 64: 681-686.
27. Ducottet C and Belzung C. (2005). Correlations between behaviours in the elevated plus-maze and sensitivity to unpredictable subchronic mild stress: evidence from inbred strains of mice. Behav Brain Res 156: 153-162. (Pubitemid 39330445)
28. Effect of long-term caffeine administration on depressive-like behavior in rats exposed to chronic unpredictable stress. Behav Pharmacol 23: 339-347.
29. Echeverry MB, Salgado ML, Ferreira FR, da-Silva CA and Del Bel EA. (2007). Intracerebroventricular administration of nitric oxide-sensitive guanylyl cyclase inhibitors induces catalepsy in mice. Psychopharmacology (Berl) 194: 271-278. (Pubitemid 47457950)
30. Fan SJ, Jiang H, Yang LJ, Liu X, Song J and Pan F. (2011). Effects of adrenergic agents on stress-induced brain microstructural and immunochemical changes in adult male Wistar rats. Ann Anat 193: 418-424.
31. Faria MS, Muscara MN, Moreno JH, Teixeira SA, Dias HB, De Oliveira B, Graeff FG and De Nucci G. (1997). Acute inhibition of nitric oxide synthesis induces anxiolysis in the plus maze test. Eur J Pharmacol 323: 37-43. (Pubitemid 27136435)
32. File SE. (1993). The interplay of learning and anxiety in the elevated plusmaze. Behav Brain Res 58: 199-202. (Pubitemid 24024058)
33. Francis D, Diorio J, Liu D and Meaney MJ. (1999). Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286: 1155-1158.
34. Gentsch C, Lichtsteiner M and Feer H. (1987). Open field and elevated plusmaze: a behavioural comparison between spontaneously hypertensive (SHR) and Wistar-Kyoto rats and the effects of chlordiazepoxide. Behav Brain Res. 25: 101-107. (Pubitemid 17137690)
35. Gouveia K and Hurst JL. (2013). Reducing mouse anxiety during handling: Effect of experience with handling tunnels. PLoS One. 8(6): e66401. doi: 10.1371/journal.pone.0066401.
36. Halcak L, Pechanova O, Zigova Z, Klemova L, Novacky M and Bernatova I. (2000). Inhibition of NO synthase activity in nervous tissue leads to decreased motor activity in the rat. Physiol Res 49: 143-149. (Pubitemid 30111308)
37. Hall CS and Ballachey EL. (1932). A study of the rat's behavior in a field: a contribution to methods in comparative psychology. University of California Publications in Psychology 6: 1-12.
38. Hall CS. (1934). Emotional behavior in the rat. I., Defecation and urination as measures of individual differences in emotionality. J Comp Psychol 18: 385-403.
39. Handley SL and McBlane JW. (1993). An assessment of the elevated X-maze for studying anxiety and anxiety-modulating drugs. J Pharmacol Toxicol Meth 29: 129-138. (Pubitemid 23193181)
40. Heisler LK, Chu HM, Brennan TJ, Danao JA, Bajwa P, Parsons LH and 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)
41. Henniger MSH, Ohl F, Hölter SM, Weiâenbacher P, Toschi N, Lörscher P Wigger A, Spanagel R and Landgraf R. (2000). Unconditioned anxiety and social behaviour in two rat lines selectively bred for high and low anxietyrelated behaviour. Behav Brain Res 111: 153-163. (Pubitemid 30326711)
42. Heredia L, Torrente M, Domingo JL and Colomina MT. (2012). Individual housing and handling procedures modify anxiety levels of Tg2576 mice assessed in the zero maze test. Physiol Behav 107: 187-191.
43. Hölscher C, McGlinchey L, Anwyl R and Rowan MJ. (1996). 7-Nitro indazole, a selective neuronal nitric oxide synthase inhibitor in vivo, impairs spatial learning in the rat. Learn Mem 2: 267-278. (Pubitemid 126683043)
44. Chakraborti A, Gulati K and Ray A. (2008). Age related differences in stress-induced neurobehavioral responses in rats: modulation by antioxidants and nitrergic agents. Behav Brain Res 194: 86-91.
45. Chaouloff F, Kulikov A, Sarrieau A, Castanon N and Mormede P. (1995). Male Fischer 344 and Lewis rats display differences in locomotor reactivity, but not in anxiety-related behaviours: relationship with the hippocampal serotonergic system. Brain Res 693: 169-178.
46. Isogawa K, Akiyoshi J, Tsutsumi T, Kodama K, Horinouti Y and Nagayama H. (2003). Anxiogenic-like effect of corticotropin-releasing factor receptor 2 antisense oligonucleotides infused into rat brain. J Psychopharmacol 17: 409-413. (Pubitemid 38076336)
47. Johnston AL and File SE. (1991). Sex differences in animal tests of anxiety. Physiol Behav 49: 245-250.
48. Jones RB, Mills AD and Faure JM. (1991). Genetic and experiential manipulation of fear-related behavior in Japanese quail chicks (Coturnix coturnix japonica). J Comp Psychol. 105: 15-24.
49. Kirchner L, Weitzdoerfer R, Hoeger H, Url A, Schmidt P, Engelmann M, Villar SR, Fountoulakis M, Lubec G and Lubec B. (2004). Impaired cognitive performance in neuronal nitric oxide synthase knockout mice is associated with hippocampal protein derangements. Nitric Oxide 11: 316-330. (Pubitemid 39626585)
50. Knardahl S and Sagvolden T. (1979). Open-field behavior of spontaneously hypertensive rats. Behav Neural Biol 27: 187-200. (Pubitemid 10192099)
51. Krishna S, Dodd CA, Hekmatyar SK and Filipov NM. (2013). Brain deposition and neurotoxicity of manganese in adult mice exposed via the drinking water. Arch Toxicol 88(1): 47-64.
52. Kulkarni SK, Singh K and Bishnoi M. (2007). Elevated zero maze: a paradigm to evaluate antianxiety effects of drugs. Methods Find Exp Clin Pharmacol 29: 343-348. (Pubitemid 47344816)
53. Lazzarini M, Salum C and Del Bel EA. (2005). Combined treatment of ascorbic acid or alpha-tocopherol with dopamine receptor antagonist or nitric oxide synthase inhibitor potentiates cataleptic effect in mice. Psychopharmacology (Berl) 181: 71-79. (Pubitemid 41440917)
54. Leussis MP and Andersen SL. Is adolescence a sensitive period for depression? (2008). Behavioral and neuroanatomical findings from a social stress model. Synapse 62: 22-30.
55. Liebsch G, Montkowski A, Holsboer F and Landgraf R. (1998). Behavioural profiles of two Wistar rat lines selectively bred for high or low anxiety-related behaviour. Behav Brain Res 94: 301-310. (Pubitemid 28352829)
56. Lister RG. (1990). Ethologically-based animal models of anxiety disorders. Pharmacol Ther 46: 321-340. (Pubitemid 20108519)
57. Mach M, Grubbs RD, Price WA, Nagaoka M, Dubovicky M and Lucott JB. (2008). Delayed behavioral and endocrine effects of sarin and stress exposure in mice. J Appl Toxicol 28: 132-139. (Pubitemid 351428285)
58. Masood A, Banerjee B, Vijayan VK and Ray A. (2003). Modulation of stressinduced neurobehavioral changes by nitric oxide in rats. Eur J Pharmacol 458: 135-139. (Pubitemid 36050711)
59. Mällo T, Alttoa A, Köiv K, Tönissaar M, Eller M and Harro J. (2006). Rats with persistently low or high exploratory activity: behaviour in tests of anxiety and depression, and extracellular levels of dopamine. Behav Brain Res 177: 269-281. (Pubitemid 46149908)
60. McCormick CM, Robarts D, Kopeikina K and Kelsey JE. (2005). Long-lasting, sex-and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats. Horm Behav 48: 64-74. (Pubitemid 40779291)
61. McEwen BS (2000). Allostasis and allostatic load: implications for neuropsychopharmacology. Neuropsychopharmacol 22: 108-124. (Pubitemid 30016013)
62. Moberg GP, Anderson CO and Underwood TR. (1980). Ontogeny of the adrenal and behavioral responses of lambs to emotional stress. J Anim Sci 51: 138-142.
63. Montgomery KC. (1955). The relation between fear induced by novel stimulation and exploratory drive. J Compar Physiol Psychol 48: 254-260.
64. Monzón ME, Varas MM and De Barioglio SR. (2001). Anxiogenesis induced by nitric oxide synthase inhibition and anxiolytic effect of melanin-concentrating hormone (MCH) in rat brain. Peptides 22: 1043-1047. (Pubitemid 32614126)
65. Moore PK, Oluyomi AO, Babbedge RC, Wallace P and Hart SL. (1991). L-NGnitro arginine methyl ester exhibits antinociceptive activity in the mouse. Br J Pharmacol 102: 198-202.
66. Mormede P, García-Belenguer S, Dulluc J and Oliver C. (1994). Independent segregation of a hyperactive hypothalamic-hypophyso-adrenal axis and a reduced behavioural reactivity in pigs. Psychoneuroendocrinology 19: 305-311. (Pubitemid 24137800)
67. Mullens BA, Lii KS, Mao Y, Meyer JA, Peterson NG and Szijj CE. (2006). Behavioural responses of dairy cattle to the stable fly, Stomoxys calcitrans, in an open field environment. Med Vet Entomol 20: 122-137.
68. Pardon MC, Gould GG, Garcia A, Phillips L, Cook MC, Miller SA, Mason PA and Morilak DA. (2002). Stress reactivity of the brain noradrenergic system in three rat strains differing in their neuroendocrine and behavioral responses to stress: implications for susceptibility to stress-related neuropsychiatric disorders. Neuroscience 115: 229-242. (Pubitemid 35232702)
69. Parfitt DB, Walton JR, Corriveau EA and Helmreich DL. (2007). Early life stress effects on adult stress-induced corticosterone secretion and anxiety-like behavior in the C57BL/6 mouse are not as robust as initially thought. Horm Behav 52: 417-426. (Pubitemid 47489775)
70. Pechlivanova DM, Tchekalarova JD, Alova LH, Petkov VV, Nikolov RP and Yakimova KS. (2012). Effect of long-term caffeine administration on depressivelike behavior in rats exposed to chronic unpredictable stress. Behav Pharmacol 23(4): 339-347.
71. Pellow S, Chopin P, File SE and 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)
72. Prast H and Philippu A. (2001). Nitric oxide as modulator of neuronal function. Prog Neurobiol 64: 51-68. (Pubitemid 32201889)
73. Pritchard LM, Van Kempen TA and Zimmerberg B. (2013). Behavioral effects of repeated handling differ in rats reared in social isolation and environmental enrichment. Neurosci Lett 536: 47-51.
74. Ramos A and Mormede P. (1998). Stress and emotionality: a multidimensional and genetic approach. Neurosci Biobehav Rev 22: 33-57. (Pubitemid 28082283)
75. Ramos A, Berton O, Mormede P and Chaouloff F. (1997). A multiple-test study of anxiety-related behaviours in six inbred rat strains. Behav Brain Res 85: 57-69. (Pubitemid 27116150)
76. Ramos A, Correia EC, Izídio GS and Brüske GR. (2003). Genetic selection of two new rat lines displaying different levels of anxiety-related behaviors. Behav Genet 33: 657-668. (Pubitemid 37444398)
77. Ramos A, Moisan MP, Chaouloff F, Mormede C and Mormede P. (1999). Identification of female-specific QTLs affecting an emotionality-related behavior in rats. Mol Psychiatry 4: 453-462. (Pubitemid 29497733)
78. Rasmussen S, Miller MM, Filipski SB and Tolwani RJ. (2011). Cage change influences serum corticosterone and anxiety-like behaviors in the mouse. J Am Assoc Lab Anim Sci 50: 479-483.
79. Rex A, Voigt JP and Fink H. (1999). Behavioral and neurochemical differences between Fischer 344 and Harlan-Wistar rats raised identically. Behav Genet 29: 187-192. (Pubitemid 29500636)
80. Rodgers RJ and Cole JC. (1993). Influence of social isolation, gender, strain, and prior novelty on plus-maze behaviour in mice. Physiol Behavior 54: 729-736. (Pubitemid 23275757)
81. Rodgers RJ and Dalvi A. (1997). Anxiety, defence and the elevated plus-maze. Neurosci Biobehav Rev 21: 801-810. (Pubitemid 27524775)
82. Rodgers RJ, Cao BJ, Dalvi A and Holmes A. (1997). Animal models of anxiety: an ethological perspective. Braz J Med Biol Res 30: 289-304. (Pubitemid 127521025)
83. Salim S, Asghar M, Chugh G, Taneja M, Xia Z and Saha K. (2010). Oxidative stress: a potential recipe for anxiety, hypertension and insulin resistance. Brain Res 1359: 178-185.
84. Salomon S, Bejar C, Schorer-Apelbaum D and Weinstock M. (2011). Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats. J Neuroendocrinol 23: 118-128.
85. Sanchez C, Bergqvist PB, Brennum LT, Gupta S, Hogg S, Larsen A and Wiborg O. (2003). Escitalopram, the S-(+)-enantiomer of citalopram, is a selective serotonin reuptake inhibitor with potent effects in animal models predictive of antidepressant and anxiolytic activities. Psychopharmacology (Berl) 167: 353-362. (Pubitemid 36754236)
86. Sestakova N, Puzserova A, Balis P, Slezak P, Mach M and Bernatova I. (2011). Effect of blood pressure on exploratory behaviour of rats in the open field test. Kidney & Blood Pressure Res 35: 101, abstract
87. Shepherd JK, Grewal SS, Fletcher A, Bill DJ and Dourish CT. (1994). Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology (Berl) 116: 56-64. (Pubitemid 24279597)
88. Shum FWF, Ko SW, Lee YS, Kaang BK and Zhuo M. (2005). Genetic alteration of anxiety and stress-like behavior in mice lacking CaMKIV. Mol Pain 1: 22.
89. Schiller GD, Daws LC, Overstreet DH and Orbach J. (1991). Lack of anxiety in an animal model of depression with cholinergic supersensitivity. Brain Res Bull 26: 433-435.
90. Schmitt U and Hiemke C. (1998). Strain differences in open-field and elevated plus-maze behavior of rats without and with pretest handling. Pharmacol Biochem Behav 59: 807-811. (Pubitemid 28237890)
91. Schulz KM, Pearson JN, Neeley EW, Berger R, Leonard S, Adams CE and Stevens KE. (2011). Maternal stress during pregnancy causes sex-specific alterations in offspring memory performance, social interactions, indices of anxiety, and body mass. Physiol Behav 104: 340-347.
92. Spiacci A Jr, Kanamaru F, Guimarǎes FS and Oliveira RM. (2008). Nitric oxidemediated anxiolytic-like and antidepressant-like effects in animal models of anxiety and depression. Pharmacol Biochem Behav 88: 247-255. (Pubitemid 350119843)
93. Steinert JR, Chernova T and Forsythe ID. (2010). Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist 16: 435-452.
94. Suo L, Zhao L, Si J, Liu J, Zhu W, Chai B, Zhang Y, Feng J, Ding Z, Luo Y, Shi H, Shi J and Lu L. (2013). Predictable chronic mild stress in adolescence increases resilience in adulthood. Neuropsychopharmacol 38: 1387-1400.
95. Swiergiel AH and Dunn AJ. (2007). Effects of interleukin-1α and lipopolysaccharide on behavior of mice in the elevated plus-maze and open field tests. Pharmacol Biochem Behav. 86: 651-659. (Pubitemid 46829318)
96. Talarovicova A, Krskova L and Blazekova J. (2009). Testosterone enhancement during pregnancy influences the 2D: 4D ratio and open field motor activity of rat siblings in adulthood. Horm Behav 55: 235-239.
97. Thompson RF and Spencer WA. (1966). Habituation: A model phenomenon for the study of neuronal substrates of behavior. Psychol Rev 73: 16-43.
98. Treit D, Menard J and Royan C. (1993). Anxiogenic stimuli in the elevated plus-maze. Pharmacol Biochem Behav 44: 463-469.
99. Vale AL, Green S, Montgomery AM and Shafi S. (1998). The nitric oxide synthesis inhibitor L-NAME produces anxiogenic-like effects in the rat elevated plus-maze test but not in the social interaction test. J Psychopharmacol 12: 268-272. (Pubitemid 28548582)
100. Vallée M, Mayo W, Dellu F, Le Moal M, Simon H and Maccari S. (1997). Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J Neurosci 17: 2626-2636. (Pubitemid 27137428)
101. van Gaalen MM and Steckler T. (2000). Behavioural analysis of four mouse strains in an anxiety test battery. Behav Brain Res 115: 95-106.
102. Van Reeth O, Weibel L, Spiegel K, Leproult R, Dugovic C and Maccari S. (2000). Physiology of sleep (review)-Interactions between stress and sleep: from basic research to clinical situations. Sleep Med Rev 4: 201-219. (Pubitemid 30249496)
103. Vendruscolo LF, Terenina-Rigaldie E, Raba F, Ramos A, Takahashi RN and Mormede P. (2006). Evidence for a female-specific effect of a chromosome 4 locus on anxiety-related behaviors and ethanol drinking in rats. Genes Brain Behav 5: 441-450. (Pubitemid 44199564)
104. Verma P, Hellemans KGC, Choi FY, Yu W and Weinberg J. (2009). Circadian phase and sex effects on depressive/anxiety-like behaviors and HPA axis responses to acute stress. Physiol Behav 99: 276-285.
105. Volke V, Soosaar A, Ko{double acute}ks S, Bourin M, Männistö PT and Vasar E. (1997). 7-Nitroindazole, a nitric oxide synthase inhibitor, has anxiolytic-like properties in exploratory models of anxiety. Psychopharmacology (Berl) 131: 399-405. (Pubitemid 27348707)
106. Webster AB and Hurnik JF. (1989). Genetic assessment of the behavior of White Leghorn type pullets in an open field. Poult Sci 68: 335-343.
107. Weiss IC, Di Iorio L, Feldon J and Domeney AM. (2000). Strain differences in the isolation-induced effects on prepulse inhibition of the acoustic startle response and on locomotor activity. Behav Neurosci 114: 364-373. (Pubitemid 30488996)
108. Weiss IC, Pryce CR, Jongen-Re{ogonek}lo AL, Nanz-Bahr NI and Feldon J. (2004). Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 152: 279-295. (Pubitemid 38757899)
109. Weiss IC, Pryce CR, Jongen-Re{ogonek}lo AL, Nanz-Bahr NI and Feldon J. (2004). Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat. Behav Brain Res 152: 279-295. (Pubitemid 38757899)
110. Wigger A and Neumann ID. (1999). Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol Behav 66: 293-302. (Pubitemid 29206522)
111. Wilking JA, Hesterberg KG, Nguyen VH, Cyboron AP, Hua AY and Stitzel JA. (2012). Comparison of nicotine oral consumption and baseline anxiety measures in adolescent and adult C57BL/6J and C3H/Ibg mice. Behav Brain Res 233: 280-287.
112. Wultsch T, Chourbaji S, Fritzen S, Kittel S, Grünblatt E and Gerlach M. (2007). Behavioural and expressional phenotyping of nitric oxide synthase-I knockdown animals. J Neural Transm Suppl 72: 69-85.
113. Zuena AR, Mairesse J, Casolini P, Cinque C, Alemŕ GS, Morley-Fletcher S, Chiodi V, Spagnoli LG, Gradini R, Catalani A, Nicoletti F and Maccari S. (2008). Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS One 3(5): e2170. doi: 10.1371/journal. pone.0002170.