Models of anxiety: Responses of rats to novelty in an open space and an enclosed space

Behavioural Brain Research

Volumn 171, Issue 1, 2006, Pages 26-49

  Ennaceur, A ^a   Michalikova, S ^a,b   Chazot, P L ^c  

^a UNIVERSITY OF SUNDERLAND   (United Kingdom)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

^c DURHAM UNIVERSITY   (United Kingdom)

Author keywords

Anthropomorphism; Benzodiazepines; GABA; Genetic; Habituation; Mice; Neophobia; Validity

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AVOIDANCE BEHAVIOR; CONTROLLED STUDY; FEMALE; MALE; METHODOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SPACE; SPATIAL DISCRIMINATION; TIME;

ADAPTATION, PSYCHOLOGICAL; ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; ENVIRONMENT; EXPLORATORY BEHAVIOR; FEMALE; HOUSING, ANIMAL; MALE; MODELS, ANIMAL; MOTOR ACTIVITY; RATS; RATS, INBRED LEW; RATS, WISTAR; REACTION TIME; SEX FACTORS; SPECIES SPECIFICITY;

EID: 33646547605     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2006.03.016     Document Type: Article

References (193)

1. Adriani W., and Laviola G. Spontaneous novelty seeking and amphetamine-induced conditioning and sensitization in adult mice: evidence of dissociation as a function of age at weaning. Neuropsychopharmacology 27 (2002) 225-236
2. Aguilar R., Gil L., Gray J.A., Driscoll P., Flint J., Dawson G.R., et al. Fearfulness and sex in F2 Roman rats: males display more fear though both sex share the same fearfulness traits. Physiol Behav 78 (2003) 723-732
3. Albrechet-Souza L., Oliveira A.R., De Luca M.C.Z., Tomazini F.M., Santos N.R., and Brandão M.L. A comparative study with two types of elevated plus-maze (transparent versus opaque walls) on the anxiolytic effects of midazolam, one-trial tolerance and fear-induced analgesia. Progr Neuro-Psychopharmacol Biol Psychiat 29 (2005) 571-579
4. Amsel A. Hippocampal function in the rat: cognitive mapping or vicarious trial and error?. Hippocampus 3 3 (1993) 251-256
5. Andrews N., and File S.E. Handling history of rats modifies behavioural effects of drugs in the elevated plus-maze test of anxiety. Eur J Pharmacol 235 (1993) 109-112
6. Arendash G.W., and King D.L. Intra- and intertask relationships in a behavioral test battery given to Tg2576 transgenic mice and controls. Physiol Behav 75 (2002) 643-652
7. Bannerman D.M., Deacon R.M.J., Brady S., Bruce A., Sprengel R., Seeburg P.H., et al. A comparison of GluR-A deficient and wild-type mice on a test battery assessing sensorimotor, affective, and cognitive behaviors. Behav Neurosci 118 (2004) 643-647
8. Becker A., and Grecksch G. Illumination has no effect on rat's behaviour in the elevated plus-maze. Physiol Behav 59 (1996) 1175-1177
9. Becker J.T., and Olton D.S. Cognitive mapping and hippocampal system function. Neuropsychologia 19 (1981) 733-744
10. Bellhorn R.W. Lighting in the animal environment. Lab Anim Sci 30 (1980) 440-450
11. Belzung C., and Griebel G. Measuring normal and pathological anxiety-like behaviour in mice: a review. Behav Brain Res 125 (2001) 141-149
12. Beninger R.J., Jhamandas K., Boegman R.J., and El-Defrawy S.R. Effects of scopolamine and unilateral lesions of the basal forebrain on T-maze spatial discrimination and alternation in rats. Pharmacol Biochem Behav 24 (1986) 1353-1360
13. Berlyne D.E. Novelty and curiosity as determinants of exploratory behavior. Brit J Psychol 41 (1950) 68-80
14. Berlyne D.E. Conflict, Arousal and Curiosity (1960), McGraw-Hill Book Co., New York
15. Bertoglio L.J., and Carobrez A.P. Behavioural profile of rats submitted to session 1-session 2 in the elevated plus-maze during diurnal/nocturnal phases and under different illumination conditions. Behav Brain Res 132 (2002) 135-143
16. Bindra D., and Spinner N. Response to different degrees of novelty: the incidence of various activities. J Exp Anal Behav 1 (1958) 341-350
17. Birch D., and Jacobs G.H. Effects of constant illumination on vision in the albino rat. Physiol Behav 19 (1977) 255-259
18. Bisagno V., Ferguson D., and Luine VN. Chronic d-amphetamine induces sexually dimorphic effects on locomotion, recognition memory, and brain monoamines. Pharmacol Biochem Behav 74 (2003) 859-867
19. Blanchard R.J., Dulloog L., Markham C., Nishimura O., Compton J.N., Jun A., et al. Sexual and aggressive interactions in a visible burrow system with provisioned burrows. Physiol Behav 72 (2001) 245-254
20. Bouwknecht J.A., and Paylor R. Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav Brain Res 136 (2002) 489-501
21. Bowman R.E., Beck K.D., and Luine V.N. Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Hormones Behav 43 (2003) 48-59
22. Brabant C., Quertemont E., and Tirelli E. Evidence that the relations between novelty-induced activity, locomotor stimulation and place preference induced by cocaine qualitatively depend upon the dose: a multiple regression analysis in inbred C57BL/6J mice. Behav Brain Res 158 (2005) 201-210
23. Brown M.F. Does a cognitive map guide choices in the radial-arm maze?. J Exp Psychol Anim Behav Process 18 (1992) 56-66
24. Calatayud F., Coubard S., and Belzung C. Emotional reactivity in mice may not be inherited but influenced by parents. Physiol Behav 80 (2004) 465-474
25. Campbell B.M., and Merchant K.M. Serotonin 2C receptors within the basolateral amygdala induce acute fear-like responses in an open-field environment. Brain Res 993 (2003) 1-9
26. Capsoni S., Ugolini G., Comparini A., Ruberti F., Berardi N., and Cattaneo A. Alzheimer-like neurodegeneration in aged antinerve growth factor transgenic mice. PNAS 97 (2000) 6826-6831
27. Clark R.E., Zola S.M., and Squire L.R. Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20 (2000) 8853-8860
28. Clément Y., Calatayud F., and Belzung C. Genetic basis of anxiety-like behaviour: a critical review. Brain Res Bull 57 (2002) 57-71
29. Colombo P.J., Davis H.P., and Volpe B.T. Allocentric spatial and tactile memory impairments in rats with dorsal caudate lesions are affected by preoperative behavioral training. Behav Neurosci 103 (1989) 1242-1250
30. Conrad C.D., Jackson J.L., Wieczorek L., Baran S.E., Harman J.S., Wright R.L., et al. Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle. Biochem Behav 78 (2004) 569-579
31. Cook M.N., Bolivar V.J., McFadyen M.P., and Flaherty L. Behavioral differences among 129 substrains: implications for knockout and transgenic mice. Behav Neurosci 116 (2002) 600-611
32. Cornilleau-Pérès V., and Gielen C.C.A.M. Interactions between self-motion and depth perception in the processing of optic flow. Trends Neurosci 19 (1996) 196-202
33. Costall B., Jones B.J., Kelly M.E., Naylor R.J., and Tomkins D.M. Exploration of mice in a black and white test box: validation as a model of anxiety. Pharmacol Biochem Behav 32 (1989) 777-785
34. Crabbe J.C., Wahlsten D., and Dudek B.C. Genetic of mouse behavior: interactions with laboratory environment. Science 284 (1999) 1670-1672
35. Crawley J.N. Exploratory behavior models of anxiety in mice. Neurosci Biobehav Rev 9 (1985) 37-44
36. Crawley J.N., and Paylor R. A proposed test battery and constellations of specific behavioral paradigms to investigate the behavioral phenotypes of transgenic and knockout mice. Horm Behav 31 (1997) 197-211
37. Crawley J.N., Belknap J.K., Collins A., Crabbe J.C., Frankel W., Henderson N., et al. Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies. Psychopharmacology (Berl) 132 (1997) 107-124
38. Cunha J.M., and Masur J. Evaluation of psychotropic drugs with a modified open field test. Pharmacology 16 (1978) 259-267
39. Dale R.H. Spatial and temporal response patterns on the eight-arm radial maze. Physiol Behav 36 (1986) 787-790
40. Dalley J.W., Mason K., and Stanford S.C. Increased levels of extracellular noradrenaline in the frontal cortex of rats exposed to naturalistic environmental stimuli: modulation by acute systemic administration of diazepam or buspirone. Psychopharmacology (Berl) 127 (1996) 47-54
41. Darwish M., Korányi L., Nyakas C., and Almeida O.F.X. Exposure to a novel stimulus reduces anxiety level in adult and aging rats. Physiol Behav 72 (2001) 403-407
42. Dawson G.R., and Tricklebank M.D. Use of the elevated plus maze in the search for novel anxiolytic agents. Trends Pharmacol Sci 16 (1995) 33-36
43. De Boer S.F., and Koolhaas J.M. Defensive burying in rodents: ethology, neurobiology and psychopharmacology. Eur J Pharmacol 463 (2003) 145-161
44. Delini-Stula A., and Hunn C. Differential effects of anxiolytics and beta-receptor blocking drugs on novelty-oriented ("neophobic") behavior in the rat. Pharmacopsychiatry 21 (1988) 186-191
45. Diaz-Veliz G., Butron S., Benavides M.S., Dussaubat N., and Mora S. Gender, estrous cycle, ovariectomy, and ovarian hormones influence the effects of diazepam on avoidance conditioning in rats. Pharmacol Biochem Behav 66 (2000) 887-892
46. Dix S.L., and Aggleton J.P. Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res 99 (1999) 191-200
47. D'Mello G.D., and Steckler T. Animal models in cognitive behavioural pharmacology: an overview. Brain Res Cogn Brain Res 3 (1996) 345-352
48. Drai D., Kafkafi N., Benjamini Y., Elmer G., and Golani I. Rats and mice share common ethologically relevant parameters of exploratory behavior. Behav Brain Res 125 (2001) 133-140
49. Dubreuil D., Tixier C., Dutrieux G., and Edeline J.-M. Does the radial arm maze necessarily test spatial memory?. Neurobiol Learn Mem 79 (2003) 109-117
50. Dulawa S.C., Grandy D.K., Low M.J., Paulus M.P., and Geyer M.A. Dopamine D4 receptor-knock-out mice exhibit reduced exploration of novel stimuli. J Neurosci 19 (1999) 9550-9556
51. Dunnett S.B., Everitt S.B., and Robbins T.W. The basal forebrain-cortical cholinergic system: interpreting the functional consequences of excitotoxic lesions. TINS 14 (1991) 494-501
52. Ennaceur A., and Meliani K. Effects of physostigmine and scopolamine on rats' performances in object recognition and radial-maze tests. Psychopharmacol 109 (1992) 321-330
53. Ennaceur A., Neave N., and Aggleton J.P. The effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat. Behav Brain Res 88 (1997) 181-193
54. Ennaceur A. Effects of amphetamine and medial septal lesions on acquisition and retention of radial maze learning in rats. Brain Res 636 (1994) 277-285
55. Ennaceur A., and Aggleton J.P. The role of contiguity between stimulus, response and reinforcement and the effect of the presence of a cue on rat's performance in a delayed non-matching to position task assessed in a novel automated visual memory apparatus. Neurosci Res Comm 22 (1998) 21-29
56. Ennaceur A., and Delacour J. A new one-trial test for neurobiological studies of memory in rats. I: behavioral data. Behav Brain Res 31 (1988) 47-59
57. Ennaceur A, Michalikova S, Bradford A, Ahmed S. Detailed analysis of the behavior of Lister and Wistar rats in anxiety, object recognition and object location tasks. Behav Brain Res 2005.
58. Ennaceur A., Neave N., and Aggleton J.P. Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80 (1996) 9-25
59. Fernandes C., and File S.E. The influence of open arm ledges and maze experience in the elevated plus-maze. Pharmacol Biochem Behav 54 (1996) 31-40
60. Fernandes C., Gonzalez M.I., Wilson C.A., and File S.E. Factor analysis shows that female rat behavior is characterized primarily by activity, male rats are driven by sex and anxiety. Pharmacol Biochem Behav 64 (1999) 731-738
61. Fibiger H.C. Cholinergic mechanisms in learning, memory and dementia: a review of recent evidence. Trends Neurosci 14 (1991) 220-223
62. File S.E. Factors controlling measures of anxiety and responses to novelty in the mouse. Behav Brain Res 125 (2001) 151-157
63. Foley J.M., Ribeiro-Filho N.P., and Da Silva J.A. Visual perception of extent and the geometry of visual space. Vision Res 44 (2004) 147-156
64. Frick K.M., Burlingame L.A., Arters J.A., and Berger-Sweeney J. Reference memory, anxiety and estrous cyclicity in C57BL/6NIA mice are affected by age and sex. Neuroscience 95 (2000) 293-307
65. Frick K.M., and Gresack J.E. Sex differences in the behavioral response to spatial and object novelty in adult C57BL/6 mice. Behav Neurosci 117 (2003) 1283-1291
66. Frick K.M., Stillner E.S., and Berger-Sweeney J. Mice are not little rats: species differences in a one-day water maze task. NeuroReport 11 (2000) 3461-3465
67. Frye C.A., Petralia S.M., and Rhodes M.E. Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3alpha,5alpha-THP. Pharmacol Biochem Behav 67 (2000) 587-596
68. Ghi P., Orsetti M., Gamalero S.R., and Ferretti C. Sex differences in memory performance in the object recognition test possible role of histamine receptors. Pharmacol Biochem Behav 64 (1999) 761-766
69. Gilbert P.E., and Kesner R.P. Recognition memory for complex visual discriminations is influenced by stimulus interference in rodents with perirhinal cortex damage learn. Membrane 10 (2003) 525-530
70. Gray J.A. Sex differences in emotional behavior in mammals including man: endocrine beses. Acta Psychol 35 (1971) 29-46
71. Gray J.A. The psychology of fear and stress (1987), Cambridge University Press, London
72. Gray J.A., and McNaughton N. The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. 2nd ed. (2000), Oxford University Press, Oxford
73. Hall C.S. Emotional behavior in rats. I. Defecation and urination as measures of individual differences in emotionality. J Comp Physiol Psychol 18 (1934) 385-403
74. Hannesson D.K., Howland J.G., and Phillips A.G. Interaction between perirhinal and medial prefrontal cortex is required for temporal order but not recognition memory for objects in rats. J Neurosci 24 (2004) 4596-4604
75. Hannesson D.K., Howland J.G., Pollock M., Mohapel P., Wallace A.E., and Corcoran M.E. Anterior perirhinal cortex kindling produces long-lasting effects on anxiety and object recognition memory. Eur J Neurosci 21 (2005) 1081-1090
76. Harlow H.F. Motivation forces underlying learning. Learning theory, personality theory, and clinical research-the kentucky symposium (1954), John Wiley & Sons, New York p. 39
77. Hascoet M., and Bourin M. A new approach to the light/dark test procedure in mice. Pharmacol Biochem Behav 60 (1998) 645-653
78. Hashimoto H., Shintani N., Tanaka K., Mori W., Hirose M., Matsuda T., et al. Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). PNAS 98 (2001) 13355-13360
79. Heisler L.K., Chu H.-M., Brennan T.J., Danao J.A., Bajwa P., Parsons L.H., et al. Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. PNAS 95 (1998) 15049-15054
80. Heyser C.J., Pelletier M., and Ferris J.S. The effects of methylphenidate on novel object exploration in weanling and periadolescent rats ann. NY Acad Sci 1021 (2004) 465-469
81. Hogg S. A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol Biochem Behav 54 (1996) 21-30
82. Holson R.R., and Walker C. Mesial prefrontal cortical lesions and timidity in rats. II. Reactivity to novel stimuli. Physiol Behav 37 (1986) 231-238
83. Indow T. Hyperbolic representation of global structure of visual space. J Math Psychol 41 (1997) 89-98
84. Jenck F., Martin J.R., and Moreau J.-L. Animal models of panic disorder-Emphasis on face and predictive validity. Eur Neuropsychopharmacol 6 (1996) S4
85. Jenck F., Moreau J.-L., and Martin J.R. Dorsal periaqueductal gray-induced aversion as a simulation of panic anxiety: elements of face and predictive validity. Psychiat Res 57 (1995) 181-191
86. Johnston A.L., and File S.E. Sex differences in animal tests of anxiety. Physiol Behav 49 (1991) 245-250
87. Jones N., King S.M., and Duxon M.S. Further evidence for the predictive validity of the unstable elevated exposed plus-maze, a behavioural model of extreme anxiety in rats: differential effects of fluoxetine and chlordiazepoxide. Behav Pharmacol 13 (2002) 525-535
88. Kallai J., Makany T., Karadi K., and Jacobs W.J. Spatial orientation strategies in Morris-type virtual water maze task for humans. Behav Brain Res 159 (2005) 187-196
89. Kaltwasser M.T. Acoustic startle induced ultrasonic vocalization in the rat: a novel animal model of anxiety?. Behav Brain Res 43 (1991) 133-137
90. Kalueff A.V., and Tuohimaa P. Mouse grooming microstructure is a reliable anxiety marker bidirectionally sensitive to GABAergic drugs. Eur J Pharmacol 508 (2005) 147-153
91. Kassed C.A., and Herkenham M. NF-κB p50-deficient mice show reduced anxiety-like behaviors in tests of exploratory drive and anxiety. Behav Brain Res 154 (2004) 577-584
92. Kawashima N., and Kusnecov A.W. Effects of staphylococcal enterotoxin A on pituitary-adrenal activation and neophobic behavior in the C57BL/6 mouse. J Neuroimmunol 123 (2002) 41-49
93. Klebaur J.E., and Bardo M.T. The effects of anxiolytic drugs on novelty-induced place preference. Behav Brain Res 101 (1999) 51-57
94. Kliethermes C.L., Finn D.A., and Crabbe J.C. Validation of a modified mirrored chamber sensitive to anxiolytics and anxiogenics in mice. Psychopharmacology (Berl) 169 (2003) 190-197
95. Knyazev GG, Savostyanov AN, Levin EA. Uncertainty, anxiety, and brain oscillations, Neurosci Lett 2005;387:121-5.
96. Kohler C., and Srebro B. Effects of lateral and medial septal lesions on exploratory behavior in the albino rat. Brain Res 182 (1980) 423-440
97. Krazem A., Marighetto A., Higueret P., and Jaffard R. Age-dependent effects of moderate chronic ethanol administration on different forms of memory expression in mice. Behav Brain Res 147 (2003) 17-29
98. Lapin I.P. Only controls: effect of handling, sham injection, and intraperitoneal injection of saline on behavior of mice in an elevated plus-maze. J Pharmacol Toxicol Meth 34 (1995) 73-77
99. Lebrun C., Durkin T.P., Marighetto A., and Jaffard R. A comparison of the working memory performances of young and aged mice combined with parallel measures of testing and drug-induced activations of septo-hippocampal and nbm-cortical cholinergic neurones. Neurobiol Aging 11 (1990) 515-521
100. Leighty R.E., Nilsson L.N.G., Potter H., Costa D.A., Low M.A., Bales K.R., et al. Use of multimetric statistical analysis to characterize and discriminate between the performance of four Alzheimer's transgenic mouse lines differing in Aß deposition. Behav Brain Res 153 (2004) 107-121
101. Leis T., Pallage V., Toniolo G., and Will B. Working memory theory of hippocampal function needs qualification. Behav Neural Biol 42 (1984) 140-157
102. Li C., Brake W.G., Romeo R.D., Dunlop J.C., Gordon M., Buzescu R., et al. Estrogen alters hippocampal dendritic spine shape and enhances synaptic protein immunoreactivity and spatial memory in female mice. PNAS 101 (2004) 2185-2190
103. Lister R.G. The use of a plus-maze to measure anxiety in the mouse. Psychopharmacology 92 (1987) 180-185
104. Luine V.N., Jacome L.F., and MacLusky N.J. Rapid enhancement of visual and place memory by estrogens in rats. Endocrinology 144 (2003) 2836-2844
105. Lukaszewska I., and Mlodkowska Z. Exploratory motivation in response to change test in rats. Acta Neurobiol Exp 40 (1980) 161-171
106. Malmkvist J., Hansen S.W., and Damgaard B.M. Effect of the serotonin agonist buspirone on behaviour and hypothalamic-pituitary-adrenal axis in confident and fearful mink. Physiol Behav 78 (2003) 229-240
107. Marcondes F.K., Miguel K.J., Melo L.L., and Spadari-Bratfisch R.C. Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol Behav 74 (2001) 435-440
108. Martijena I.D., Calvo N., Volosin M., and Molina V.A. Prior exposure to a brief restraint session facilitates the occurrence of fear in response to a conflict situation: behavioral and neurochemical correlates. Brain Res 752 (1997) 136-142
109. Martínez J.C., Cardenas F., Lamprea M., and Morato S. The role of vision and proprioception in the aversion of rats to the open arms of an elevated plus-maze. Behav Process 60 (2002) 15-26
110. Mathis C., Neumann P.E., Gershenfeld H., Paul S.M., and Crawley J.N. Genetic analysis of anxiety-related behaviors and responses to benzodiazepine-related drugs in AXB and BXA recombinant inbred mouse strains. Behav Genet 25 (1995) 557-568
111. McIlwain K.L., Merriweather M.Y., Yuva-Paylor L.A., and Paylor R. The use of behavioral test batteries: effects of training history. Physiol Behav 73 5 (2001) 705-717
112. McNaughton N., and Corr P.J. A two-dimensional neuropsychology of defense: fear/anxiety and defensive distance. Neurosci Biobehav Rev 28 (2004) 285-305
113. Meck W.H., Church R.M., and Olton D.S. Hippocampus, time, and memory. Behav Neurosci 98 (1984) 3-22
114. Meehan C.L., and Mench J.A. Environmental enrichment affects the fear and exploratory responses to novelty of young Amazon parrots. Appl Anim Behav Sci 79 (2002) 75-88
115. Michalikova S, Ennaceur A. How rats are trained to solve a T-maze alternation task. Program No. 184.2. Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2002. Online.
116. Millan M.J. The neurobiology and control of anxious states. Progr Neurobiol 70 (2003) 83-244
117. Montgomery K.C. The relation between fear induced by novel stimulation and exploratory behavior. J Comp Physiol Psychol 48 (1955) 254-260
118. Montgomery K.C., and Monkman J.A. The relation between fear and exploratory behavior. J Comp Physiol Psychol 48 (1955) 132-136
119. Moser P.C., Bergis O.E., Jegham S., Lochead A., Duconseille E., Terranova J.-P., et al. SL65.0155, a novel 5-hydroxytryptamine4 receptor partial agonist with potent cognition-enhancing properties. J Pharmacol Exp Ther 302 (2002) 731-741
120. Mostafa R.M., Michalikova S., and Ennaceur A. A 3D spatial navigation task for assessing memory in rodents. Neurosci Res Commun 31 (2002) 19-28
121. Murray E.A., and Mishkin M. Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J Neurosci 18 (1998) 6568-6582
122. Myhrer T. Exploratory behavior and reaction to novelty in rats: effects of medial and lateral septal lesions. Behav Neurosci 103 (1989) 1226-1233
123. Nadel L., and MacDonald L. Hippocampus: cognitive map or working memory?. Behav Neural Biol 29 (1980) 405-409
124. O'Keefe J., and Nadel L. The hippocampus as a cognitive map (1978), Clarendon Press, Oxford
125. O'Shea M., Singh M.E., McGregor I.S., and Mallet P.E. Chronic cannabinoid exposure produces lasting memory impairment and increased anxiety in adolescent but not adult rats. J Psychopharmacol 18 (2004) 502-508
126. Ohl F. Testing for anxiety. Clin Neurosci Res 3 (2003) 233-238
127. Olivier B., Zethof T., Pattij T., van Boogaert M., van Oorschot R., Leahy C., et al. Stress-induced hyperthermia and anxiety: pharmacological validation. Eur J Pharmacol 463 (2003) 117-132
128. Olton D.S. The radial arm maze as a tool in behavioral pharmacology. Physiol Behav 40 (1987) 793-797
129. Olton D.S., Becker J.T., and Handelmann G.E. Hippocampus, space and memory. Behav Brain Sci 2 (1979) 313-322
130. Organisciak D.T., Darrow R.M., Barsalou L., Darrow R.A., Kutty R.K., Kutty G., et al. Light history and age-related changes in retinal light damage. Invest Ophthalmol Vis Sci 39 (1998) 1107-1116
131. Orsini C., Buchini F., Piazza P.V., Puglisi-Allegra S., and Cabib S. Susceptibility to amphetamine-induced place preference is predicted by locomotor response to novelty and amphetamine in the mouse. Psychopharmacology (Berl) 172 (2004) 264-270
132. O'Steen W.K., Shear C.R., and Anderson K.V. Retinal damage after prolonged exposure to visible light. A light and electron microscopic study. Am J Anat 134 (1972) 5-21
133. Overstreet D.H., Commissaris R.C., De La Garza R., File S.E., Knapp D.J., and Seiden L.S. Involvement of 5-HT1A receptors in animal tests of anxiety and depression: evidence from genetic models. Stress 6 (2003) 101-110
134. Pawlak C.R., and Schwarting R.K. Object preference and nicotine consumption in rats with high versus low rearing activity in a novel open field. Pharmacol Biochem Behav 73 (2002) 679-687
135. Pellow S., Chopin P., File S.E., and Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Meth 14 (1985) 149-167
136. Pellow S., and File S.E. Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol Biochem Behav 24 (1986) 525-529
137. Pereira L.O., da Cunha I.C., Neto J.M., Paschoalini M.A., and Faria M.S. The gradient of luminosity between open/enclosed arms, and not the absolute level of Lux, predicts the behaviour of rats in the plus maze. Behav Brain Res 159 (2005) 55-61
138. Piper B.J., and Meyer J.S. Memory deficit and reduced anxiety in young adult rats given repeated intermittent MDMA treatment during the periadolescent period. Pharmacol Biochem Behav 79 (2004) 723-731
139. Popovic M., Caballero-Bleda M., Puelles L., and Guerri C. Multiple binge alcohol consumption during rat adolescence increases anxiety but does not impair retention in the passive avoidance task. Neurosci Lett 357 (2004) 79-82
140. Powell S.B., Geyer M.A., Gallagher D., and Paulus M.P. The balance between approach and avoidance behaviors in a novel object exploration paradigm in mice. Behav Brain Res 152 (2004) 341-349
141. Prut L., and Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol 463 (2003) 3-33
142. Pryce C.R., Lehmann J., and Feldon J. Effect of sex on fear conditioning is similar for context and discrete CS in Wistar, Lewis and Fischer rat strains. Pharmacol Biochem Behav 64 (1999) 753-759
143. Rawlins J.N.P., and Olton D.S. The septo-hippocampal system and cognitive mapping. Behav Brain Res 5 (1982) 331-358
144. Reines B.P. The relationship between laboratory and clinical studies in psychopharmacologic discovery. Perspec Med Res 2 (1990) 13-26
145. Robbins T.W. Homology in behavioural pharmacology: an approach to animal models of human cognition. Behav Pharmacol 9 (1998) 509-519
146. Roberts A.C. Comparison of cognitive function in human and non-human primates. Brain Res Cogn Brain Res 3 (1996) 319-327
147. Rodgers R.J., and Johnson N.J.T. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus maze. Pharmacol Biochem Behav 52 (1995) 297-303
148. Rogers D.C., Jones D.N.C., Nelson P.R., Jones C.M., Quilter C.A., Robinson T.L., et al. Use of SHIRPA and discriminant analysis to characterise marked differences in the behavioural phenotype of six inbred mouse strains. Behav Brain Res 105 (1999) 207-217
149. Roy V., Belzung C., Delarue C., and Chapillon P. Environmental enrichment in BALB/c mice: effects in classical tests of anxiety and exposure to a predatory odor. Physiol Behav 74 (2001) 313-320
150. Roy V., and Chapillon P. Further evidences that risk assessment and object exploration behaviours are useful to evaluate emotional reactivity in rodents. Behav Brain Res 154 (2004) 439-448
151. Sagvolden T, Russell VA, Aase H, Johansen EB, Farshbaf M. Rodent models of attention-deficit/hyperactivity disorder, Biol Psychiatry 2005;57:1239-47.
152. Sarter M., Hagan J., and Dudchenko P. Behavioral screening for cognition enhancers: from indiscriminate to valid testing. Part I. Psychopharmacology (Berl) 107 (1992) 144-159
153. Schmitt U., and Hiemke C. Strain differences in open-field and elevated plus-maze behavior of rats without and with pretest handling. Pharmacol Biochem Behav 59 (1998) 807-811
154. Sheldon A.B. Preferences for familiar versus novel stimuli as a function of the familiarity of the environment. J Comp Phys Psychol 50 (1969) 509-513
155. Shepherd J.K., Grewal S.S., Fletcher A., Bill D.J., and Dourish C.T. Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology (Berl) 116 (1994) 56-64
156. Sherwin C.M., and Glen E.F. Cage colour preferences and effects of home cage colour on anxiety in laboratory mice. Anim Behav 66 (2003) 1085-1092
157. Simon P., Dupuis R., and Costentin J. Thigmotaxis as an index of anxiety in mice: influence of dopaminergic transmissions. Behav Brain Res 31 (1994) 59-64
158. Stansfield K.H., Philpot R.M., and Kirstein C.L. An animal model of sensation seeking: the adolescent rat. Ann NY Acad Sci 1021 (2004) 453-458
159. Stefanski R., Palejko W., Bidzinski A., Kostowski W., and Plaznik A. Serotonergic innervation of the hippocampus and nucleus accumbens septi and the anxiolytic-like action of the 5-HT3 receptor antagonists. Neuropharmacology 32 (1993) 987-993
160. Steward O. Evaluation of short-term cue recollection following entorhinal cortical lesions in rats. Behav Neural Biol 31 (1981) 187-197
161. Stock H., Foradori C., Ford K., and Wilson M.A. A lack of tolerance to the anxiolytic effects of diazepam on the plus-maze: comparison of male and female rats. Psychopharmacology 147 (2000) 362-370
162. Szechtman H., Eckert M.J., Tse W.S., Boersma J.T., Bonura C.A., McClelland J.Z., et al. Compulsive checking behavior of quinpirole-sensitized rats as an animal model of obsessive-compulsive disorder (OCD): form and control. BMC Neurosci 2 (2001) 4
163. Tang X., Orchard S.M., and Sanford L.D. Home cage activity and behavioral performance in inbred and hybrid Mice. Behav Brain Res 136 (2002) 555-569
164. Tang X., and Sanford L.D. Home cage activity and activity-based measures of anxiety in 129P3/J, 129X1/SvJ and C57BL/6J mice. Physiol Behav 84 (2005) 105-115
165. Tarantino L.M., and Bucan M. Dissection of behavior and psychiatric disorders using the mouse as a model. Hum Mol Genet 9 (2000) 953-965
166. Tizabi Y., Louis V.A., Taylor C.T., Waxman D., Culver K.E., and Szechtman H. Effect of nicotine on quinpirole-induced checking behavior in rats: implications for obsessive-compulsive disorder. Biol Psychiat 51 (2002) 164-171
167. Toledano A., and Alvarez M.I. Lesions and dysfunctions of the nucleus basalis as Alzheimer's disease models: general and critical overview and analysis of the long-term changes in several excitotoxic models. Curr Alzheimer Res 1 (2004) 189-214
168. Treit D., and Fundytus M. Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav 31 (1988) 959-962
169. Treit D., and Pesold C. Septal lesions inhibit fear reactions in two animal models of anxiolytic drug action. Physiol Behav 47 (1990) 365-371
170. van der Staay F.J., Kerbusch S., and Raaijmakers W. Genetic correlations in validating emotionality. Behav Genet 20 (1990) 51-62
171. van der Stelt HM, Breuer ME, Olivier B, Westenberg HGM. Permanent deficits in serotonergic functioning of olfactory bulbectomized rats: an in vivo microdialysis study. Biol Psychiatry 2005;57:1061-7.
172. van Drief K.S., and Talling J.C. Familiarity increases consistency in animal tests. Behav Brain Res 159 (2005) 243-245
173. van Gaalen M.M., and Steckler T. Behavioural analysis of four mouse strains in an anxiety test battery. Behav Brain Res 115 (2000) 95-106
174. Vnek N., and Rothblat L.A. The hippocampus and long-term object memory in the rat. J Neurosci 16 (1996) 2780-2787
175. Vogel J.R., Beer B., and Clody D.E. A simple and reliable conflict procedure for testing anti-anxiety agents. Psychopharmacologia 21 (1971) 1-7
176. Voikar V., Koks S., Vasar E., and Rauvala H. Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol Behav 72 (2001) 271-281
177. Wahlsten D. Standardizing tests of mouse behavior: reasons, recommendations, and reality. Physiol Behav 73 (2001) 695-704
178. Wahlsten D., Metten P., Phillips T.J., Boehm II S.L., Burkhat-Kasch S., Dorow J., et al. Different data from different labs: lessons from studies of gene-environment interaction. J Neurobiol 54 (2003) 283-311
179. Walker J.A., and Olton D.S. Fimbria-fornix lesions impair spatial working memory but not cognitive mapping. Behav Neurosci 98 (1984) 226-242
180. Wall P.M., and Messier C. Ethological confirmatory factor analysis of anxiety-like behaviour in the murine elevated plus-maze. Behav Brain Res 114 (2000) 199-212
181. Weiss S.M., Wadsworth G., Fltcher A., and Dourish C.T. Utility of ethological analysis to overcome locomotor confounds in elevated maze models of anxiety. Neurosci Biobehav Rev 23 (1998) 265-271
182. Welker W.I. "Free" versus "forced" exploration of a novel situation by rats. Psychol Rep 3 (1957) 95-108
183. Welker W.I. Escape, exploratory, and food-seeking responses of rats in a novel situation. J Comp Physiol Psychol 52 (1959) 106-111
184. Wêsierska M., Walasek G., Kilijanek J., Djavadian R.L., and Turlejski K. Behavior of the gray short-tailed opossum (Monodelphis domestica) in the open field and in response to a new object, in comparison with the rat. Behav Brain Res 143 (2003) 31-40
185. Whiting J.W.M., and Mowrer O.H. Habit progression and regression-a laboratory study of some factors relevant to human socialization. J Comp Psychol 36 (1943) 229-253
186. Wilson M.A., Burghardt P.R., Ford K.A., Wilkinson M.B., and Primeaux S.D. Anxiolytic effects of diazepam and ethanol in two behavioral models: comparison of males and females. Pharmacol Biochem Behav 78 (2004) 445-458
187. Wozniak D.F., Stewart G.R., Finger S., and Olney J.W. Comparison of behavioral effects of nucleus basalis magnocellularis lesions and somatosensory cortex ablation in the rat. Neuroscience 32 (1989) 685-700
188. Wozniak R.H. Classics in psychology, 1855-1914: historical essays (1999), Thoemmes Press
189. Xu S.J., Chen Z., Zhu L.J., Shen H.Q., and Luo J.H. Visual recognition memory is related to basic expression level of NMDA receptor NR1/NR2B subtype in hippocampus and striatum of rats. Acta Pharmacol Sin 26 (2005) 177-180
190. Yoerg S.I., and Kamil A.C. Response strategies in the radial arm maze: running around in circles. Anim Lear Behav 10 (1982) 530-534
191. Zimmerberg B., and Farley M.J. Sex differences in anxiety behavior in rats: role of gonadal hormones. Physiol Behav 54 (1993) 1119-1124
192. Zola-Morgan S., Squire L.R., and Ramus S.J. Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system. Hippocampus 4 (1994) 483-495
193. Zörner B., Wolfer D.P., Brandis D., Kretz O., Zacher C., Madani R., et al. Forebrain-specific trkB-receptor knockout mice: behaviorally more hyperactive than "depressive". Biol Psychiat 54 (2003) 972-982