Spatial memory: Theoretical basis and comparative review on experimental methods in rodents

Behavioural Brain Research

Volumn 203, Issue 2, 2009, Pages 151-164

  Paul, Carrillo Mora ^a   Magda, Giordano ^b   Abel, Santamaría ^a  

^a NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

^b INSTITUTO DE NEUROBIOLOGÍA   (Mexico)

Author keywords

Barnes maze; Morris maze; Radial maze; Spatial reference memory; Spatial working memory

Indexed keywords

AGING; AMNESIA; ANALYTIC METHOD; ANIMAL BEHAVIOR; ASSOCIATION; BRAIN DAMAGE; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CENTRAL NERVOUS SYSTEM DISEASE; CLINICAL ASSESSMENT TOOL; COGNITION; DEMENTIA; EGO; EXPLORATORY BEHAVIOR; FUNCTIONAL ASSESSMENT; HUMAN; LATENT PERIOD; LEARNING; LONG TERM MEMORY; MAZE TEST; MEMORY CONSOLIDATION; MEMORY DISORDER; MENTAL CAPACITY; MENTAL PERFORMANCE; MENTAL TASK; METHODOLOGY; NEUROTOXICITY; NONHUMAN; PERCEPTIVE DISCRIMINATION; PRIORITY JOURNAL; PROBLEM SOLVING; PSYCHOPATHY; RECALL; REVIEW; SHORT TERM MEMORY; SKILL; SPATIAL DISCRIMINATION; SPATIAL MEMORY; SYMBOLISM; VERBAL MEMORY; VISUAL INFORMATION; VISUAL MEMORY; WORKING MEMORY;

ANIMALS; COGNITION; MAZE LEARNING; MEMORY; MEMORY DISORDERS; RODENTIA; SPACE PERCEPTION; SPATIAL BEHAVIOR;

EID: 67649644720     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2009.05.022     Document Type: Review

References (142)

1. Arolfo M.P., Nerad F., Schenk F., and Bures J. Absence of snapshot memory of the target view interferes with place navigation learning by rats in the water maze. Behav Neurosci 108 (1994) 308-316
2. 2) promote memory deterioration. Neurotoxicology 27 (2006) 1007-1012
3. Awh E., and Jonides J. Overlapping mechanisms of attention and spatial working memory. Trends Cog Sci 5 (2001) 119-126
4. Bach M.E., Hawkins R.D., Osman M., Kandel E.R., and Mayford M. Impairment of spatial but not contextual memory in CaMKII mutant mice with a selective loss of hippocampal LTP in the range of the theta frequency. Cell 81 (1995) 905-915
5. Balderas I., Rodriguez-Ortiz C.J., Salgado-Tonda P., Chavez-Hurtado J., McGaugh J.L., and Bermudez-Rattoni F. The consolidation of object and context recognition memory involves different regions of the temporal lobe. Learn Mem 15 (2008) 618-624
6. Baldi E., Efoudebe M., Lorenzini C.A., and Bucherelli C. Spatial navigation in the Morris water maze: working and long lasting reference memories. Neurosci Lett 378 (2005) 176-180
7. Bammer G. Pharmachological investigations of neurotransmitter involvement in passive avoidance responding: a review and some new results. Neurosci Biobehav Rev 6 (1982) 247-296
8. Barnes C. Memory deficit associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 93 (1979) 74-104
9. Barnes C., Nadel L., and Honig W.K. Spatial memory deficit in senescent rats. Can J Psychol 34 (1980) 29-39
10. Barnes C.A., Markowska A.L., Ingram D.K., Kametani H., Spangler E.L., Lemken V.J., et al. Acetyl-l-carnitine 2: effects of learning and memory performance of aged rats in simple and complex mazes. Neurobiol Aging 11 (1990) 499-506
11. Bats S., Thoumas J.L., Lordi B., Tonon M.C., Lalonde R., and Caston J. The effects of a mild stressor on spontaneous alternation in mice. Behav Brain Res 118 (2001) 11-15
12. Beatty W., and Bierley R. Scopolamine degrades spatial working memory but spares spatial reference memory: dissimilarity of anticholinergic effect and restriction of distal visual cues. Pharmacol Biochem Behav 23 (1985) 1-6
13. Benhamou S., and Poucet B. A comparative analysis of spatial memory processes. Behav Process 35 (1996) 113-126
14. Berlyne D.E. Novelty and curiosity as determinants of exploratory behavior. Br J Psychol 41 (1950) 68-80
15. Bolding K., and Rudy J.W. Place learning in the Morris water task. Making the memory stick. Learn Mem 13 (2006) 278-286
16. Brandeis R., Brandys Y., and Yehuda S. The use of the Morris water maze in the study of memory and learning. Int J Neurosci 48 (1989) 29-69
17. Broadbent N.J., Squire L.R., and Clark R.E. Spatial memory, recognition memory and hippocampus. Proc Natl Acad Sci 101 (2004) 14515-14520
18. Brown M.F. Does a cognitive map guide choices in tha radial-arm maze?. J Exp Psychol Anim Behav Process 18 (1992) 56-66
19. Brown M.F., and Terrinoni M. Control of choice by the spatial configuration of goals. J Exp Psychol Anim Behav Process 22 (1996) 438-446
20. Bucci D.J., Chiba A.A., and Gallagher M. Spatial learning in male and female Long-Evans rats. Behav Neurosci 109 (1995) 180-183
21. Bures J., Fenton A.A., Kaminsky Y., Wesierska M., and Zahalka A. Rodent navigation after dissociation of the allocentric and idiothetic representations of space. Neuropharmacology 37 (1998) 689-699
22. Buresova O., Bures J., Oitzl M.S., and Zahalka A. Radial maze in the water tank. An aversively motivated spatial working memory task. Physiol Behav 34 (1985) 1003-1005
23. Burgess N. Spatial memory: how egocentric and allocentric combine. Trends Cog Sci 10 (2006) 551-557
24. Chess A.C., Simoni M.K., Alling T.E., and Bucci D.J. Elevations of endogenous kynurenic acid produces spatial working memory deficits. Schizo Bull 33 (2007) 797-804
25. Cimadevilla J.M., Fenton A., and Bures J. Continuous place avoidance task reveals differences in spatial navigation in male and female rats. Behav Brain Res 107 (2000) 161-169
26. Cimadevilla J.M., Kaminsky Y., Fenton A., and Bures J. Passive and active place avoidance as a tool for spatial memory research in rats. J Neurosci Methods 102 (2000) 155-164
27. Coluccia E., and Louse G. Gender differences in spatial orientation: a review. J Environ Psychol 24 (2004) 329-340
28. Czurko A., Czeh B., Seress L., Nadel L., and Bures J. Severe spatial navigation deficits in the Morris water maze after single high dose of neonatal X-ray irradiation in the rat. Proc Natl Acad Sci 94 (1997) 2766-2771
29. Das A., Dikshit M., Singh H.K., and Nath C. Evaluation of effect of scopolamine on stages of active avoidance learning in rats. Ind J Pharmachol 35 (2003) 47-50
30. Dawood M.Y., Lumley L.A., Robison C.L., Saviolakis G.A., and Meyerhoff J.L. Accelerated Barnes maze test in mice for assessment of stress effects on memory. Ann N Y Acad Sci 1032 (2004) 304-307
31. Deacon R.M., and Rawlins N.P. T-maze alternation in the rodent. Nat Protoc 1 (2006) 7-12
32. Del Arco A., Segovia G., Garrido P., de Blas M., and Mora F. Stress, prefrontal cortex and environmental enrichment: studies on dopamine and acetylcholine release and working memory performance in rats. Behav Brain Res 176 (2007) 267-273
33. Delcasso S., Jeantet Y., and Cho Y.H. A new test for long-term spatial memory using an operant chamber in mice. Behav Brain Res 178 (2007) 200-207
34. Dember W.N., and Fowler H. Spontaneous alternation after free and forced trials. Can J Psychol 13 (1959 l) 151-154
35. Dere E., Huston J.P., and De Souza-Silva M.A. Integrated memory for objects, place and temporal order: evidence for episodic-like memory in mice. Neurobiol Learn Mem 84 (2005) 214-221
36. Dere E., Kart-Teke E., Huston J.P., and De Souza-Silva M.A. The case for episodic memory in animals. Neurosci Biobehav Rev 30 (2006) 1206-1224
37. D'Hooge R., and De Deyn P. Aplications of the Morris water maze in the study of learning and memory. Brain Res Rev 36 (2001) 60-90
38. Dubreuil D., Tixer C., Dutrieux G., and Edeline J.M. Does the radial arm maze necessarily test spatial memory?. Neurobiol Learn Mem 79 (2003) 109-117
39. Dudchenko P.A. An overview of the task used to test working memory in rodents. Neurosci Biobehav Rev 28 (2004) 699-709
40. Eichenbaum H., Dudchenko P., Wood E., Shapiro M., and Tanila H. The hippocampus, memory, and place cells: is it spatial memory or a memory space?. Neuron 23 (1999) 209-226
41. Ennaceur A., and Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1. Behavioral data. Behav Brain Res 31 (1988) 47-59
42. Fedorova I., Hussein N., Di Martino C., Muriguchi T., Hoshiba J., Majchrzak S., et al. An n-3 fatty acids deficient diet affects mouse spatial learning in the Barnes circular maze. Prost Leuko Essen Fatty Acids 77 (2007) 277-279
43. Fox G.B., Fan L., LeVasseur R.A., and Faden A.I. Effect of traumatic brain injury on mouse spatial and non-spatial learning in the Barnes circular maze. J Neurotrauma 15 (1998) 1037-1046
44. Francis D.D., Zaharia M.D., Shanks H., and Anisman H. Stress induced disturbances in Morris water-maze performance inter-strain variability. Physiol Behav 58 (1995) 57-65
45. Frautschy S.A., Yang F., Calderon L., and Cole G.M. Rodent models of Alzheimer's disease: rat Aβ infusion approaches to amyloid deposits. Neurobiol Aging 17 (1996) 311-321
46. Geinisman Y., DeToledo-Morrell L., Morrell F., and Heller R.E. Hippocampal markers of aged-related memory dysfunction: behavioral, electrophysiological and morphological perspectives. Prog Neurobiol 45 (1995) 223-252
47. Gerlai R. A new continuous alternation task in the T maze detects hippocampal dysfunction in mice. A strain comparison and lesion study. Behav Brain Res 95 (1998) 91-101
48. Goodrick C.L. Learning by mature-young and aged Wistar rats as a function of test complexity. J Gerontol 27 (1972) 353-357
49. Grobety M.C., and Schenk F. The influence of spatial irregularity upon radial maze performance in the rat. Learn Behav 20 (1992) 393-400
50. Hamilton D.A., Aker s.K.G., Johnson T.E., Rice J.P., Candelaria F.T., Weisend M.P., et al. The relative influence of place and direction in the Morris water task. J Exp Psychol 34 (2008) 31-53
51. Harrison F.E., Reiserer R.S., Tomarken A.J., and McDonald M.P. Spatial and non spatial escape strategies in the Barnes maze. Learn Mem 13 (2006) 809-819
52. Healy S.D., Braham S.R., and Braithwaite V.A. Spatial working memory in rats: no differences between the sexes. Proc Roy Soc B 266 (1999) 2303-2308
53. Hodges H. Maze procedures: the radial-arm and water maze compared. Cog Brain Res 3 (1996) 167-181
54. Holdstock J.S., Mayes A.R., Cezayirli E., Isaac C.L., Aggleton J.P., and Roberts N. A comparison of egocentric and allocentric spatial memory in a patient with selective hipocampal damage. Neuropsychologia 38 (2000) 410-425
55. Holscher C. Stress impairs performance in spatial water maze learning task. Behav Brain Res 100 (1999) 225-235
56. Hong S.M., Lui Z., Fan Y., Neumann M., Won S.J., Lac D., et al. Reduced hippocampal neurogenesis and skill reaching performance in adult Emx1 mutant mice. Exp Neurol 206 (2007) 24-32
57. Hyde L.A., Hopligth B.J., and Denenberg V.H. Water version of the radial-arm maze: learning in three inbred strains of mice. Brain Res 785 (1998) 236-244
58. Hyde L.A., Sherman G., and Denenberg V.H. Non-spatial water radial arm maze learning in mice. Brain Res 863 (2000) 151-159
59. Ingram D.K., Sprangler E.L., Iijima S., Ikari H., Kuo H., Greig N.H., et al. Rodent models of memory dysfunction in Alzheimer's disease and normal aging: moving beyond the cholinergic hypothesis. Life Sci 55 (1994) 2037-2049
60. Ingram D.K. Complex maze learning in rodents as a model of aged related memory impairment. Neurobiol Aging 9 (1988) 475-485
61. Inman-Wood S.L., Williams M.T., Morford L.L., and Vorhees C.V. Effects of prenatal cocaine on Morris and Barnes maze tests of spatial learning and memory in the offspring of C57BL/6J mice. Neurotoxicol Teratol 22 (2000) 547-557
62. James T.W., and Kimura D. Sex differences in remembring the locations of objects in an array: location-shifts versus location-exchanges. Evol Hum Behav 18 (1997) 155-163
63. Jarvik M.E., and Kopp A. An improved one-trial passive avoidance learning situation. Psychol Rep 21 (1967) 221-224
64. Jonasson Z. Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci Biobehav Rev 28 (2005) 811-825
65. Kealy J., Diviney M., Kehoe E., McGonagle V., ÓShea A., Harvey D., et al. The effects of overtraining in the Morris water maze on allocentric and egocentric learning strategies in rats. Behav Brain Res 192 (2008) 259-263
66. Kessels R.P.C., de Haan E.H.F., Kappelle L.J., and Postma A. Varieties of human spatial memory: a meta-analysis on the effects of hippocampal lesions. Brain Res Rev 35 (2001) 295-303
67. Kimura D., and Hampson E. Cognitive pattern in men and women is influenced by fluctuations in sex hormones. Curr Dir Psychol Sci 3 (1994) 57-61
68. Klatzky R.L. Allocentric and egocentric spatial representations: definitions, distinctions, and interconnections. In: Freksa C., Habel C., and Wender K.F. (Eds). Spatial cognition-an interdisciplinary approach to representation and processing of spatial knowledge (1998), Springer-Verlag, Berlin 1-17
69. Koopmans G., Blokland A., Nieuwenhuijzen P.V., and Prickaerts J. Assesment of spatial learning abilities of mice in a circular maze. Physiol Behav 79 (2003) 683-693
70. Kyrkby D.L., Jones D.N.C., and Higgins G.A. Influence of prefeeding and scopolamine upon performance in a delayed matching-to-position task. Behav Brain Res 67 (1995) 221-227
71. LaBuda C.J., Mellgren R.L., and Hale R.L. Sex differences in the acquisition of a radial maze task in the CD-1 mouse. Physiol Behav 76 (2002) 213-217
72. Lalonde R. The neurobiological basis of spontaneous alternation. Brain Res Rev 26 (2002) 91-104
73. Lamberty Y., and Gower A.J. Simplifying environmental cues in a Morris-type water maze improves place learning in old NMRI mice. Behav Neural Biol 54 (1991) 89-100
74. Lindner M.D., and Schallert A. Aging and atropine effects on spatial navigation in the Morris water task. Behav Neurosci 102 (1988) 621-634
75. Lipp H.P., and Wolfer D.P. Genetically modified mice and cognition. Curr Op Neurobiol 8 (1998) 272-280
76. Locchi F., Dall'Ollio R., Gandolfi O., and Rimondini R. Water T-maze, an improved method to assess spatial working memory in rats: pharmacological validation. Neurosci Lett 422 (2007) 213-216
77. Lukoyanov N.V., Madeira M.D., and Paula-Barbosa M.M. Behavioral and neuroanatomical consequences of chronic ethanol intake and withdrawal. Physiol Behav 66 (1999) 337-346
78. Maei H.R., Zaslavsky K., Teixeira C.M., and Frankland P.W. What is the most sensitive measure of water maze probe test performance?. Front Integr Neurosci 3 (2009) 1-9
79. Markowska A.L., Spangler E.L., and Ingram D.K. Behavioral assessment of the senescence-accelerated mouse (SAM P8 and R1). Physiol Behav 64 (1998) 15-26
80. Maviel T., and Durkin T.P. Role of central cholinergic receptor sub-types in spatial working memory: a five-arm maze task in mice provides evidence for a functional role of nicotinic receptors in mediating trace access processes. Neuroscience 120 (2003) 1049-1059
81. Mazmanian D.S., and Roberts W.A. Spatial memory in rats under restricted viewing conditions. Learn Motiv 14 (1983) 123-139
82. McDonald M.P., and Overmier J.B. Present imperfect: a critical review of animal models of the mnemonic impairments in Alzheimer's disease. Neurosci Biobehav Rev 22 (1998) 99-120
83. Mclay R.N., Freeman S.M., and Zadina J.E. Chronic corticosterone impairs memory performance in the Barnes maze. Physiol Behav 63 (1998) 933-937
84. McNamara R.K., dePape G.E., and Skelton R.W. Differential effects of benzodiacepine receptor agonist on hipocampal long term potentiation and spatial learning in the Morris water maze. Brain Res 626 (1993) 63-70
85. Moffat S.D., Hampson E., and Hatzipantelis M. Navigation in virtual maze: sex differences and correlation with psychometric measures of spatial ability in humans. Evol Hum Behav 19 (1998) 73-87
86. Moghaddam M., and Bures J. Contribution of egocentric spatial memory to place navigations of rats in the Morris water maze. Behav Brain Res 78 (1996) 121-129
87. Morris R.G.M. Developments of a water maze procedure for studying spatial learning in the rat. J Neurosci Methods 11 (1984) 47-60
88. Morris R.G.M. Spatial localization does not require the presence of local cues. Learn Motiv 12 (1981) 239-260
89. Moscovitch M., Nadel L., Winocur G., Gilboa A., and Rosenbaum R.S. The cognitive neuroscience of remote episodic, semantic and spatial memory. Curr Opin Neurobiol 16 (2006) 179-190
90. Moscovitch M., Rosenbaum R.S., Gilboa A., Addis D.R., Westmacott R., Grady C., et al. Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J Anat 207 (2005) 35-66
91. Mueller B.R., and Bale T.L. Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav 91 (2007) 55-65
92. Nyffeler T., Gutbrod K., Pflugshaupt T., vonWartburg R., Hess C.W., and Müri R.M. Allocentric and egocentric spatial impairments in a case of topographical disorientation. Cortex 41 (2005) 133-143
93. O'Keefe J. An allocentric spatial model for the hippocampal cognitive map. Hippocampus 1 (1991) 230-235
94. ÓKeefe J., and Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34 (1971) 171-175
95. O'Keefe J., and Nadel L. The hippocampus as a cognitive map (1978), Clarendon Press, Oxford
96. Olton D.S. The radial arm maze as a tool in behavioural phamachology. Physiol Behav 40 (1985) 793-797
97. Olton D.S., and Samuelson R.J. Remembrance of place passed. Spatial memory in rats. J Exp Psychol: Anim Behav Process 2 (1976) 97-116
98. Olton D.S., Collison C., and Werz M. Spatial memory and radial arm maze performance of rats. Learn Motiv 8 (1977) 289-314
99. Olton D.S., Becker J.T., and Handelmann G.E. Hippocampus space and memory. Behav Brain Sci 2 (1979) 313-365
100. Ormerod B.K., and Beinnger R.J. Water maze versus radial maze: differential performance of rats in spatial delayed match-to-position task and responde to scopolamine. Behav Brain Res 128 (2002) 139-152
101. O'Tuathaigh C.M., Babovic D., ÓSullivan G.J., Clifford J.J., Tighe O., Croke D.T., et al. Phenotypic characterization of spatial cognition and social behavior in mice with "knockout" of the schizophrenia risk gene neuregulin 1. Neuroscience 147 (2007) 18-27
102. Paganelli R.A., Benetolli A., Miltus-Lima K.C., Cestari-Junior L.A., Favero-Filho, and Milani H. A novel version of the 8-arm radial maze: effects of cerebral ischemia on learning and memory. J Neurosci Methods 132 (2004) 9-18
103. sw transgenic mouse model for Alzheimer disease. J Neurosci Methods 87 (1999) 87-95
104. Raber J., Rola R., LeFevour A., Morhardt D., Curley J., Mitzumatsu S., et al. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162 (2004) 39-47
105. Rains D.G. Sistemas de memoria. In: Rains D.G. (Ed). Principios de neuropsicología humana. 1st ed. (2004), Mc Graw Hill, México 241-286
106. Rogers D.C., and Hunter A.J. Phototrombotic lesions of the rat cortex impair acquisition of the water maze. Pharmacol Biochem Behav 56 (1997) 747-754
107. Roullet P., Lassalle J., and Jegat R. A study of behavioral and sensorial bases of radial maze learning in maze. Behav Neural Biol 59 (1993) 173-179
108. Rutten K., Reneerkens O.A.H., Hamers H., Sik A., McGregor I.S., Prickaerts J., et al. Automated scoring of novel object recognition in rats. J Neurosci Methods 171 (2008) 72-77
109. Sandi C. The role and mechanisms of action of glucocorticoid involvement in memory storage. Neural Plast 6 (1998) 41-52
110. Seymoure P., Hui-Dou H., and Juraska J.M. Sex differences in radial arm maze performance: Influence of rearing environment and room cues. Psychobiology 24 (1996) 33-37
111. Sherry D.G.H., and Hampson E. Evolution and the hormonal control of sexually dimorphic spatial abilities in humans. Trends Cog Sci 1 (1997) 50-56
112. Spowart-Manning L., and van der Staay F.J. The T-maze continuous alternation task for assessing the effects of putative cognition enhancers in the mouse. Behav Brain Res 151 (2004) 37-46
113. Squire L.R. Mechanisms of memory. Science 232 (1986) 1612-1619
114. Steckler T., Drinkenburg W.H., Sahgal A., and Aggleton J.P. Recognition memory in rats. I. Concepts and classification. Prog Neurobiol 54 (1998) 289-311
115. Stone C. The age factor in animal learning. I. Rats in the problem box and the maze. Gen Psychol Monogr 5 (1929) 1-30
116. Sunyer B., Patil S., Hoger H., and Lubec G. Barnes maze, a useful task to assess spatial reference memory in the mice. Nat Protoc 390 (2007) 10-38
117. Susuki S., Augerinos G., and Black A.H. Stimulus control of spatial behavior on the eight-arm maze in rats. Learn Motiv 11 (1980) 1-18
118. Sutherland R.J., Chew G.L., Baker J.C., and Linggard R.C. Some limitations on the use of distal cues in place navigation by rats. Psychobiology 15 (1987) 48-57
119. Talpos J.C., Dias R., Bussey T.J., and Saksida L.M. Hippocampal lesions in rats impair learning and memory for locations on a touch-sensitive computer screen: The "ASAT" task. Behav Brain Res 192 (2008) 216-225
120. Thinus-Blanc C. Exploration and spatial knowledge. Animal Spatial Cognition. Behavioral and Neural Approaches. 1st ed. (1996), Word Scientific, Singapore p. 1-42
121. Tolman E.C. Cognitive maps in rats and men. Psychol Rev 55 (1948) 189-208
122. Torrejais J.C., Rosa C.C., Boerngen-Lacerda R., and Andreatini R. The elevated T-maze as a measure of two types of defensive reactions: a factor analysis. Brain Res Bull 76 (2008) 376-379
123. Tulving E. How many memory systems are there?. Am Psychol 40 (1985) 385-398
124. Tulving E., and Markowitsch H.J. Episodic and declarative memory: role of the hippocampus. Hippocampus 8 (1998) 198-204
125. Tulving E., and Schacter D.L. Priming and human memory systems. Science 247 (1990) 301-306
126. Upchurch M., and Wehner J.M. Differences between inbred strains of mice in Morris water maze performance. Behav Gen 18 (1988) 55-68
127. Uttal D.H. Seeing the big picture: map use and the development of spatial cognition. Dev Sci 3 (2000) 247-286
128. Van Dam D., Lenders G., and De Deyn P.P. Effect of Morris water maze diameter on visual-spatial learning in different mouse strains. Neurobiol Learn Mem 85 (2006) 164-172
129. van der Staay F.J. Effects of the size of the Morris water tank on spatial discrimination learning in the CFW1 mouse. Physiol Behav 68 (2000) 599-602
130. van Haaren F., van Hest A., and Heinsbroek R.P. Behavioral differences between male and female rats: effects of gonadal hormones on learning and memory. Neurosci Biobehav Rev 14 (1990) 23-33
131. van Haaren F., Wouters M., and van de Poll N. Absence of behavioural differences between male and female rats in different radial arm maze procedures. Physiol Behav 39 (1987) 409-412
132. Verzar-McDougall E.J. Studies in learning and memory in ageing rats. Gerontologia 1 (1957) 65-85
133. Vincent S.B. The white rat and the maze problem. J Anim Behav 5 (1915) 1-24
134. Vorhees C.V. Maze learning in rats: a comparison of performance in two water mazes in progeny prenatally exposed to different doses of phenytoin. Neurotoxicol Teratol 9 (1987) 235-241
135. Vorhees C.V., Acuff-Smith K.D., Weisenburger W.P., Minck D.R., and Berry H.K. Branched chain amino acids improve radial arm maze and water maze forced choice learning in rat offspring exposed in utero to hyperphenylalaninemia. Neurotoxicol Teratol 14 (1992) 35-41
136. Wasserman E.A., and Jensen D.D. Olfactory stimuli and the "pseudo-extinction" effect. Science 166 (1969) 1307-1309
137. Watson J.B. Kinaesthetic and organic sensation: their role in interactions of the white rat to the maze. Psychol Rev Monogr Suppl. 8 33 (1907) 1-100
138. Weniger G., Ruhleder M., Wolf S., Lange C., and Irle E. Egocentric memory impaired and allocentric memory intact as assessed by virtual reality in subjects with unilateral parietal cortex lesions. Neuropsychologia 47 (2009) 59-69
139. Whishaw I.Q., and Tomie J.A. Of mice and mazes: similarities between mice and rats on dry land but not water maze. Physiol Behav 60 (1996) 1191-1197
140. Wolfer D.P., Stagljar-Bozicevic M., Errington M.L., and Lipp H.P. Spatial memory and learning in transgenic mice: fact or artifact?. News Physiol Sci 13 (1998) 118-123
141. Yamaki T., Murakami N., Iwamoto Y., Sakakibara T., Kobori N., Ueda S., et al. Cognitive dysfunction and histological findings in rats with chronic stage contusions and diffuse axonal injury. Brain Res Protocol 3 (1998) 100-106
142. Yonemori F., Yamada H., Yamaguchi A., Uemura A., and Tamura A. Spatial memory disturbance after focal cerebral ischemia in rats. J Cereb Blood Flow Metab 16 (1996) 973-980