Assessing spatial learning and memory in rodents

ILAR Journal

Volumn 55, Issue 2, 2014, Pages 310-332

  Vorhees, Charles V ^a   Williams, Michael T ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RODENTIA;

ANIMAL; ASSOCIATION; BRAIN; MAZE TEST; MEMORY; MOUSE; ORIENTATION; PHYSIOLOGY; RAT; SPATIAL LEARNING;

ANIMALS; BRAIN; CUES; MAZE LEARNING; MEMORY; MICE; ORIENTATION; RATS; SPATIAL LEARNING;

EID: 84911461416     PISSN: 10842020     EISSN: 19306180     Source Type: Journal    
DOI: 10.1093/ilar/ilu013     Document Type: Article

References (142)

1. Alamed J,Wilcock DM, Diamond DM, Gordon MN, Morgan D. 2006. Twoday radial-arm water maze learning and memory task; robust resolution of amyloid-related memory deficits in transgenic mice. Nat Protoc 1:1671-1679.
2. Anisman H, Merali Z. 2001. Rodent models of depression: learned helplessness induced in mice. Curr Protoc Neurosci Chapter 8:Unit 8.10C.
3. Armario A, Jolin T. 1986. Effects of water restriction on circadian rhythms of corticosterone, growth hormone and thyroid stimulating hormone in adult male rats. Physiol Behav 38:327-330.
4. Baldi E, Efoudebe M, Lorenzini CA, Bucherelli C. 2005. Spatial navigation in the Morris water maze: working and long lasting reference memories. Neurosci Lett 378:176-180.
5. Bannerman DM, Good MA, Butcher SP, Ramsay M, Morris RGM. 1995. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 378:182-186.
6. Barnes CA, Suster MS, Shen J, McNaughton BL. 1997. Multistability of cognitive maps in the hippocampus of old rats. Nature 388:272-275.
7. Barrett RJ, Leith NJ, Ray OS. 1973. A behavioral and pharmacological analysis or variables mediating active avoidance behavior in rats. J Comp Physiol Psychol 82:489-500.
8. Barrett RJ, Leith NJ, Ray OS. 1974. An analysis of the facilitation of avoidance acquisition produced by d-amphetamine and scopolamine. Behav Biol 11:189-203.
9. Bimonte HA, Hyde LA, Hoplight BJ, Denenberg VH. 2000. In two species, females exhibit superior working memory and inferior reference memory on the water radial-arm maze. Physiol Behav 70:311-317.
10. Bliss TV, Lomo T. 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331-356.
11. Blokland A, Geraerts E, Been M. 2004. A detailed analysis of rats' spatial memory in a probe trial of a Morris task. Behav Brain Res 154:71-75.
12. Brandeis R, Brandys Y, Yehuda S. 1989. The use of the Morris water maze in the study of memory and learning. Int J Neurosci 48:29-69.
13. Brun VH, Solstad T, Kjelstrup KB, Fyhn M, Witter MP, Moser EI, Moser MB. 2008. Progressive increase in grid scale from dorsal to ventral medial entorhinal cortex. Hippocampus 18:1200-1212.
14. Burgess N, Maguire EA, O'Keefe J. 2002. The human hippocampus and spatial and episodic memory. Neuron 35:625-641.
15. Buzsaki G, Moser EI. 2013. Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130-138.
16. Cain DP. 1997. LTP, NMDA, genes and learning. Curr Opin Neurobiol 7:235-242.
17. Cain DP, Saucier D. 1996. The neuroscience of spatial navigation: Focus on behavior yields advances. Rev Neurosci 7:215-231.
18. Cain DP, Saucier D, Hall J, Hargreaves EL, Boon F. 1996. Detailed behavioral analysis of water maze acquisition under APVor CNQX: Contribution of sensorimotor disturbances to drug-induced acquisition deficits. Behav Neurosci 110:86-102.
19. Carman HM, Mactutus CF. 2002. Proximal versus distal cue utilization in spatial navigation: the role of visual acuity? Neurobiol Learn Mem 78:332-346.
20. Caul WF, Barrett RJ. 1973. Shuttle-box versus Y-maze avoidance: value of multiple response measures in interpreting active-avoidance performance of rats. J Comp Physiol Psychol 84:572-578.
21. Clapcote SJ, Lazar NL, Bechard AR,Wood GA, Roder JC. 2005. NIH Swiss and Black Swiss mice have retinal degeneration and performance deficits in cognitive tests. Comp Med 55:310-316.
22. Clark RE, Broadbent NJ, Squire LR. 2007. The hippocampus and spatial memory: Findings with a novel modification of the water maze. J Neurosci 27:6647-6654.
23. Commins S, Cunningham L, Harvey D, Walsh D. 2003. Massed but not spaced training impairs spatial memory. Behav Brain Res 139:215-223.
24. Coover GD, Murison R, Sundberg H, Jellestad F, Ursin H. 1984. Plasma corticosterone and meal expectancy in rats: effects of low probability cues. Physiol Behav 33:179-184.
25. Couzin-Frankel J. 2013. When mice mislead. Science 342:922-925.
26. Crabbe JC, Wahlsten D, Dudek BC. 1999. Genetics of mouse behavior: Interactions with laboratory environment. Science 284:1670-1672.
27. Cravens RW. 1974. Effects of maternal undernutrition on offspring behavior: Incentive value of a food reward and ability to escape from water. Dev Psychobiol 7:61-69.
28. D'Hooge R, De Deyn PP. 2001. Applications of the Morris water maze in the study of learning and memory. Brain Res Rev 36:60-90.
29. Daily JL, Nash K, Jinwal U, Golde T, Rogers J, Peters MM, Burdine RD, Dickey C, Banko JL,Weeber EJ. 2011. Adeno-associated virus-mediated rescue of the cognitive defects in a mouse model for Angelman syndrome. PLoS One 6:e27221.
30. Dalm S, Grootendorst J, De Kloet ER, Oitzl MS. 2000. Quantification of swim patterns in the Morris water maze. Behav Res Methods Instrum Comput 32:134-139.
31. Devan BD, McDonald RJ, White NM. 1999. Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: Relation to thigmotaxis. Behav Brain Res 100:5-14.
32. Dubreuil D, Tixier C, Dutrieux G, Edeline JM. 2003. Does the radial arm maze necessarily test spatial memory? Neurobiol Learn Mem 79:109-117.
33. Etienne AS. 1992. Navigation of a small mammal by dead reckoning and local cues. Curr Dir Psychol Sci 1:48-52.
34. Food and Drug Administration. 2007. Guidance for Industry and Other Stakeholders Toxicological Principles for the Safety Assessment of Food Ingredients Redbook 2000. College Park MD: US Department of Health and Human Services.
35. Fouquet C, Babayan BM,Watilliaux A, Bontempi B, Tobin C, Rondi-Reig L. 2013. Complementary roles of the hippocampus and the dorsomedial striatum during spatial and sequence-based navigation behavior. PLoS One 8:e67232.
36. Gad SC. 2009. Drug safety evaluation. Hoboken NJ: John Wiley & Sons.
37. Gallagher M, Burwell R, Burchinal M. 1993. Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behav Neurosci 107:618-626.
38. Garcia-Belenguer S, Oliver C, Mormede P. 1993. Facilitation and feedback in the hypothalamo-pituitary-adrenal axis during food restriction in rats. J Neuroendocrinol 5:663-668.
39. Hafting T, Fyhn M, Molden S, Moser MB, Moser EI. 2005. Microstructure of a spatial map in the entorhinal cortex. Nature 436:801-806.
40. Hamilton DA, Akers KG, Weisend MP, Sutherland RJ. 2007. How do room and apparatus cues control navigation in the Morris water task? Evidence for distinct contributions to a movement vector. J Exp Psychol Anim Behav Process 33:100-114.
41. Harrison FE, Hosseini AH, McDonald MP. 2009. Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks. Behav Brain Res 198:247-251.
42. Heiderstadt KM, McLaughlin RM, Wright DC, Walker SE, Gomez-Sanchez CE. 2000. The effect of chronic food and water restriction on open-field behaviour and serum corticosterone levels in rats. Lab Anim 34:20-28.
43. Henry M, Beguin M, Requier F, Rollin O, Odoux JF, Aupinel P, Aptel J, Tchamitchian S, Decourtye A. 2012. A common pesticide decreases foraging success and survival in honey bees. Science 336:348-350.
44. Heys JG, MacLeod KM, Moss CF, Hasselmo ME. 2013. Bat and rat neurons differ in theta-frequency resonance despite similar coding of space. Science 340:363-367.
45. Hodges H. 1996. Maze procedures: The radial-arm and water maze compared. Cog Brain Res 3:167-181.
46. Hoh T, Beiko J, Boon F,Weiss S, Cain DP. 1999. Complex behavioral strategy and reversal learning in the water maze without NMDA receptordependent long-term potentiation. J Neurosci 19:RC2.
47. Hoh TE, Cain DP. 1997. Fractionating the nonspatial pretraining effect in the water maze task. Behav Neurosci 111:1285-1291.
48. Hollup SA, Molden S, Donnett JG, Moser M-B, Moser EI. 2001. Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J Neurosci 21:1635-1644.
49. Holscher C. 1999. Stress impairs performance in spatial watermaze learning tasks. Behav Brain Res 100:225-235.
50. Holson RR, Pearce B. 1992. Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species. Neurotoxicol Teratol 14:221-228.
51. Honma K, Honma S, Hirai T, Katsuno Y, Hiroshige T. 1986. Food ingestion is more important to plasma corticosterone dynamics than water intake in rats under restricted daily feeding. Physiol Behav 37: 791-795.
52. Johansson A, Fredriksson R, Winnergren S, Hulting AL, Schioth HB, Lindblom J. 2008. The relative impact of chronic food restriction and acute food deprivation on plasma hormone levels and hypothalamic neuropeptide expression. Peptides 29:1588-1595.
53. Jonasson Z. 2005. Meta-analysis of sex differences in rodent models of learning and memory: A review of behavioral and biological data. Neurosci Biobehav Rev 28:811-825.
54. Kjelstrup KB, Solstad T, Brun VH, Hafting T, Leutgeb S, Witter MP, Moser EI, Moser MB. 2008. Finite scale of spatial representation in the hippocampus. Science 321:140-143.
55. Lazic SE, Essioux L. 2013. Improving basic and translational science by accounting for litter-to-litter variation in animal models. BMC Neurosci 14:37.
56. Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, Moser MB. 2005a. Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309:619-623.
57. Leutgeb S, Leutgeb JK, Moser MB, Moser EI. 2005b. Place cells, spatial maps and the population code for memory. Curr Opin Neurobiol 15:738-746.
58. Lindner MD, Ribkoff VK. 1991. Relationship between performance in the Morris water task, visual acuity, and thermoregulatory function in aged F-344 rats. Behav Brain Res 45:45-55.
59. Lipp HP, Wolfer DP. 1998. Genetically modified mice and cognition. Curr Opin Neurobiol 8:272-280.
60. Maaswinkel H, Whishaw IQ. 1999. Homing with locale, taxon, and dead reckoning strategies by foraging rats: sensory hierarchy in spatial navigation. Behav Brain Res 99:143-152.
61. Mactutus CF, Booze RM. 1994. Accuracy of spatial navigation: The role of platform and tank size. Soc Neurosci Abst 20:1014.
62. Maei HR, Zaslavsky K, Teixeira CM, Frankland PW. 2009. What is the most sensitive measure of water maze probe test performance? Front Integr Neurosci 3:4.
63. Malenka RC, Nicoll RA. 1999. Long-term potentiation-A decade of progress? Science 285:1870-1874.
64. Marinkovic P, Pesic V, Loncarevic N, Smiljanic K, Kanazir S, Ruzdijic S. 2007. Behavioral and biochemical effects of various food-restriction regimens in the rats. Physiol Behav 92:492-499.
65. Markowska AL, Long JM, Johnson CT, Olton DS. 1993. Variable-interval probe test as a tool for repeated measurements of spatial memory in the water maze. Behav Neurosci 107:627-632.
66. Maurer R, Derivaz V. 2000. Rats in a transparent morris water maze use elemental and configural geometry of landmarks as well as distance to the pool wall. Spatial Cogn Comput 2:135-156.
67. Maviel T, Durkin TP, Menzaghi F, Bontempi B. 2004. Sites of neocortical reorganization critical for remote spatial memory. Science 305:96-99.
68. McDonald RJ, White NM. 1994. Parallel information processing in the water maze: Evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol 61:260-270.
69. McNamara RK, Skelton RW. 1993. The neuropharmacological and neurochemical basis of place learning in the Morris water maze. Brain Res Rev 18:33-49.
70. Means LW, Alexander SR, O'Neal MF. 1992. Those cheating rats: Male and female rats use odor trails in a water-escape "working memory" task. Behav Neural Biol 58:144-151.
71. Menzel R, Geiger K, Joerges J, Muller U, Chittka L. 1998. Bees travel novel homeward routes by integrating separately acquired vector memories. Anim Behav 55:139-152.
72. Miller JF, Neufang M, Solway A, Brandt A, Trippel M, Mader I, Hefft S, Merkow M, Polyn SM, Jacobs J, Kahana MJ, Schulze-Bonhage A. 2013. Neural activity in human hippocampal formation reveals the spatial context of retrieved memories. Science 342:1111-1114.
73. Morford LL, Inman-Wood SL, Gudelsky GA, Williams MT, Vorhees CV. 2002. Impaired spatial and sequential learning in rats treated neonatally with d-fenfluramine. Eur J Neurosci 16:491-500.
74. Morris R. 1984. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Methods 11:47-60.
75. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 297:681-683.
76. Morris RGM. 1981. Spatial localization does not require the presence of local cues. Learn Motiv 12:239-260.
77. Morris RGM. 1993. An attempt to dissociate "spatial-mapping" and "working-memory" theories of hippocampal function. In: Seifert W, ed. Neurobiology of the Hippocampus. New York: Academic Press. p 405-432.
78. Morris RGM, Anderson E, Lynch GS, Baudry M. 1986. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate antagonist, AP5. Nature 329:774-776.
79. Morris RGM, Hagan JJ, Rawlins JNP. 1986. Allocentric spatial learning by hippocampectomized rats: A further test of the "spatial mapping" and "working memory" theories of hippocampal function.Quart J Exp Psychol 38B:365-395.
80. Morris RGM, Schenk F, Jarrard LE. 1990. Ibotenate lesions of hippocampus and/or subiculum: Dissociating components of allocentric spatial learning. Eur J Neurosci 2:1016-1028.
81. Moser EI, Krobert KA, Moser M-B, Morris RGM. 1998. Impaired spatial learning after saturation of long-term potentiation. Science 281:2038-2042.
82. Nguyen PV, Abel T, Kandel ER, Bourtchouladze R. 2000. Strain-dependent differences in LTP and hippocampus-dependent memory in inbred mice. Learn Mem 7:170-179.
83. O'Keefe J, Nadal L. 1978. The Hippocampus as a Cognitive Map. Oxford: Oxford University Press.
84. Olton DS, Samuelson RJ. 1976. Remembrance of places passed: Spatial memory in rats. J Exp Psychol Anim Behav Processes 2:97-116.
85. Packard MG, McGaugh JL. 1992. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems. Behav Neurosci 106:439-446.
86. Paquette C, Franzen E, Jones GM, Horak FB. 2011. Walking in circles: navigation deficits from Parkinson's disease but not from cerebellar ataxia. Neuroscience 190:177-183.
87. Park KE, Telugu BP. 2013. Role of stem cells in large animal genetic engineering in the TALENs-CRISPR era. Reprod Fertil Dev 26:65-73.
88. Penner MR, Mizumori SJ. 2012. Neural systems analysis of decision making during goal-directed navigation. Prog Neurobiol 96:96-135.
89. Pesic V, Marinkovic P, Janac B, Ignjatovic S, Popic J, Kanazir S, Ruzdijic S. 2010. Changes of behavioral parameters during long-term food restriction in middle-aged Wistar rats. Physiol Behav 101:672-678.
90. Porsolt RD, Anton G, Blavet N, Jalfre M. 1978. Behavioural despair in rats: A new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379-391.
91. Porsolt RD, Bertin A, Jalfre M. 1977. Behavioural despair in mice: A primary screening test for antidepressants. Arch Int Pharmacodyn 229:327-336.
92. Porsolt RD, LePichon M, Jalfre M. 1977. Depression: A new animal model sensitive to antidepressant treatments. Nature 226:730-731.
93. Post AM, Wultsch T, Popp S, Painsipp E, Wetzstein H, Kittel-Schneider S, Sontag TA, Lesch KP, Reif A. 2011. The COGITAT holeboard system as a valuable tool to assess learning, memory and activity in mice. Behav Brain Res 220:152-158.
94. Rauch TM, Welch DI, Gallego L. 1989a. Hyperthermia impairs retrieval of an overtrained spatial task in the Morris water maze. Behav Neural Biol 52:321-330.
95. Rauch TM,Welch DI, Gallego L. 1989b. Hypothermia impairs performance in the Morris water maze. Physiol Behav 45:315-320.
96. Ray OS, Barrett RJ. 1975. Behavioral, pharmacological, and biochemical analysis of genetic differences in rats. Behav Biol 15:391-417.
97. Rondi-Reig L, Petit GH, Tobin C, Tonegawa S, Mariani J, Berthoz A. 2006. Impaired sequential egocentric and allocentric memories in forebrain-specific-NMDA receptor knock-out mice during a new task dissociating strategies of navigation. J Neurosci 26:4071-4081.
98. Rudy JW, Paylor R. 1988. Reducing the temporal demands of the Morris place-learning task fails to ameliorate the place-learning impairment of preweanling rats. Psychobiology 16:152-156.
99. Rudy JW, Stadler-Morris S, Albert P. 1987. Ontogeny of spatial navigation behaviors in the rat: Dissociation of "proximal" and "distal"-cue-based behaviors. Behav Neurosci 101:62-73.
100. Sampson TR,Weiss DS. 2014. Exploiting CRISPR/Cas systems for biotechnology. Bioessays 36:34-38.
101. Saucier D, Hargreaves EL, Boon F, Vanderwolf CH, Cain DP. 1996. Detailed behavioral analysis of water maze acquisition under systemic NMDA or muscarinic antagonism: Nonspatial pretraining eliminates spatial learning deficits. Behav Neurosci 110:103-116.
102. Schaefer TL, Lingrel JB, Moseley AE, Vorhees CV, Williams MT. 2011. Targeted mutations in the Na,K-ATPase alpha 2 isoform confer ouabain resistance and result in abnormal behavior in mice. Synapse 65:520-531.
103. Schaefer TL, Vorhees CV, Williams MT. 2009. Mouse plasmacytomaexpressed transcript 1 knock out induced 5-HT disruption results in a lack of cognitive deficits and an anxiety phenotype complicated by hypoactivity and defensiveness. Neuroscience 164:1431-1443.
104. Schenk F. 1985. Development of place navigation in rats from weaning to puberty. Behav Neural Biol 43:69-85.
105. Scott S, Kranz JE, Cole J, Lincecum JM, Thompson K, Kelly N, Bostrom A, Theodoss J, Al-Nakhala BM, Vieira FG, Ramasubbu J, Heywood JA. 2008. Design, power, and interpretation of studies in the standard murine model of ALS. Amyotroph Lateral Scler 9:4-15.
106. Sharma S, Rakoczy S, Brown-Borg H. 2010. Assessment of spatial memory in mice. Life Sci 87:521-536.
107. Sherrill KR, Erdem UM, Ross RS, Brown TI, Hasselmo ME, Stern CE. 2013. Hippocampus and retrosplenial cortex combine path integration signals for successful navigation. J Neurosci 33:19304-19313.
108. Shrager Y, Kirwan CB, Squire LR. 2008. Neural basis of the cognitive map: path integration does not require hippocampus or entorhinal cortex. Proc Natl Acad Sci U S A 105:12034-12038.
109. Silva AJ, Paylor R,Wehner JM, Tonegawa S. 1992. Impaired spatial learning in a-calcium-calmodulin kinase II mutant mice. Science 257:206-211.
110. Skelton MR, Schaefer TL, Graham DL, deGrauw TJ, Clark JF,Williams MT, Vorhees CV. 2011. Creatine transporter (CrT; Slc6a8) knockout mice as a model of human CrT deficiency. PLoS One 6:e16187.
111. Skelton MR, Williams MT, Schaefer TL, Vorhees CV. 2007. Neonatal (+)-methamphetamine increases brain derived neurotrophic factor, but not nerve growth factor, during treatment and results in long-term spatial learning deficits. Psychoneuroendocrinology 32:734-745.
112. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI. 2008. Representation of geometric borders in the entorhinal cortex. Science 322: 1865-1868.
113. Stackman RW Jr, Lora JC, Williams SB. 2012. Directional responding of C57BL/6J mice in the Morris water maze is influenced by visual and vestibular cues and is dependent on the anterior thalamic nuclei. J Neurosci 32:10211-10225.
114. Stewart CA, Morris RGM. 1993. The watermaze. In: Sahgal A, ed. Behavioural Neuroscience, Volume I, A Practical Approach. Oxford: IRL Press at Oxford University Press. p 107-122.
115. Suh J, Rivest AJ, Nakashiba T, Tominaga T, Tonegawa S. 2011. Entorhinal cortex layer III input to the hippocampus is crucial for temporal association memory. Science 334:1415-1420.
116. Sung JY, Goo JS, Lee DE, Jin DQ, Bizon JL, Gallagher M, Han JS. 2008. Learning strategy selection in the water maze and hippocampal CREB phosphorylation differ in two inbred strains of mice. Learn Mem 15:183-188.
117. Tees RC, Buhrmann K, Hanley J. 1990. The effect of early experience on water maze spatial learning and memory in rats. Dev Psychobiol 23:427-439.
118. Tonkiss J, Shultz P, Galler JR. 1992. Long-Evans and Sprague-Dawley rats differ in their spatial navigation performance during ontogeny and at maturity. Dev Psychobiol 25:567-579.
119. Tyl RW, Marr MC. 2012. Developmental toxicity testing-Methodology. In: Hood RD, ed. Developmental and Reproductive Toxicology: A Practical Approach. New York: Informa Healthcare. p 129-183.
120. Upchurch M, Wehner JM. 1988. Differences between inbred strains of mice in Morris water maze performance. Behav Genet 18:55-68.
121. Van Dam D., Lenders G, De Deyn PP. 2006. Effect of Morris water maze diameter on visual-spatial learning in different mouse strains. Neurobiol Learn Mem 85:164-172.
122. van Strien NM, Cappaert NL,Witter MP. 2009. The anatomy of memory: An interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10:272-282.
123. Vorhees CV. 1987. Maze learning in rats: A comparison of performance in two water mazes in progeny prenatally exposed to different doses of phenytoin. Neurotoxicol Teratol 9:235-241.
124. Vorhees CV, Herring NR, Schaefer TL, Grace CE, Skelton MR, Johnson HL, Williams MT. 2008. Effects of neonatal (+)-methamphetamine on path integration and spatial learning in rats: effects of dose and rearing conditions. Int J Dev Neurosci 26:599-610.
125. Vorhees CV, Reed TM, Acuff-Smith KD, Schilling MA, Cappon GD, Fisher JE, Pu C. 1995. Long-term learning deficits and changes in unlearned behaviors following in utero exposure to multiple daily doses of cocaine during different exposure periods and maternal plasma cocaine concentrations. Neurotoxicol Teratol 17:253-264.
126. Vorhees CV, Schaefer TL, Skelton MR, Grace CE, Herring NR,WilliamsMT. 2009. (+/-)3,4-Methylenedioxymethamphetamine (MDMA) dosedependently impairs spatial learning in the morris water maze after exposure of rats to different five-day intervals from birth to postnatal day twenty. Dev Neurosci 31:107-120.
127. Vorhees CV, Skelton MR, Grace CE, Schaefer TL, Graham DL, Braun AA, Williams MT. 2009. Effects of (+)-methamphetamine on path integration and spatial learning, but not locomotor activity or acoustic startle, align with the stress hyporesponsive period in rats. Int J Dev Neurosci 27:289-298.
128. Vorhees CV,Weisenburger WP, Acuff-Smith KD, Minck DR. 1991. An analysis of factors influencing complex water maze learning in rats: Effects of task complexity, path order and escape assistance on performance following prenatal exposure to phenytoin. Neurotoxicol Teratol 13:213-222.
129. Vorhees CV, Williams MT. 2006. Morris water maze: Procedures for assessing spatial and related forms of learning and memory. Nat Protocols 1:848-858.
130. Wade SE, Maier SF. 1986. Effects of individual housing and stressor exposure upon the acquisition of watermaze escape. Learn Motiv 17:287-310.
131. Wahlsten D, Cooper SF, Crabbe JC. 2005. Different rankings of inbred mouse strains on the Morris maze and a refined 4-arm water escape task. Behav Brain Res 165:36-51.
132. Wenk GL. 2004. Assessment of spatial memory using the radial arm and Morris water maze. In: Crawley JN, Gerhardt GA, Rogawski MA, Sibley DR, Skolnick P, Wray S, eds. Current Protocols in Neuroscience. New York: Wiley Interscience. Unit 8.5A.
133. Whishaw IQ, Hines DJ, Wallace DG. 2001. Dead reckoning (path integration) requires the hippocampal formation: evidence from spontaneous exploration and spatial learning tasks in light (allothetic) and dark (idiothetic) tests. Behav Brain Res 127:49-69.
134. Whishaw IQ, Tomie J-A. 1997. Perseveration on place reversals in spatial swimming pool tasks: Further evidence for place learning in hippocampal rats. Hippocampus 7:361-370.
135. Whitlock JR, Heynen AJ, Shuler MG, Bear MF. 2006. Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097.
136. Williams MT, Braun AA, Amos-Kroohs R, McAllister JPI, Lindquist DM, Mangao FT, Vorhees CV, Yuan W. 2014. Kaolin-induced ventriculomegaly at weaning produces long-term learnng, memory, and motor deficits in rats. Int J Dev Neurosci 35:7-15.
137. Williams MT, Moran MS, Vorhees CV. 2004. Behavioral and growth effects induced by low dose methamphetamine administration during the neonatal period in rats. Int J Dev Neurosci 22:273-283.
138. Williams MT, Morford LL, Wood SL, Rock SL, McCrea AE, Fukumura M, Wallace TL, Broening HW,Moran MS, Vorhees CV. 2003. Developmental 3,4-methylenedioxymethamphetamine (MDMA) impairs sequential and spatial but not cued learning independent of growth, litter effects, or injection stress. Brain Res 968:89-101.
139. Williams MT, Morford LL, Wood SL, Wallace TL, Fukumura M, Broening HW, Vorhees CV. 2003. Developmental d-methamphetamine treatment selectively induces spatial navigation impairments in reference memory in the Morris water maze while sparing working memory. Synapse 48:138-148.
140. Williams MT, Vorhees CV, Boon F, Saber AJ, Cain DP. 2002. Methamphetamine exposure from postnatal days 11 to 20 causes impairments in both behavioral strategies and spatial learning in adult rats. Brain Res 958:312-321.
141. Wittlinger M,Wehner R,Wolf H. 2006. The ant odometer: Stepping on stilts and stumps. Science 312:1965-1967.
142. Yan HC, Cao X, Das M, Zhu XH, Gao TM. 2010. Behavioral animal models of depression. Neurosci Bull 26:327-337.