Detailed analysis of the behavior and memory performance of middle-aged male and female CD-1 mice in a 3D maze

Behavioural Brain Research

Volumn 187, Issue 2, 2008, Pages 312-326

  Ennaceur, A ^a   Michalikova, S ^a   van Rensburg, R ^b   Chazot, P L ^b  

^a UNIVERSITY OF SUNDERLAND   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

Aging; Alzheimer's; Amnesia; Amygdala; Amyloid; Benzodiazepines; Hippocampus; Rats; Strains

Indexed keywords

ANALYTIC METHOD; ANIMAL EXPERIMENT; ARTICLE; BEHAVIORAL SCIENCE; COMPARATIVE STUDY; CONTROLLED STUDY; EMOTION; FEMALE; HABITUATION; MALE; MAZE TEST; MEMORY; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; TASK PERFORMANCE; WORKING MEMORY;

AGING; ANALYSIS OF VARIANCE; ANIMALS; CHOICE BEHAVIOR; DISCRIMINATION LEARNING; EXPLORATORY BEHAVIOR; FEMALE; MALE; MAZE LEARNING; MEMORY, SHORT-TERM; MICE; ORIENTATION; SEX FACTORS;

EID: 38049080523     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbr.2007.09.025     Document Type: Article

References (101)

1. Ennaceur A., Michalikova S., van Rensburg R., and Chazot P.L. Models of anxiety: responses of mice to novelty and open spaces in a 3D-maze. Behav Brain Res 174 (2006) 9-38
2. Ennaceur A, Michalikova S, van Rensburg R, Chazot PL. Are benzodiazepines really anxiolytics? Dogmas, popularity and scientific methods. Neuroscience Meeting Planner, Program No. 937.16. San Diego, CA: Society for Neuroscience; 2007 [online].
3. Michalikova S., Ennaceur A., van Rensburg R., and Chazot PL. Behavior and memory performance of middle-aged female CD1 mice in a 3D maze: effects of near infrared light. Neurobiol Learn Memory (2007) 10.1016/j.nlm.2007.07.014
4. Maita K., Hirano M., Harada T., Mitsumori K., Yoshida A., Takahashi K., et al. Mortality, major cause of moribundity, and spontaneous tumors in CD-1 mice. Toxicol Pathol 16 (1988) 340-349
5. Homburger F., Russfield A.B., Weisburger J.H., Lim S., Chak S.P., and Weisburger E.K. Aging changes in CD-1 HaM/ICR mice reared under standard Laboratory conditions. J Natl Cancer Inst 55 (1975) 37-45
6. Son W.C., and Gopinath C. Early occurrence of spontaneous tumors in CD-1 mice and Sprague-Dawley rats. Toxicol Pathol 32 (2004) 371-374
7. Son W.C. Factors contributory to early death of young CD-1 mice in carcinogenicity studies. Toxicol Lett 145 (2003) 88-98
8. Engelhardt J.A., Gries C.L., and Long G.G. Incidence of spontaneous neoplastic and nonneoplastic lesions in Charles River CD-1 mice varies with breeding origin. Toxicol Pathol 21 (1993) 538-541
9. Lavie L., and Weinreb O. Age- and strain-related changes in tissue transglutaminase activity in murine macrophages: the effects of inflammation and induction by retinol. Mech Ageing Dev 90 (1996) 129-143
10. Navarro A., Sanchez-del-Pino M.J., Gomez C., Peralta J.L., and Boveris A. Behavioral dysfunction, brain oxidative stress, and impaired mitochondrial electron transfer in aging mice. Am J Physiol Regul Integr Comp Physiol 282 (2002) R985-R992
11. Chandra M., and Frith C.H. Spontaneous neoplasms in aged CD-l mice. Toxicol Lett 61 (1992) 14-61
12. Ennaceur A., Michalikova S., Bradford A., and Ahmed S. Detailed analysis of the behavior of Lister and Wistar rats in anxiety, object recognition and object location tasks. Behav Brain Res 159 (2005) 247-266
13. Tolman E.C. The determiners of behavior at a choice point. Psychol Rev 46 (1938) 318-336
14. Tolman E.C. Prediction of vicarious trial and error by means of the schematic sowbug. Psychol Rev 46 (1939) 318-336
15. Bimonte H.A., and Denenberg V. Sex differences in vicarious trial-and-error behavior during radial arm maze learning. Physiol Behav 68 (2000) 495-499
16. Forster M.J., Dubey A., Dawson K.M., Stutts W.A., Lal H., and Sohal R.S. Age-related losses of cognitive function and motor skills in mice are associated with oxidative. PNAS 93 (1996) 4765-4769
17. 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
18. Benice T.S., Rizk A., Kohama S., Pfankuch T., and Raber J. Sex differences in age-related cognitive decline in C57BL/6J mice associated with increased brain microtubule-associated protein 2 and synaptohysin immunoreactivity. Neuroscience 137 (2006) 413-423
19. Astur R.S., Ortiz M.L., and Sutherland R.J. A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav Brain Res 93 (1998) 185-190
20. Astur R.S., Tropp J., Sava S., Constable R.T., and Markus E.J. Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behav Brain Res 151 (2004) 103-115
21. Berger-Sweeney J., Arnold A., Gabeau D., and Mills J. Sex differences in learning and memory in mice: effects of sequence of testing and cholinergic blockade. Behav Neurosci 109 (1995) 859-873
22. Bimonte H.A., Hyde L.A., Hoplight B.J., and Denenberg V.H. In two species, females exhibit superior working memory and inferior reference memory on the water radial-arm maze. Physiol Behav 70 (2000) 311-317
23. Dabbs J.M., Chang E.-L., Strong R.A., and Milun R. Spatial ability, navigation strategy, and geographic knowledge among men and women. Evol Hum Behav 19 (1998) 89-98
24. 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
25. 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
26. James T.W., and Kimura D. Sex differences in remembering the locations of objects in an array: location-shifts versus location exchanges. Evol Hum Behav 18 (1997) 155-163
27. 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
28. Jones C.M., Braithwaite V.A., and Healy S.D. The evolution of sex differences in spatial ability. Behav Neurosci 117 (2003) 403-411
29. McBurney D.H., Gaulin S.J.C., Devineni T., and Adams C. Superior spatial memory of women: stronger evidence for the gathering hypothesis. Evol Hum Behav 18 (1997) 165-174
30. Mishima N., Higashitani F., Teraoka K., and Yoshioka R. Sex differences in appetitive learning of mice. Physiol Behav 37 (1986) 263-268
31. Perrot-Sinal T.S., Kostenuik A.M., Ossenkopp K.P., and Kavaliers M. Sex differences in performance in the Morris water maze and the effects of initial nonstationary hidden platform training. Behav Neurosci 110 (1996) 1309-1320
32. Ricceri L., Colozza C., and Calamandrei G. Ontogeny of spatial discrimination in mice: a longitudinal analysis in the modified open-field with objects. Dev Psychobiol 37 (2000) 109-118
33. Roof R.L., and Stein D.G. Gender differences in Morris water maze performance depend on task parameters. Physiol Behav 68 (1999) 81-86
34. Veng L.M., Granholm A.C., and Rose G.M. Age-related sex differences in spatial learning and basal forebrain cholinergic neurons in F344 rats. Physiol Behav 80 (2003) 27-36
35. Bowman R.E., Maclusky N.J., Diaz S.E., Zrull M.C., and Luine V.N. Aged rats: sex differences and responses to chronic stress. Brain Res 1126 (2006) 156-166
36. Bucci D.J., Chiba A.A., and Gallagher M. Spatial learning in male and female Long-Evans rats. Behav Neurosci 109 (1995) 180-183
37. Driscoll I., Hamilton D.A., Yeo R.A., Brooks W.M., and Sutherland R.J. Virtual navigation in humans: the impact of age, sex, and hormones on place learning. Hormones Behav 47 (2005) 326-335
38. Einon D. Spatial memory and response strategies in rats: age, sex and rearing differences in performance. Q J Exp Psychol 32 (1980) 473-489
39. Galea L.A., Kavaliers M., and Ossenkopp K.P. Sexually dimorphic spatial learning in meadowvoles (Microtus pennsylvanicus) and deer mice (Peromyscus maniculatus). J Exp Biol 199 (1996) 195-200
40. Gresack J.E., and Frick K.M. Male mice exhibit better spatial working and reference memory than females in a water-escape radial arm maze task. Brain Res 982 (2003) 98-107
41. Kavaliers M., Ossenkopp K.P., Prato F.S., Innes D.G., Galea L.A., Kinsella D.M., et al. Spatial learning in deer mice: sex differences and the effects of endogenous opioids and 60 Hz magnetic fields. J Comp Physiol 179 (1996) 715-724
42. 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
43. Lacreuse A., Kim C.B., Rosene D.L., Killiany R.J., Moss M.B., Moore T.L., et al. Sex, age, and training modulate spatial memory in the Rhesus monkey (Macaca mulatta). Behav Neurosci 119 (2005) 118-126
44. Moffat S.D., Hampson E., and Hatzipantelis M. Navigation in a "virtual" maze: sex differences and correlation with psychometric measures of spatial ability in humans: evolution and human behavior. Evol Hum Behav 19 (1998) 73-87
45. Roof R.L. Neonatal exogenous testosterone modifies sex differences in radial arm and Morris water maze performance in prepubescent and adult rats. Behav Brain Res 53 (1993) 1-10
46. Sanders B., Soares M.P., and D'Aquila J.M. The sex difference on one test of spatial visualization: a nontrivial difference. Child Dev 53 (1982) 1106-1110
47. Sandstrom N.J., Kaufman J., and Huettel S.A. Males and females use different distal cues in a virtual environment navigation task. Cogn Brain Res 6 (1998) 351-360
48. Williams C.L., Barnett A.M., and Meck W.H. Organizational effects of early gonadal secretions on sexual differentiation in spatial memory. Behav Neurosci 104 (1990) 84-97
49. Chen G.H., Wang Y.J., Zhang L.Q., and Zhou J.N. Age- and sex-related disturbance in a battery of sensorimotor and cognitive tasks in Kunming mice. Physiol Behav 83 (2004) 531-541
50. Driscoll I., Hamilton D.A., Petropoulos H., Yeo R.A., Brooks W.M., Baumgartner R.N., et al. The aging hippocampus: cognitive, biochemical and structural findings. Cereb Cortex 13 (2003) 1344-1351
51. Elias M.F., and Kinsbourne M. Age and sex differences in the processing of verbal and nonverbal stimuli. J Gerontol 29 (1974) 162-171
52. Foster T.C., Sharrow K.M., Kumar A., and Masse J. Interaction of age and chronic estradiol replacement on memory and markers of brain aging. Neurobiol Aging 24 (2003) 839-852
53. Grootendorst J., Enthoven L., Dalm S., de Kloet E.R., and Oitzl M.S. Increased corticosterone secretion and early-onset of cognitive decline in female apolipoprotein E-knockout mice. Behav Brain Res 148 (2004) 167-177
54. Markowska A.L. Sex dimorphisms in the rate of age-related decline in spatial memory: relevance to alterations in the estrous cycle. J Neurosci 19 (1999) 8122-8133
55. Small G.W., La Rue A., Komo S., Kaplan A., and Mandelkern M.A. Predictors of cognitive change in middle-aged and older adults with memory loss. Am J Psychiatry 152 (1995) 1757-1764
56. Barrett-Connor E., and Kritz-Silverstein D. Gender differences in cognitive function with age: the Rancho Bernardo study. J Am Geriatr Soc 47 (1999) 159-164
57. Elias M.F., Elias P.K., D'Agostino R.B., Silbershatz H., and Wolf P.A. Role of age, education, and gender on cognitive performance in the Framingham heart study: community-based norms. Exp Aging Res 23 (1997) 201-235
58. Lacreuse A., Herndon J.G., Killiany R., Rosene D.L., and Moss M.B. Spatial cognition in rhesus monkeys: male superiority declines with age. Hormones Behav 36 (1999) 70-76
59. Meyer J.S., Rauch G.M., Crawford K., Rauch R.A., Konno S., Akiyama H., et al. Risk factors accelerating cerebral degenerative changes, cognitive decline and dementia. Int J Geriatr Psychiatry 14 (1999) 1050-1061
60. van Exel E., Gussekloo J., de Craen A.J., Bootsma-van der Wiel A., Houx P., Knook D.L., et al. Cognitive function in the oldest old: women perform better than men. J Neurol Neurosurg Psychiatry 71 (2001) 29-32
61. Wiederholt W.C., Cahn D., Butters N.M., Salmon D.P., Kritz-Silverstein D., and Barrett-Connor E. Effects of age, gender and education on selected neuropsychological tests in an elderly community cohort. J Am Geriatr Soc 41 (1993) 639-647
62. Barnes L.L., Wilson R.S., Schneider J.A., Bienias J.L., Evans D.A., and Bennett D.A. Gender, cognitive decline, and risk of AD in older persons. Neurology 60 (2003) 1777-1781
63. Maitland S.B., Intrieri R.C., Schaie K.W., and Willis S.L. Gender differences and changes in cognitive abilities across the adult life span. Aging Neuropsychol Cogn 7 (2000) 32-53
64. Singer T., Verhaeghen P., Ghisletta P., Lindenberger U., and Baltes P.B. The fate of cognition in very old age: six-year longitudinal findings in the Berlin Aging Study (BASE). Psychol Aging 18 (2003) 318-331
65. Gage F.H., Dunnett S.B., and Bjorklund A. Spatial learning and motor deficits in aged rats. Neurobiol Aging 5 (1984) 43-48
66. Ingram D.K., London E.D., and Goodrick C.L. Age and neurochemical correlates of radial maze performance in rats. Neurobiol Aging 2 (1981) 41-47
67. Lamberty Y., and Gower A.J. Spatial processing and emotionality in aged NMRI mice: a multivariate analysis. Physiol Behav 54 (1993) 339-343
68. Sprott R.L., and Eleftheriou B.E. Open-field behavior in aging inbred mice. Gerontologia 20 (1974) 155-162
69. Moffat S.D., Zonderman A.B., and Resnick S.M. Age differences in spatial memory in a virtual environment navigation task. Neurobiol Aging 22 (2001) 787-796
70. Sjölinder M., Höök K., Nilsson L.G., and Andersson G. Age differences and the acquisition of spatial knowledge in a three-dimensional environment: evaluating the use of an overview map as a navigation aid. Int J Hum Computer Studies 63 (2005) 537-564
71. Brown M.F. Effects of maze arm length on performance in the radial-arm maze. Anim Learn Behav 18 (1990) 13-22
72. Dale R.H.I., and Innis N.K. Interactions between response stereotypy and memory strategies on the eight-arm radial maze. Learn Motiv 24 (1993) 23-29
73. 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
74. Ennaceur A. Effects of lesions of the substantia innominata/ventral pallidum, globus pallidus and medial septum in object recognition and radial-maze tasks: physostigmine and amphetamine treatments. Pharmacol Res 38 (1998) 251-263
75. Yoerg S.I., and Kamil A.C. Response strategies in the radial arm maze: running around in circles. Anim Learn Behav 10 (1982) 530-534
76. Sherrick M.F., Brunner R.L., Roth T.G., and Dember W.N. Rats' sensitivity to their direction of movement and spontaneous alternation behavior. Q J Exp Psychol 31 (1979) 83-93
77. Pico R.M., and Davis J.L. The radial maze performance of mice: assessing the dimensional requirements for serial order memory in animals. Behav Neural Biol 40 (1984) 5-26
78. Salthouse T.A. Adult cognition: an experimental psychology of human aging (1982), Springer, New York
79. Salthouse T.A. Theoretical perspectives on cognitive aging (1991), Lawrence Erlbaum Associates, Hillsdale, NJ
80. Chandra M., and Frith C.H. Spontaneous renal lesions in CD-1 and B6C3F1 mice. Exp Toxicol Pathol 46 (1994) 189-198
81. Mizumori S.J.Y., Rosenzweig M.R., and Kermisch M.G. Failure of mice to demonstrate spatial memory in the radial maze. Behav Neural Biol 35 (1982) 33-45
82. Muenzinger K. Vicarious trial and error at a point of choice: A general survey of its relation of learning efficiency. J Genet Psychol 53 (1938) 75-86
83. Czaja S.J. Aging and the acquisition of computer skills. In: Rogers W.A., Fisk A.D., and Walker N. (Eds). Aging and Skilled Performance - Advances in Theory and Applications (1996), Lawrence Erlbaum Associates, Hillsdale, NJ pp. 201-220
84. Brayne C., Gill C., Paykel E.S., Huppert F., and O'Connor D.W. Cognitive decline in an elderly population-A two wave study of change. Psycholo Med 25 (1995) 673-683
85. Francia N., Cirulli F., Chiarotti F., Antonelli A., Aloe L., and Alleva E. Spatial memory deficits in middle-aged mice correlate with lower exploratory activity and a subordinate status: role of hippocampal neurotrophins. Eur J Neurosci 23 (2006) 711-728
86. Frith C.H., and Chandra M. Incidence, distribution, and morphology of amyloidosis in Charles Rivers CD-1 mice. Toxicol Pathol 19 (1991) 123-127
87. Gruys E., Tooten P.C., and Kuijpers M.H. Lung, ileum and heart are predilection sites for AApoAII amyloid deposition in CD-1 Swiss mice used for toxicity studies. Pulmonary amyloid indicates AApoAII. Lab Anim 30 (1996) 28-34
88. Ison J.R., Bowen G.P., and del Cerro M. A Behavioral Study of Temporal Processing and Visual Persistence in Young and Aged Rats. Behav Neurosci 112 (1998) 1273-1279
89. Kirasic K.C. Spatial cognition and behavior in young and elderly adults: implications for learning new environments. Psychol Aging 6 (1991) 10-18
90. Lachenmayr B.J., Kojetinsky S., Oslermaier N., Angstwurm K., Vivell P.M., and Schaumberger M. The different effects of aging on normal sensitivity in flicker and light-sense perimetry. Invest Ophth Vis Sci 35 (1994) 2741-2748
91. Levy L.J., Astur R.S., and Frick K.M. Men and women differ in object memory but not performance of a virtual radial maze. Behav Neurosci 119 (2005) 853-862
92. Light L.L., and Zelinski E. Memory for spatial information in young and old adults. Dev Psychol 19 (1983) 901-906
93. Magnusson K.A., Scruggs B., Aniya J., Wright K.C., Ontl T., Xing Y., and Bai L. Age-related deficits in mice performing working memory tasks in a water maze. Behav Neurosci 117 (2003) 485-495
94. Majeed S.K. Survey on spontaneous systemic amyloidosis in aging mice. Arzneimittelforschung 43 (1993) 170-178
95. McDowd J.M., and Shaw R.J. Attention and aging: a functional perspective. In: Craik F.I.M., and Salthouse T.A. (Eds). The Handbook of Aging and Cognition (2000), Lawrence Erlbaum Associates, Hillsdale, NJ pp. 221-292
96. Meinz E.J., and Salthouse T.A. Is age kinder to females than to males?. Psychon B Review 5 (1998) 56-70
97. Nilsson L.-G., Backman L., Erngrund K., Nyberg L., Adolfsson R., Bucht R., Karlsson S., Widing M., and Winblad B. The betula prospective cohort study: memory, health and aging. Aging Neuropsychol C 1 (1997) 1-32
98. Prince M., Lewis G., Bird A., Blizard R., and Mann A. A longitudinal study of factors predicting change in cognitive test scores over time, in an older hypertensive population. Psychol Med 26 (1996) 555-568
99. Verbitsky M., Yonan A.L., Malleret G., Kandel E.R., Gilliam T.C., and Pavlidid P. Altered hippocampal transcript profile accompanies an age-related spatial memory deficit in mice. Learn Mem 11 (2004) 253-260
100. Vicens P., Bernal M.C., Carrasco M.C., and Redolat R. Previous training in the water maze: differential effects in NMRI and C57BL mice. Physiol Behav 67 (1999) 197-203
101. Vicens P., Redolt R., and Carrasco M.C. Effects of early spatial training on water performance: a longitudinal study in mice. Exp Gerontol 37 (2002) 575-581