Tests to assess motor phenotype in mice: A user's guide

Nature Reviews Neuroscience

Volumn 10, Issue 7, 2009, Pages 519-529

  Brooks, Simon P ^a   Dunnett, Stephen B ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORDIAZEPOXIDE; LEVODOPA; PSYCHOTROPIC AGENT;

ANXIETY; AUDITORY RESPONSE; BEHAVIOR; BRAIN FUNCTION; CIRCADIAN RHYTHM; CLIMBING; CLINICAL ASSESSMENT; CLINICAL RESEARCH; DRUG INHIBITION; DYSKINESIA; GAIT; GRIP STRENGTH; INSTRUMENTAL CONDITIONING; LEARNING TEST; LIMB; LOCOMOTION; MOTOR CONTROL; MOTOR COORDINATION; MOTOR PERFORMANCE; MOUSE; NEUROLOGIC EXAMINATION; NONHUMAN; OPEN FIELD BEHAVIOR; OPEN FIELD TEST; PARKINSON DISEASE; PHENOTYPE; PRIORITY JOURNAL; RATING SCALE; RESPONSE TIME; REVIEW; ROTATION; SWIMMING; TASK PERFORMANCE; TEST RETEST RELIABILITY; TRANSGENIC ANIMAL; TREADMILL;

ANIMAL EXPERIMENTATION; ANIMALS; BEHAVIOR, ANIMAL; CIRCADIAN RHYTHM; DISEASE MODELS, ANIMAL; HUMANS; LOCOMOTION; MICE; MOTOR ACTIVITY; NERVOUS SYSTEM DISEASES; NEUROPSYCHOLOGICAL TESTS; PHENOTYPE; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY;

MUS;

EID: 67649506191     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2652     Document Type: Review

References (130)

1. Nolan, P. M. et al. A systematic, genome-wide, phenotype-driven mutagenesis programme for gene function studies in the mouse. Nature Genet. 25, 440-443 (2000).
2. Lalonde, R. & Strazielle, C. Spontaneous and induced mouse mutations with cerebellar dysfunctions: behavior and neurochemistry. Brain Res. 1140, 51-74 (2007).
3. Lalonde, R. & Strazielle, C. Motor performance and regional brain metabolism of spontaneous murine mutations with cerebellar atrophy. Behav. Brain Res. 125, 103-108 (2001).
4. Triarhou, L. C. Neural Transplantation in Cerebellar Ataxia (Landes, 1997).
5. McIlwain, K. L., Merriweather, M. Y., Yuva-Paylor, L. A. & Paylor, R. The use of behavioral test batteries: effects of training history. Physiol. Behav. 73, 705-717 (2001).
6. Carter, R. J. et al. Characterisation of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J. Neurosci. 19, 3248-3257 (1999).
7. Brooks, S. P., Pask, T., Jones, A. L. & Dunnett, S. B. Behavioural profiles of inbred mouse strains used as transgenic backgrounds. I: motor tests. Genes Brain Behav. 3, 206-215 (2004).
8. Crawley, J. N. & 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, 197-211 (1997).
9. Rogers, D. C. et al. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm. Genome 8, 711-713 (1997).
10. Irwin, S. Comprehensive observational assessment: Ia. A systematic, quantitative procedure for assessing the behavioral and physiologic state of the mouse. Psychopharmacologia 13, 222-257 (1968).
11. Rogers, D. C. 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, 207-217 (1999). This study demonstrated the sensitivity of the SHIRPA screen for characterizing different mouse lines.
12. Schallert, T. & Tillerson, J. L. in Central Nervous System Diseases: Innovative Animal Models from Lab to Clinic (eds Emerich, D. F., Dean, R. L. & Sanberg, P. R.) 131-151 (Humana, Totowa, New Jersey, 2000).
13. Cenci, M. A. & Lundblad, M. in Animal Models of Movement Disorders (ed. LeDoux, M.) 193-209 (Elsevier, Amsterdam, 2005).
14. Iancu, R., Mohapel, P., Brundin, P. & Paul, G. Behavioral characterization of a unilateral 6-OHDA-lesion model of Parkinson's disease in mice. Behav. Brain Res. 162, 1-10 (2005). This paper describes the unilateral 6-OHDA model of PD and various behavioural tests that have been used to characterize the lesion effects.
15. Cenci, M. A., Lee, C. S. & Björklund, A. L-DOPA-induced dyskinesia in the rat is associated with striatal overexpression of prodynorphin- and glutamic acid decarboxylase mRNA. Eur. J. Neurosci. 10, 2694-2706 (1998).
16. Steece-Collier, K. et al. Embryonic mesencephalic grafts increase levodopa-induced forelimb hyperkinesia in Parkinsonian rats. Mov. Disord. 18, 1442-1454 (2003).
17. Lane, E. L., Winkler, C., Brundin, P. & Cenci, M. A. The impact of graft size on the development of dyskinesia following intrastriatal grafting of embryonic dopamine neurons in the rat. Neurobiol. Dis. 22, 334-346 (2006).
18. Lundblad, M. et al. Pharmacological validation of a mouse model of l-DOPA-induced dyskinesia. Exp. Neurol. 194, 66-75 (2005).
19. Santini, E. et al. Critical involvement of cAMP/ DARPP-32 and extracellular signal-regulated protein kinase signaling in l-DOPA-induced dyskinesia. J. Neurosci. 27, 6995-7005 (2007).
20. Gold, S. J. et al. RGS9-2 negatively modulates l-3,4-dihydroxyphenylalanine-induced dyskinesia in experimental Parkinson's disease. J. Neurosci. 27, 14338-14348 (2007).
21. Glynn, D., Sizemore, R. J. & Morton, A. J. Early motor development is abnormal in complexin 1 knockout mice. Neurobiol. Dis. 25, 483-495 (2007).
22. Hickey, M. A. et al. Extensive early motor and nonmotor behavioral deficits are followed by striatal neuronal loss in knock-in Huntington's disease mice. Neuroscience 157, 280-295 (2008).
23. Lin, C. H. et al. Neurological abnormalities in a knockin mouse model of Huntington's disease. Hum. Mol. Genet. 10, 137-144 (2001).
24. Mangiarini, L. et al. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87, 493-506 (1996).
25. Barnéoud, P., Lolivier, J., Sanger, D. J., Scatton, B. & Moser, P. Quantitative motor assessment in FALS mice: a longitudinal study. Neuroreport 8, 2861-2865 (1997).
26. Ma, M., Basso, D. M., Walters, P., Stokes, B. T. & Jakeman, L. B. Behavioral and histological outcomes following graded spinal cord contusion injury in the C57Bl/6 mouse. Exp. Neurol. 169, 239-254 (2001).
27. de Visser, L., van den Boss, R., Kuurman, W. W., Kas, M. J. & Spruijt, B. M. Novel approach to the behavioural characterization of inbred mice: automated home cage observations. Genes Brain Behav. 5, 458-466 (2006). This paper describes how home cage monitoring systems can be used to produce a detailed analysis of mouse home cage activity.
28. Menalled, L. B. et al. Early motor dysfunction and striosomal distribution of huntingtin microaggregates in Huntington's disease knock-in mice. J. Neurosci. 22, 8266-8276 (2002).
29. Grusser, C. & Grusser-Cornehls, U. Improvement in motor performance of Weaver mutant mice following lesions of the cerebellum. Behav. Brain Res. 97, 189-194 (1998).
30. De Leonibus, E. et al. Spatial deficits in a mouse model of Parkinson disease. Psychopharmacology (Berl.) 194, 517-525 (2007).
31. Kas, M. J., de Mooij-van Malsen, A. J., Olivier, B., Spruijt, B. M. & Van Ree, J. M. Differential genetic regulation of motor activity and anxiety-related behaviors in mice using an automated home cage task. Behav. Neurosci. 122, 769-776 (2008).
32. Thifault, S., Lalonde, R., Sanon, N. & Hamet, P. Longitudinal analysis of motor activity and coordination, anxiety, and spatial learning in mice with altered blood pressure. Brain Res. 910, 99-105 (2001).
33. Brooks, S., Kaur, S., Starr, B. S. & Starr, M. S. Motor actions of eliprodil in the normal and monoaminedepleted mouse: a role in the treatment of Parkinson's disease? J. Neural Transm. 103, 737-748 (1996).
34. Drai, D., Kafkafi, N., Benjamini, Y., Elmer, G. & Golani, I. Rats and mice share common ethologically relevant parameters of exploratory behavior. Behav. Brain Res. 125, 133-140 (2001).
35. Hickey, M. A., Gallant, K., Gross, G. G., Levine, M. S. & Chesselet, M. F. Early behavioral deficits in R6/2 mice suitable for use in preclinical drug testing. Neurobiol. Dis. 20, 1-11 (2005).
36. Valentinuzzi, V. S. et al. Locomotor response to an open field during C57BL/56J active and inactive phases: differences dependent on conditions of illumination. Physiol. Behav. 69, 269-275 (2000).
37. Van Raamsdonk, J. M. et al. Phenotypic abnormalities in the YAC128 mouse model of Huntington disease are penetrant on multiple genetic backgrounds and modulated by strain. Neurobiol. Dis. 26, 189-200 (2007).
38. Harri, M. et al. Effect of access to a running wheel on behavior of C57BL/56J mice. Lab. Anim. Sci. 49, 401-405 (1999).
39. Kent, S., Hurd, M. & Satinoff, E. Interactions between body temperature and wheel running over the estrous cycle in rats. Physiol. Behav. 49, 1079-1084 (1991).
40. Salam, J. N. et al. Voluntary exercise in C57 mice is anxiolytic across several measures of anxiety. Behav. Brain Res. 197, 31-40 (2008).
41. Hastings, M. H., Maywood, E. S. & Reddy, A. B. Two decades of circadian time. J. Neuroendocrinol. 20, 812-819 (2008).
42. Morton, A. J. et al. Disintegration of the sleep-wake cycle and circadian timing in Huntington's disease. J. Neurosci. 25, 157-163 (2005).
43. Dell'Omo, G. et al. Early behavioural changes in mice infected with BSE and scrapie: automated home cage monitoring reveals prion strain differences. Eur. J. Neurosci. 16, 735-742 (2002).
44. Nielsen, D. M. et al. Paw preference, rotation, and dopamine function in Collins HI and LO mouse strains. Physiol. Behav. 61, 525-535 (1997).
45. Nishimura, F. et al. Potential use of embryonic stem cells for the treatment of mouse parkinsonian models: improved behavior by transplantation of in vitro differentiated dopaminergic neurons from embryonic stem cells. Stem Cells 21, 171-180 (2003).
46. Zhang, X., Andren, P. E., Greengard, P. & Svenningsson, P. Evidence for a role of the 5-HT1B receptor and its adaptor protein, p11, in L-DOPA treatment of an animal model of Parkinsonism. Proc. Natl Acad. Sci. USA 105, 2163-2168 (2008).
47. Ungerstedt, U. & Arbuthnott, G. W. Quantitative recording of rotational behaviour in rats after 6-hydroxydopamine lesions of the nigrostriatal dopamine system. Brain Res. 24, 485-493 (1970).
48. Matsuya, T. et al. Synergistic effects of adenosine A2A antagonist and L-DOPA on rotational behaviors in 6-hydroxydopamine-induced hemi-Parkinsonian mouse model. J. Pharmacol. Sci. 103, 329-332 (2007).
49. Yu, L., Schwarzschild, M. A. & Chen, J. F. Crosssensitization between caffeine- and L-dopa-induced behaviors in hemiparkinsonian mice. Neurosci. Lett. 393, 31-35 (2006).
50. Björklund, L. et al. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl Acad. Sci. USA 99, 2344-2349 (2002).
51. Bensadoun, J. C., Mirochnitchenko, O., Inouye, M., Aebischer, P. & Zurn, A. D. Attenuation of 6-OHDA-induced neurotoxicity in glutathione peroxidase transgenic mice. Eur. J. Neurosci. 10, 3231-3236 (1998).
52. Dunham, N. W. & Miya, T. S. A note on a simple apparatus for detecting neurological deficit in rats and mice. J. Am. Pharm. Assoc. 46, 208-209 (1957).
53. Jones, B. J. & Roberts, D. J. A rotarod suitable for quantitative measurements of motor inco-ordination in naive mice. Naunyn-Schmiedebergs Arch. Pharmacol. 259, 211 (1968).
54. Monville, C., Torres, E. M. & Dunnett, S. B. Comparison of two different protocols of the rotarod test to assess motor deficit and lesion size in the 6-OHDA model. J. Neurosci. Methods 158, 219-223 (2006). Although this study used rats, the findings are applicable to mouse models of disease. They demonstrate that different lesion types are differentially sensitive to different rotarod test protocols.
55. Wallace, J. E., Krauter, E. E. & Campbell, B. A. Motor and reflexive behavior in the aging rat. J. Gerontol. 35, 364-270 (1980).
56. Kiernan, B. W. et al. Myelination and behaviour of tenascin-C null transgenic mice. Eur. J. Neurosci. 11, 3082-3092 (1999).
57. Perry, T. A. et al. Cognitive and motor function in transgenic mice carrying excess copies of the 695 and 751 amino acid isoforms of the amyloid precursor protein gene. Alz. Res. 1, 5-14 (1995).
58. Schallert, T., Woodlee, M. T. & Fleming, S. M. in Pharmacology of Cerebral Ischemia (eds Krieglstein, J. & Klumpp, S.) 201-216 (Medpharm Scientific Publishers, Stuttgart, 2002).
59. Heglund, N. C., Taylor, C. R. & McMahon, T. A. Scaling stride frequency and gait to animal size: mice to horses. Science 186, 1112-1113 (1974).
60. Clarke, K. A. & Still, J. Development and consistency of gait in the mouse. Physiol. Behav. 73, 159-164 (2001). Demonstrates the use of video technology to measure several aspects of mouse gait in detail.
61. Glynn, D., Drew, C. J., Reim, K., Brose, N. & Morton, A. J. Profound ataxia in complexin I knockout mice masks a complex phenotype that includes exploratory and habituation deficits. Hum. Mol. Genet. 14, 2369-2385 (2005).
62. Guillot, T. S., Asress, S. A., Richardson, J. R., Glass, J. D. & Miller, G. W. Treadmill gait analysis does not detect motor deficits in animal models of Parkinson's disease or amyotrophic lateral sclerosis. J. Mot. Behav. 40, 568-577 (2008).
63. Marshall, J. F., Richardson, J. S. & Teitelbaum, P. Nigrostriatal bundle damage and the lateral hypothalamic syndrome. J. Comp. Physiol. Psychol. 87, 808-830 (1974).
64. Ogawa, N., Hirose, Y., Ohara, S., Ono, T. & Watanabe, Y. A simple quantitative bradykinesia test in MPTPtreated mice. Res. Commun. Chem. Pathol. Pharmacol. 50, 435-441 (1985).
65. Ohno, Y. et al. Evaluation of the antibradykinetic actions of 5-HT1A agonists using the mouse pole test. Prog. Neuropsychopharmacol. Biol. Psychiatry 32, 1302-1307 (2008).
66. Thullier, F., Lalonde, R., Cousin, X. & Lestienne, F. Neurobehavioral evaluation of lurcher mutant mice during ontogeny. Brain Res. Dev. Brain Res. 100, 22-28 (1997).
67. Crawley, J. N. What's Wrong With My Mouse?: Behavioral Phenotyping of Transgenic and Knockout Mice (Wiley, New York, 2000). Probably the most informative text on behavioural phenotyping of the mouse.
68. Kashiwabuchi, N. et al. Impairment of motor coordination, Purkinje cell synapse formation, and cerebellar long-term depression in GluRd2 mutant mice. Cell 81, 245-252 (1995).
69. Lalonde, R., Qian, S. & Strazielle, C. Transgenic mice expressing the PS1-A246E mutation: effects on spatial learning, exploration, anxiety, and motor coordination. Behav. Brain Res. 138, 271-279 (2003).
70. Lalonde, R. & Strazielle, C. Motor coordination, exploration, and spatial learning in a natural mouse mutation (nervous) with Purkinje cell degeneration. Behav. Genet. 33, 59-66 (2003).
71. Le Cudennec, C., Faure, A., Ly, M. & Delatour, B. Oneyear longitudinal evaluation of sensorimotor functions in APP751SL transgenic mice. Genes Brain Behav. . (Suppl. 1), 783-791 (2008).
72. Baskin, Y. K., Dietrich, W. D. & Green, E. J. Two effective behavioral tasks for evaluating sensorimotor dysfunction following traumatic brain injury in mice. J. Neurosci. Methods 129, 87-93 (2003).
73. Farr, T. D., Liu, L., Colwell, K. L., Whishaw, I. Q. & Metz, G. A. Bilateral alteration in stepping pattern after unilateral motor cortex injury: a new test strategy for analysis of skilled limb movements in neurological mouse models. J. Neurosci. Methods 153, 104-113 (2006).
74. Metz, G. A. & Whishaw, I. Q. Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J. Neurosci. Methods 115, 169-179 (2002).
75. Cabe, P. A., Tilson, H. A., Mitchell, C. L. & Dennis, R. A simple recording grip strength device. Pharmacol. Biochem. Behav. 8, 101-102 (1978).
76. Joseph, J. A. & Lippa, A. S. Reduction of motor behavioral deficits in senescent animals via chronic prolactin administration. II. Non-stereotypic behaviors. Neurobiol. Aging 7, 37-40 (1986).
77. van Riezen, H. & Boersma, L. A new method for quantitative grip strength evaluation. Eur. J. Pharmacol. 6, 353-356 (1969).
78. Jodogne, C., Tirelli, E., Klingbiel, P. & Legros, J. J. Oxytocin attenuates tolerance not only to the hypothermic but also to the myorelaxant and akinesic effects of ethanol in mice. Pharmacol. Biochem. Behav. 40, 261-265 (1991).
79. Lorivel, T. & Hilber, P. Motor effects of delta 9 THC in cerebellar Lurcher mutant mice. Behav. Brain Res. 181, 248-253 (2007).
80. Whishaw, I. Q., Sarna, J. R. & Pellis, S. M. Evidence for rodent-common and species-typical limb and digit use in eating, derived from a comparative analysis of ten rodent species. Behav. Brain Res. 96, 79-91 (1998).
81. Eshkol, N. & Wachmann, A. Movement Notation (Weidenfeld and Nicholson, London, 1958).
82. Whishaw, I. Q., Woodward, N. C., Miklyaeva, E. & Pellis, S. M. Analysis of limb use by control rats and unilateral DA-depleted rats in the Montoya staircase test: movements, impairments and compensatory strategies. Behav. Brain Res. 89, 167-177 (1997).
83. Farr, T. D. & Whishaw, I. Q. Quantitative and qualitative impairments in skilled reaching in the mouse (Mus musculus) after a focal motor cortex stroke. Stroke 33, 1869-1875 (2002).
84. Whishaw, I. Q. & Pellis, S. M. The structure of skilled forelimb reaching in the rat: a proximally driven movement with a single distal rotatory component. Behav. Brain Res. 41, 49-59 (1990).
85. Whishaw, I. Q., Pellis, S. M., Gorny, B. P. & Pellis, V. C. The impairments in reaching and the movements of compensation in rats with motor cortex lesions: an endpoint, videorecording, and movement notation analysis. Behav. Brain Res. 42, 77-91 (1991).
86. Whishaw, I. Q. An endpoint, descriptive, and kinematic comparison of skilled reaching in mice (Mus musculus) with rats (Rattus norvegicus). Behav. Brain Res. 78, 101-111 (1996).
87. Whishaw, I. Q., O'Connor, W. T. & Dunnett, S. B. The contributions of motor cortex, nigrostriatal dopamine and caudate-putamen to skilled forelimb use in the rat. Brain 109, 805-843 (1986).
88. Wells, J. E. et al. Matrix metalloproteinase (MMP)-12 expression has a negative impact on sensorimotor function following intracerebral haemorrhage in mice. Eur. J. Neurosci. 21, 187-196 (2005).
89. Collins, R. L. On the inheritance of handedness. I. Laterality in inbred mice. J. Hered. 59, 9-12 (1968).
90. Cabib, S. et al. Paw preference and brain dopamine asymmetries. Neuroscience 64, 427-432 (1995).
91. Baird, A. L., Meldrum, A. & Dunnett, S. B. The staircase test of skilled reaching in mice. Brain Res. Bull. 54, 243-250 (2001). Demonstration of the staircase test in mice as a method to assess fine motor control.
92. Puskovic, V. et al. Prolonged biologically active transgene expression driven by HSV LAP2 in brain in vivo. Mol. Ther. 10, 67-75 (2004).
93. Starkey, M. L. et al. Assessing behavioural function following a pyramidotomy lesion of the corticospinal tract in adult mice. Exp. Neurol. 195, 524-539 (2005).
94. Bouet, V. et al. Sensorimotor and cognitive deficits after transient middle cerebral artery occlusion in the mouse. Exp. Neurol. 203, 555-567 (2007).
95. Paylor, R. & Crawley, J. N. Inbred strain differences in prepulse inhibition of the mouse startle response. Psychopharmacology (Berl.) 132, 169-180 (1997). This paper shows the sensitivity of prepulse inhibition across a range of inbred mouse strains.
96. Hoffman, H. S. & Searle, J. L. Acoustic variables in the modification of startle reaction in the rat. J. Comp. Physiol. Psychol. 60, 53-58 (1965).
97. Grillon, C., Ameli, R., Charney, D. S., Krystal, J. & Braff, D. Startle gating deficits occur across prepulse intensities in schizophrenic patients. Biol. Psychiatry 32, 939-943 (1992).
98. Perriol, M. P. et al. Disturbance of sensory filtering in dementia with Lewy bodies: comparison with Parkinson's disease dementia and Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 76, 106-108 (2005).
99. Swerdlow, N. R. et al. Impaired prepulse inhibition of acoustic and tactile startle response in patients with Huntington's disease. J. Neurol. Neurosurg. Psychiatry 58, 192-200 (1995).
100. Semenova, S., Geyer, M. A., Sutcliffe, J. G., Markou, A. & Hedlund, P. B. Inactivation of the 5-HT7 receptor partially blocks phencyclidine-induced disruption of prepulse inhibition. Biol. Psychiatry 63, 98-105 (2008).
101. Yee, B. K., Chang, D. L. & Feldon, J. The effects of dizocilpine and phencyclidine on prepulse inhibition of the acoustic startle reflex and on prepulse-elicited reactivity in C57BL6 mice. Neuropsychopharmacology 29, 1865-1877 (2004).
102. Van Raamsdonk, J. M. et al. Cognitive dysfunction precedes neuropathology and motor abnormalities in the YAC128 mouse model of Huntington's disease. J. Neurosci. 25, 4169-4180 (2005).
103. Plappert, C. F., Rodenbucher, A. M. & Pilz, P. K. Effects of sex and estrous cycle on modulation of the acoustic startle response in mice. Physiol. Behav. 84, 585-594 (2005).
104. Willott, J. F. et al. The BALB/c mouse as an animal model for progressive sensorineural hearing loss. Hear. Res. 115, 162-174 (1998).
105. Mackintosh, N. J. The Psychology of Animal Learning (Academic, 1974).
106. Humby, T., Laird, F. M., Davis, W. & Wilkinson, L. S. Visuospatial attentional functioning in mice: interactions between cholinergic manipulations and genotype. Eur. J. Neurosci. 11, 2813-2823 (1999). Demonstration of the five-choice reaction time task for operant motor learning in the mouse in the nine-hole box.
107. Baron, S. P. & Meltzer, L. T. Mouse strains differ under a simple schedule of operant learning. Behav. Brain Res. 118, 143-152 (2001).
108. Bensadoun, J. C., Brooks, S. P. & Dunnett, S. B. Free operant and discrete trial performance of mice in the 9-hole box apparatus: validation using amphetamine and scopolamine. Psychopharmacology (Berl.) 174, 396-405 (2004).
109. Derenne, A., Arsenault, M. L., Austin, D. P. & Weatherly, J. N. Weaver mutant mice exhibit long-term learning deficits under several measures of instrumental behavior. Physiol. Behav. 92, 1002-1009 (2007).
110. Carli, M., Robbins, T. W., Evenden, J. L. & Everitt, B. J. Effects of lesions to ascending noradrenergic neurones on performance of a 5-choice serial reaction task in rats; implications for theories of dorsal noradrenergic bundle function based on selective attention and arousal. Behav. Brain Res. 9, 361-380 (1983).
111. Cho, Y. H., Delcasso, S., Israel, A. & Jeantet, Y. A long list visuo-spatial sequential learning in mice. Behav. Brain Res. 179, 152-158 (2007).
112. Christie, M. A. & Hersch, S. M. Demonstration of nondeclarative sequence learning in mice: development of an animal analog of the human serial reaction time task. Learn. Mem. 11, 720-723 (2004).
113. Trueman, R. C., Brooks, S. P. & Dunnett, S. B. Implicit learning in a serial choice visual discrimination task in the operant 9-hole box by intact and striatal lesioned mice. Behav. Brain Res. 159, 313-322 (2005).
114. Brooks, S. P., Trueman, R. C. & Dunnett, S. B. Striatal lesions in the mouse disrupt acquisition and retention, but not implicit learning, in the SILT procedural motor learning task. Brain Res. 1185, 179-188 (2007).
115. Trueman, R. C., Brooks, S. P., Jones, L. & Dunnett, S. B. Time course of choice reaction time deficits in the HdhQ92/Q92 knock-in mouse model of Huntington's disease in the operant Serial Implicit Learning Task (SILT). Behav. Brain Res. 189, 317-324 (2008). This paper demonstrates the sensitivity of the SILT to motor learning in a knock-in mouse model of disease.
116. Wrenn, C. C. et al. Performance of galanin transgenic mice in the 5-choice serial reaction time attentional task. Pharmacol. Biochem. Behav. 83, 428-440 (2006).
117. Marsden, C. D. & Parkes, J. D. Success and problems of long-term levodopa therapy in Parkinson's disease. Lancet 1, 345-349 (1977).
118. Ohl, F. Animal models of anxiety. Handb. Exp. Pharmacol. 169, 35-69 (2005).
119. Caligiuri, M. P. & Buitenhuys, C. Do preclinical findings of methamphetamine-induced motor abnormalities translate to an observable clinical phenotype? Neuropsychopharmacology 30, 2125-2134 (2005).
120. Willner, P. The validity of animal models of depression. Psychopharmacology (Berl.) 83, 1-16 (1984).
121. Lalonde, R. & Strazielle, C. Brain regions and genes affecting postural control. Prog. Neurobiol. 81, 45-60 (2007).
122. Winer, B. J., Brown, D. R. & Michels, K. M. Statistical Principles in Experimental Design (McGraw-Hill, New York, 1991).
123. Robinson, V. Finding alternatives: an overview of the 3Rs and the use of animals in research. Sch. Sci. Rev. 87, 111-114 (2005).
124. Masuya, H. et al. Implementation of the modified- SHIRPA protocol for screening of dominant phenotypes in a large-scale ENU mutagenesis program. Mamm. Genome 16, 829-837 (2005).
125. Inoue, M. et al. Sensory stimulation accelerates dopamine release in the basal ganglia. Brain Res. 1026, 179-184 (2004).
126. Ferdinandusse, S. et al. Ataxia with loss of Purkinje cells in a mouse model for Refsum disease. Proc. Natl Acad. Sci. USA 105, 17712-17717 (2008).
127. Lackner, P. et al. Behavioural and histopathological alterations in mice with cerebral malaria. Neuropathol. Appl. Neurobiol. 32, 177-188 (2006).
128. Lalonde, R., Dumont, M., Paly, E., London, J. & Strazielle, C. Characterization of hemizygous SOD1/ wild-type transgenic mice with the SHIRPA primary screen and tests of sensorimotor function and anxiety. Brain Res. Bull. 64, 251-258 (2004).
129. Rafael, J. A., Nitta, Y., Peters, J. & Davies, K. E. Testing of SHIRPA, a mouse phenotypic assessment protocol, on Dmd(mdx) and Dmd(mdx3cv) dystrophin-deficient mice. Mamm. Genome 11, 725-728 (2000).
130. Harms, L. R., Eyles, D. W., McGrath, J. J., Mackay-Sim, A. & Burne, T. H. Developmental vitamin D deficiency alters adult behaviour in 129/SvJ and C57BL/56J mice. Behav. Brain Res. 187, 343-350 (2008).