The development, validation and application of automated home-cage based tasks to
assess cognition in mice
Remmelink, E.
2017
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Remmelink, E. (2017). The development, validation and application of automated home-cage based tasks to
assess cognition in mice.
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References
1. Millan, M. J. et al. Cognitive dysfunction in psychiatric disorders:
characteristics, causes and the quest for improved therapy. Nat. Rev. Drug
Discov. 11, 141–168 (2012).
2. Pessoa, L. On the relationship between emotion and cognition. Nat. Rev.
Neurosci. 9, 148–58 (2008).
3. Logue, S. F. & Gould, T. J. The neural and genetic basis of executive function: Attention, cognitive flexibility, and response inhibition.
Pharmacol. Biochem. Behav. 123, 45–54 (2014).
4. Scott, W. A. Cognitive Complexity and Cognitive Flexibility. Sociometry 25,
405 (1962).
5. Winstanley, C. A., Eagle, D. M. & Robbins, T. W. Behavioral models of impulsivity in relation to ADHD: Translation between clinical and preclinical studies. Clin. Psychol. Rev. 26, 379–395 (2006).
6. Bienvenu, O. J., Davydow, D. S. & Kendler, K. S. Psychiatric ‘diseases’ versus behavioral disorders and degree of genetic influence. Psychol. Med. 41, 33–
40 (2011).
7. Chinwalla, A. T. et al. Initial sequencing and comparative analysis of the mouse genome. Nature 420, 520–562 (2002).
8. van der Staay, F. J. Animal models of behavioral dysfunctions: basic concepts and classifications, and an evaluation strategy. Brain Res. Rev. 52,
131–59 (2006).
9. Crawley, J. N. What’s Wrong With My Mouse? Behavioral Phenotyping of
Transgenic and Knockout Mice. (Wiley, 2007).
10. Mucke, L. et al. High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation. J. Neurosci. 20, 4050–8 (2000).
11. Gavériaux-Ruff, C. & Kieffer, B. L. Conditional gene targeting in the mouse nervous system: Insights into brain function and diseases. Pharmacol. Ther.
113, 619–634 (2007).
12. Crawley, J. N. Behavioral phenotyping strategies for mutant mice. Neuron
57, 809–18 (2008).
13. Wahlsten, D. Mouse behavioral testing: how to use mice in behavioral
neuroscience. (Academic Press, 2011).
doi:10.1016/B978-0-12-375674-9.10011-4
&
learning in the rat. J. Neurosci. Methods 11, 47–60 (1984).
15. Barnes, C. A. Memory deficits associated with senescence: a
neurophysiological and behavioral study in the rat. J. Comp. Physiol.
Psychol. 93, 74–104 (1979).
16. Skinner, B. F. Superstition in the pigeon. J. Exp. Psychol. 38, 168–72 (1948).
17. Floresco, S. B., Block, A. E. & Tse, M. T. L. Inactivation of the medial prefrontal cortex of the rat impairs strategy set-shifting, but not reversal learning, using a novel, automated procedure. Behav. Brain Res. 190, 85–96
(2008).
18. Ortega, L. A., Tracy, B. A., Gould, T. J. & Parikh, V. Effects of chronic low- and high-dose nicotine on cognitive flexibility in C57BL/6J mice. Behav.
Brain Res. 238, 134–45 (2013).
19. 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).
20. Humby, T., Laird, F. M., Davies, W. & Wilkinson, L. S. Visuospatial attentional functioning In mice: Interactions between cholinergic manipulations and genotype. Eur. J. Neurosci. 11, 2813–2823 (1999).
21. Bussey, T. J., Muir, J. L., Everitt, B. J. & Robbins, T. W. Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat.
Behav. Neurosci. 111, 920–36 (1997).
22. Mar, A. C. et al. The touchscreen operant platform for assessing executive function in rats and mice. Nat. Protoc. 8, 1985–2005 (2013).
23. Horner, A. E. et al. The touchscreen operant platform for testing learning and memory in rats and mice. Nat. Protoc. 8, 1961–84 (2013).
24. Goldstein, J. M., Cherkerzian, S. & Simpson, C. in Textbook of Psychiatric
Epidemiology 664 (2011). doi:10.1002/9780470976739.ch17
25. Markou, A., Chiamulera, C., Geyer, M. A., Tricklebank, M. & Steckler, T. Removing obstacles in neuroscience drug discovery: the future path for animal models. Neuropsychopharmacology 34, 74–89 (2009).
26. Sarter, M. Animal cognition: defining the issues. Neurosci. Biobehav. Rev.
28, 645–50 (2004).
27. Pratt, J., Winchester, C., Dawson, N. & Morris, B. Advancing schizophrenia drug discovery: optimizing rodent models to bridge the translational gap.
28. Couzin-Frankel, J. When Mice Mislead. Science 342, 922–924 (2013).
29. Crabbe, J. C., Wahlsten, D. & Dudek, B. C. Genetics of Mouse Behavior: Interactions with Laboratory Environment. Science 284, 1670–1672 (1999).
30. Wahlsten, D. et al. Different Data from Different Labs: Lessons from Studies of Gene – Environment Interaction. J. Neurobiol. 54, 283–311 (2003).
31. Stewart, A. M. & Kalueff, A. V. Developing better and more valid animal models of brain disorders. Behav. Brain Res. 276, 28–31 (2015).
32. Chesler, E. J., Wilson, S. G., Lariviere, W. R., Rodriguez-Zas, S. L. & Mogil, J. S. Influences of laboratory environment on behavior. Nat. Neurosci. 5,
1101–2 (2002).
33. Balcombe, J. P., Barnard, N. D. & Sandusky, C. Laboratory routines cause animal stress. Contemp. Top. Lab. Anim. Sci. 43, 42–51 (2004).
34. Longordo, F., Fan, J., Steimer, T., Kopp, C. & Lüthi, A. Do mice habituate to ‘gentle handling?’ A comparison of resting behavior, corticosterone levels and synaptic function in handled and undisturbed C57BL/6J mice. Sleep
34, 679–681 (2011).
35. Hurst, J. L. & West, R. S. Taming anxiety in laboratory mice. Nat. Methods 7,
825–6 (2010).
36. Tecott, L. H. & Nestler, E. J. Neurobehavioral assessment in the information age. Nat. Neurosci. 7, 462–6 (2004).
37. Wahlsten, D. Standardizing tests of mouse behavior: reasons, recommendations, and reality. Physiol. Behav. 73, 695–704 (2001).
38. 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).
39. Gainetdinov, R. R. et al. Role of Serotonin in the Paradoxical Calming Effect of Psychostimulants on Hyperactivity. 283, (1999).
40. Roedel, A., Storch, C., Holsboer, F. & Ohl, F. Effects of light or dark phase testing on behavioural and cognitive performance in DBA mice. Lab. Anim.
40, 371–381 (2006).
41. Spruijt, B. M., Peters, S. M., de Heer, R. C., Pothuizen, H. H. J. & van der Harst, J. E. Reproducibility and relevance of future behavioral sciences should benefit from a cross fertilization of past recommendations and today’s technology: ‘Back to the future’. J. Neurosci. Methods 234, 2–12
(2014).
&
43. Benjamini, Y. et al. Ten ways to improve the quality of descriptions of whole-animal movement. Neurosci. Biobehav. Rev. 34, 1351–65 (2010).
44. Steckler, T. Not only how, but also what and why. Trends in Neurosciences
22, (1999).
45. Cabib, S., Orsini, C., Le Moal, M. & Piazza, P. V. Abolition and Reversal of Strain Differences in Behavioral Responses to Drugs of Abuse After a Brief Experience. Science 289, 463–465 (2000).
46. Conrad, C. D. A critical review of chronic stress effects on spatial learning and memory. Prog. Neuropsychopharmacol. Biol. Psychiatry 34, 742–55
(2010).
47. Papaleo, F., Erickson, L., Liu, G., Chen, J. & Weinberger, D. R. Effects of sex and COMT genotype on environmentally modulated cognitive control in mice. Proc. Natl. Acad. Sci. U. S. A. 109, 20160–5 (2012).
48. Kant, G. J., Anderson, S. M., Dhillon, G. S. & Mougey, E. H. Neuroendocrine correlates of sustained stress: The activity-stress paradigm. Brain Res. Bull.
20, 407–414 (1988).
49. Guarnieri, D. J. et al. Gene profiling reveals a role for stress hormones in the molecular and behavioral response to food restriction. Biol. Psychiatry 71,
358–65 (2012).
50. Heiderstadt, K. M., McLaughlin, R. M., Wrighe, D. C., Walker, S. E. & Gomez-Sanchez, C. E. The effect of chronic food and water restriction on open-field behaviour and serum corticosterone levels in rats. Lab. Anim. 34,
20–28 (2000).
51. Paus, T., Keshavan, M. & Giedd, J. N. Why do many psychiatric disorders emerge during adolescence? Nat. Rev. Neurosci. 9, 947–957 (2008).
52. Willner, P. in Neuromethods. Animal Models in Psychiatry, I 18, (Humana
Press, 1991).
53. Belzung, C. & Lemoine, M. Criteria of validity for animal models of psychiatric disorders: focus on anxiety disorders and depression. Biol.
Mood Anxiety Disord. 1, 9 (2011).
54. Calatayud, F., Belzung, C. & Aubert, A. Ethological validation and the assessment of anxiety-like behaviours: methodological comparison of classical analyses and structural approaches. Behav. Processes 67, 195–206
(2004).
55. Homberg, J. R. Measuring behaviour in rodents: towards translational neuropsychiatric research. Behav. Brain Res. 236, 295–306 (2013).
57. Gerlai, R. Phenomics: fiction or the future? Trends Neurosci. 25, 506–9
(2002).
58. Schaefer, A. T. & Claridge-Chang, A. The surveillance state of behavioral automation. Curr. Opin. Neurobiol. 22, 170–6 (2012).
59. Fonio, E., Golani, I. & Benjamini, Y. Measuring behavior of animal models: faults and remedies. Nat. Methods 9, 1167–1170 (2012).
60. Brunner, D., Nestler, E. & Leahy, E. In need of high-throughput behavioral systems. Drug Discov. Today 7, 107–112 (2002).
61. Visser, L. de, Bos, R. van den & Spruijt, B. M. Automated home cage
observations as a tool to measure the effects of wheel running on cage floor locomotion. Behav. Brain Res. 160, 382–8 (2005).
62. 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).
63. Steele, A. D., Jackson, W. S., King, O. D. & Lindquist, S. The power of automated high-resolution behavior analysis revealed by its application to mouse models of Huntington’s and prion diseases. Proc. Natl. Acad. Sci. U.
S. A. 104, 1983–8 (2007).
64. Goulding, E. H. et al. A robust automated system elucidates mouse home cage behavioral structure. Proc. Natl. Acad. Sci. U. S. A. 105, 20575–82
(2008).
65. Jhuang, H. et al. Automated home-cage behavioural phenotyping of mice.
Nat. Commun. 1, 68 (2010).
66. Loos, M. et al. Sheltering Behavior and Locomotor Activity in 11 Genetically Diverse Common Inbred Mouse Strains Using Home-Cage Monitoring.
PLoS One 9, e108563 (2014).
67. Mechan, A. O., Wyss, A., Rieger, H. & Mohajeri, M. H. A comparison of learning and memory characteristics of young and middle-aged wild-type mice in the IntelliCage. J. Neurosci. Methods 180, 43–51 (2009).
68. Endo, T. et al. Automated test of behavioral flexibility in mice using a behavioral sequencing task in IntelliCage. Behav. Brain Res. 221, 172–81
(2011).
69. Puścian, A. et al. A novel automated behavioral test battery assessing cognitive rigidity in two genetic mouse models of autism. Front. Behav.
Neurosci. 8, 140 (2014).
&
71. Krackow, S. et al. Consistent behavioral phenotype differences between inbred mouse strains in the IntelliCage. Genes, Brain Behav. 9, 722–31
(2010).
72. Codita, A. et al. Effects of spatial and cognitive enrichment on activity pattern and learning performance in three strains of mice in the IntelliMaze. Behav. Genet. 42, 449–460 (2012).
73. Gallistel, C. R. et al. Screening for Learning and Memory Mutations : A New Approach. Acta Psychol. Sin. 42, 138–158 (2010).
74. Urbach, Y. K. et al. Automated phenotyping and advanced data mining exemplified in rats transgenic for Huntington’s disease. J. Neurosci. Methods
234, 38–53 (2014).
75. Koot, S., Adriani, W., Saso, L., van den Bos, R. & Laviola, G. Home cage testing of delay discounting in rats. Behav. Res. Methods 41, 1169–76 (2009).
76. Visser, L. de, Bos, R. van den, Kuurman, W. W., Kas, M. J. H. & Spruijt, B. M. Novel approach to the behavioural characterization of inbred mice: automated home cage observations. Genes, Brain Behav. 5, 458–66 (2006).
77. Arndt, S. S. et al. Individual housing of mice -impact on behaviour and stress responses. Physiol. Behav. 97, 385–93 (2009).
78. Kamakura, R., Kovalainen, M., Leppäluoto, J., Herzig, K. & Mäkelä, K. A. The effects of group and single housing and automated animal monitoring on urinary corticosterone levels in male C57BL/6 mice. Physiol. Rep. 4,
e12703 (2016).
79. Van Loo, P. L. P., Van de Weerd, H. a, Van Zutphen, L. F. M. & Baumans, V. Preference for social contact versus environmental enrichment in male laboratory mice. Lab. Anim. 38, 178–188 (2004).
80. Aarts, E. et al. The light spot test: measuring anxiety in mice in an
automated home-cage environment. Behav. Brain Res. 294, 123–130 (2015).
81. Maroteaux, G. et al. High-throughput phenotyping of avoidance learning in mice discriminates different genotypes and identifies a novel gene. Genes.
Brain. Behav. 11, 772–84 (2012).
82. Heer, R. C. de, Schenke, M., Kuurman, W. W. & Spruijt, B. M. Learning (in) the PhenoTyper: an integrative approach to conducting cognitive behavioural challenges in a home cage environment. Proc. Meas. Behav.
2008 (Maastricht, Netherlands) (2008).
83. Kas, M. J. H. et al. Advances in multidisciplinary and cross-species approaches to examine the neurobiology of psychiatric disorders. Eur.
Neuropsychopharmacol. 21, 532–544 (2011).
development of valid animal models. Genes. Brain. Behav. 5, 113–9 (2006).
85. Gerlai, R. & Clayton, N. S. Analysing hippocampal function in transgenic mice: an ethological perspective. Trends Neurosci. 22, 47–51 (1999).
86. Olsson, I. A. S. et al. Understanding behaviour: the relevance of ethological approaches in laboratory animal science. Appl. Anim. Behav. Sci. 81, 245–
264 (2003).
87. Thorndike, E. L. Animal intelligence experimental studies. (Macmillan, 1911). 88. Skinner, B. F. Selection by consequences. Science 213, 501–504 (1981).
89. Sorge, R. E. et al. Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nat. Methods 11, 629–632 (2014).
90. Beck, K. D. & Luine, V. N. Food deprivation modulates chronic stress effects on object recognition in male rats: role of monoamines and amino acids.
Brain Res. 830, 56–71 (1999).
91. Hut, R. A., Pilorz, V., Boerema, A. S., Strijkstra, A. M. & Daan, S. Working for food shifts nocturnal mouse activity into the day. PLoS One 6, e17527 (2011).
92. Hashimoto, T. & Watanabe, S. Chronic food restriction enhances memory in mice--analysis with matched drive levels. Neuroreport 16, 1129–33 (2005).
93. Vannoni, E. et al. Spontaneous behavior in the social homecage
discriminates strains, lesions and mutations in mice. J. Neurosci. Methods
234, 26–37 (2014).
94. Noldus, L. P., Spink, A. J. & Tegelenbosch, R. A. EthoVision: a versatile video tracking system for automation of behavioral experiments. Behav. Res.
methods, instruments, Comput. 33, 398–414 (2001).
95. R Development Core Team. R: A Language and Environment for Statistical Computing. (2012).
96. Brown, P. L. & Jenkins, H. M. Auto-shaping of the pigeon’s key-peck. J. Exp.
Anal. Behav. 11, 1–8 (1968).
97. Luksys, G., Gerstner, W. & Sandi, C. Stress, genotype and norepinephrine in the prediction of mouse behavior using reinforcement learning. Nat.
Neurosci. 12, 1180–6 (2009).
98. Koot, S., van den Bos, R., Adriani, W. & Laviola, G. Gender differences in delay-discounting under mild food restriction. Behav. Brain Res. 200, 134–
143 (2009).
99. Orsini, C., Buchini, F., Conversi, D. & Cabib, S. Selective improvement of strain-dependent performances of cognitive tasks by food restriction.
Neurobiol. Learn. Mem. 81, 96–99 (2004).
&
of food restriction on acquisition and expression of a conditioned odor discrimination in mice. Physiol. Behav. 72, 559–66 (2001).
101. Makowiecki, K., Hammond, G. & Rodger, J. Different levels of food restriction reveal genotype-specific differences in learning a visual discrimination task. PLoS One 7, e48703 (2012).
102. Kant, G. J., Yen, M. H., D’Angelo, P. C., Brown, A. J. & Eggleston, T. Maze performance: A direct comparison of food vs. water mazes. Pharmacol.
Biochem. Behav. 31, 487–491 (1988).
103. Wayner, M. J. & Rondeau, D. B. Schedule Dependent and Schedule Induced Behavior at Reduced and Recovered Body Weight. Physiol. Behav. 17, 325–
336 (1976).
104. Ghiglieri, O. et al. Palatble food induces appetitive behaviour in satiated rats which can be inhibited by chronic stress. Behav. Pharmacol. 8, 619–628
(1997).
105. Wahlsten, D. Mouse behavioral testing: how to use mice in behavioral
neuroscience. (Academic Press, 2011).
doi:10.1016/B978-0-12-375674-9.10011-4
106. Malkki, H. A. I., Donga, L. A. B., de Groot, S. E., Battaglia, F. P. & Pennartz, C. M. A. Appetitive operant conditioning in mice: heritability and
dissociability of training stages. Front. Behav. Neurosci. 4, 171 (2010).
107. Graybeal, C. et al. Strains and stressors: an analysis of touchscreen learning in genetically diverse mouse strains. PLoS One 9, e87745 (2014).
108. Lederle, L. et al. Reward-related behavioral paradigms for addiction
research in the mouse: performance of common inbred strains. PLoS One 6,
e15536 (2011).
109. Dym, C. T., Pinhas, A., Ginzberg, M., Kest, B. & Bodnar, R. J. Genetic variance contributes to naltrexone-induced inhibition of sucrose intake in inbred and outbred mouse strains. Brain Res. 1135, 136–45 (2007).
110. Johnson, J. M., Bailey, J. M., Johnson, J. E. & Newland, M. C. Performance of BALB/c and C57BL/6 mice under an incremental repeated acquisition of behavioral chains procedure. Behav. Processes 84, 705–14 (2010).
111. Murray, G. K. et al. Reinforcement and reversal learning in first-episode psychosis. Schizophr. Bull. 34, 848–55 (2008).
112. Leeson, V. C. et al. Discrimination learning, reversal, and set-shifting in first-episode schizophrenia: stability over six years and specific associations with medication type and disorganization syndrome. Biol. Psychiatry 66,
586–93 (2009).
disorders. Neuropsychology 27, 152–60 (2013).
114. Brigman, J. L., Graybeal, C. & Holmes, A. Predictably irrational: assaying cognitive inflexibility in mouse models of schizophrenia. Front. Neurosci. 4,
19–28 (2010).
115. Laughlin, R. E., Grant, T. L., Williams, R. W. & Jentsch, J. D. Genetic Dissection of Behavioral Flexibility: Reversal Learning in Mice. Biol.
Psychiatry 69, 1109–1116 (2011).
116. Brigman, J. L., Bussey, T. J., Saksida, L. M. & Rothblat, L. A. Discrimination of multidimensional visual stimuli by mice: intra- and extradimensional shifts. Behav. Neurosci. 119, 839–42 (2005).
117. Martin, B., Ji, S., Maudsley, S. & Mattson, M. P. ‘Control’ laboratory rodents are metabolically morbid: why it matters. Proc. Natl. Acad. Sci. U. S. A. 107,
6127–33 (2010).
118. Dias, R., Robbins, T. W. & Roberts, A. C. Dissociable forms of inhibitory control within prefrontal cortex with an analog of the Wisconsin Card Sort Test: restriction to novel situations and independence from ‘on-line’ processing. J. Neurosci. 17, 9285–97 (1997).
119. Tsuchida, A., Doll, B. B. & Fellows, L. K. Beyond reversal: a critical role for human orbitofrontal cortex in flexible learning from probabilistic feedback.
J. Neurosci. 30, 16868–75 (2010).
120. Jankowsky, J. L. et al. Mutant presenilins specifically elevate the levels of the 42 residue β-amyloid peptide in vivo: Evidence for augmentation of a 42-specific β secretase. Hum. Mol. Genet. 13, 159–170 (2004).
121. Reiserer, R. S., Harrison, F. E., Syverud, D. C. & McDonald, M. P. Impaired spatial learning in the APPSwe + PSEN1DeltaE9 bigenic mouse model of Alzheimer’s disease. Genes. Brain. Behav. 6, 54–65 (2007).
122. Cramer, P. E. et al. ApoE-Directed Therapeutics Rapidly Clear b-Amyloid and Reverse Deficits in AD Mouse Models. Science 335, 1503–1506 (2012).
123. Elgersma, Y. et al. Inhibitory autophosphorylation of CaMKII controls PSD association, plasticity, and learning. Neuron 36, 493–505 (2002).
124. Cools, R., Clark, L., Owen, A. M. & Robbins, T. W. Defining the Neural Mechanisms of Probabilistic Reversal Learning Using Event-Related Functional Magnetic Resonance Imaging. J. Neurosci. 22, 4563–4567 (2002).
125. Hornak, J. et al. Reward-related reversal learning after surgical excisions in orbito-frontal or dorsolateral prefrontal cortex in humans. J. Cogn. Neurosci.
16, 463–478 (2004).
&
cannabinoid-1 receptor antagonist SR141716A. Behav. Brain Res. 161, 164–
168 (2005).
127. Anderson, M. E., Runesson, J., Saar, I., Langel, Ü. & Robinson, J. K. Galanin, through GalR1 but not GalR2 receptors, decreases motivation at times of high appetitive behavior. Behav. Brain Res. 239, 90–93 (2013).
128. Haass, C. & Selkoe, D. J. Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer’s amyloid beta-peptide. Nat. Rev. Mol. Cell Biol.
8, 101–112 (2007).
129. den Ouden, H. E. M. et al. Dissociable effects of dopamine and serotonin on reversal learning. Neuron 80, 1090–100 (2013).
130. Izquierdo, A. & Jentsch, J. D. Reversal learning as a measure of impulsive and compulsive behavior in addictions. Psychopharmacology (Berl). 219,
607–20 (2012).
131. Bari, A. & Robbins, T. W. Inhibition and impulsivity: behavioral and neural basis of response control. Prog. Neurobiol. 108, 44–79 (2013).
132. Hamilton, D. A. & Brigman, J. L. Behavioral flexibility in rats and mice: Contributions of distinct frontocortical regions. Genes. Brain. Behav. 14,
4–21 (2015).
133. Nakayama, D. et al. Frontal association cortex is engaged in stimulus integration during associative learning. Curr. Biol. 25, 117–23 (2015).
134. Garner, J. P., Thogerson, C. M., Würbel, H., Murray, J. D. & Mench, J. A. Animal neuropsychology: validation of the Intra-Dimensional Extra-Dimensional set shifting task for mice. Behav. Brain Res. 173, 53–61 (2006).
135. Remmelink, E. et al. A 1-night operant learning task without
food-restriction differentiates among mouse strains in an automated home-cage environment. Behav. Brain Res. 283, 53–60 (2015).
136. Smolen, P., Zhang, Y. & Byrne, J. H. The right time to learn: mechanisms and optimization of spaced learning. Nat. Rev. Neurosci. 17, 77–88 (2016).
137. Balci, F. et al. High-Throughput Automated Phenotyping of Two Genetic Mouse Models of Huntington’s Disease. PLOS Curr. Huntingt. Dis. 5, (2013).
138. Arnsten, A. F. T., Lin, C. H., Van Dyck, C. H. & Stanhope, K. J. The effects of 5-HT3 receptor antagonists on cognitive performance in aged monkeys.
Neurobiol. Aging 18, 21–28 (1997).
139. Jentsch, J. D., Olausson, P., De La Garza, R. & Taylor, J. R. Impairments of reversal learning and response perseveration after repeated, intermittent cocaine administrations to monkeys. Neuropsychopharmacology 26, 183–
90 (2002).
D3 receptors play a specific role in the reversal of a learned visual
discrimination in monkeys. Neuropsychopharmacology 32, 2125–34 (2007).
141. Blake, D. J., Weir, A., Newey, S. E. & Davies, K. E. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol. Rev. 82,
291–329 (2002).
142. Muntoni, F., Torelli, S. & Ferlini, A. Dystrophin and mutations: one gene, several proteins, multiple phenotypes. Lancet Neurol. 2, 731–740 (2003).
143. Cohen, H. J., Molnar, G. E. & Taft, L. T. The genetic relationship of
progressive muscular dystrophy (Duchenne type) and mental retardation.
Dev. Med. Child Neurol. 10, 754–65 (1968).
144. Cotton, S., Voudouris, N. J. & Greenwood, K. M. Intelligence and Duchenne muscular dystrophy: full-scale, verbal, and performance intelligence quotients. Dev. Med. Child Neurol. 43, 497–501 (2001).
145. Billard, C. et al. Cognitive functions in Duchenne muscular dystrophy: a reappraisal and comparison with spinal muscular atrophy. Neuromuscul.
Disord. 2, 371–8 (1992).
146. Donders, J. & Taneja, C. Neurobehavioral characteristics of children with Duchenne muscular dystrophy. Child Neuropsychol. 15, 295–304 (2009).
147. Donald, K. A. M., Mathema, H., Thomas, K. G. F. & Wilmshurst, J. M. Intellectual and behavioral functioning in a South african cohort of boys with duchenne muscular dystrophy. J. Child Neurol. 26, 963–9 (2011).
148. Hinton, V. J., De Vivo, D. C., Nereo, N. E., Goldstein, E. & Stern, Y. Poor verbal working memory across intellectual level in boys with Duchenne dystrophy. Neurology 54, 2127–32 (2000).
149. Hinton, V. J., De Vivo, D. C., Nereo, N. E., Goldstein, E. & Stern, Y. Selective deficits in verbal working memory associated with a known genetic
etiology: the neuropsychological profile of duchenne muscular dystrophy. J.
Int. Neuropsychol. Soc. 7, 45–54 (2001).
150. Mento, G., Tarantino, V. & Bisiacchi, P. S. The neuropsychological profile of infantile Duchenne muscular dystrophy. Clin. Neuropsychol. 25, 1359–77
(2011).
151. Wicksell, R. K., Kihlgren, M., Melin, L. & Eeg-Olofsson, O. Specific cognitive deficits are common in children with Duchenne muscular dystrophy. Dev.
Med. Child Neurol. 46, 154–9 (2004).
152. Snow, W. M., Anderson, J. E. & Jakobson, L. S. Neuropsychological and neurobehavioral functioning in Duchenne muscular dystrophy: a review.
Neurosci. Biobehav. Rev. 37, 743–52 (2013).
&
with duchenne muscular dystrophy: frequency rate of attention-deficit hyperactivity disorder (ADHD), autism spectrum disorder, and obsessive--compulsive disorder. J. Child Neurol. 23, 477–481 (2008).
154. Banihani, R. et al. Cognitive and Neurobehavioral Profile in Boys With Duchenne Muscular Dystrophy. J. Child Neurol. 30, 1472–1482 (2015).
155. Roccella, M., Pace, R. & De Gregorio, M. T. Psychopathological assessment in children affected by Duchenne de Boulogne muscular dystrophy.
Minerva Pediatr. 55, 267–73, 273–6 (2003).
156. Daoud, F. et al. Analysis of Dp71 contribution in the severity of mental retardation through comparison of Duchenne and Becker patients differing by mutation consequences on Dp71 expression. Hum. Mol. Genet. 18, 3779–
3794 (2009).
157. Moizard, M. P. et al. Are Dp71 and Dp140 brain dystrophin isoforms related to cognitive impairment in Duchenne muscular dystrophy? Am. J. Med.
Genet. 80, 32–41 (1998).
158. Muntoni, F., Mateddu, A., Marchei, F., Clerk, A. & Serra, G. Muscular weakness in the mdx mouse. J. Neurol. Sci. 120, 71–77 (1993).
159. Grounds, M. D., Radley, H. G., Lynch, G. S., Nagaraju, K. & De Luca, A. Towards developing standard operating procedures for pre-clinical testing in the mdx mouse model of Duchenne muscular dystrophy. Neurobiol. Dis.
31, 1–19 (2008).
160. Vaillend, C., Rendon, A., Misslin, R. & Ungerer, A. Influence of dystrophin-gene mutation on mdx mouse behavior. I. Retention deficits at long delays in spontaneous alternation and bar-pressing tasks. Behav. Genet. 25, 569–
579 (1995).
161. Turk, R. et al. Muscle regeneration in dystrophin-deficient mdx mice studied by gene expression profiling. BMC Genomics 6, 98 (2005).
162. van Putten, M. et al. The effects of low levels of dystrophin on mouse muscle function and pathology. PLoS One 7, e31937 (2012).
163. Chamberlain, J. S., Metzger, J., Reyes, M., Townsend, D. & Faulkner, J. A. Dystrophin-deficient mdx mice display a reduced life span and are susceptible to spontaneous rhabdomyosarcoma. FASEB J. 21, 2195–2204
(2007).
164. Perronnet, C. & Vaillend, C. Dystrophins, utrophins, and associated scaffolding complexes: Role in mammalian brain and implications for therapeutic strategies. J. Biomed. Biotechnol. 2010, Article ID 849426 (2010).
to executive processes. Neurobiol. Learn. Mem. 124, 111–122 (2015).
166. Loos, M. et al. Neuregulin-3 in the Mouse Medial Prefrontal Cortex Regulates Impulsive Action. Biol. Psychiatry 76, 1–8 (2014).
167. Deacon, R. M. J. & Rawlins, J. N. P. T-maze alternation in the rodent. Nat.
Protoc. 1, 7–12 (2006).
168. Crawley, J. & Goodwin, F. K. Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol. Biochem.
Behav. 13, 167–70 (1980).
169. Manning, J., Kulbida, R., Rai, P. & Jensen, L. Amitriptyline is efficacious in ameliorating muscle inflammation and depressive symptoms in the mdx mouse model of Duchenne muscular dystrophy. Exp. Physiol. 99, 1370–1386
(2014).
170. Sekiguchi, M. et al. A deficit of brain dystrophin impairs specific amygdala GABAergic transmission and enhances defensive behaviour in mice. Brain
132, 124–135 (2009).
171. O’Leary, T. P., Gunn, R. K. & Brown, R. E. What are we measuring when we test strain differences in anxiety in mice? Behav. Genet. 43, 34–50 (2013).
172. Võikar, V., Kõks, S., Vasar, E. & Rauvala, H. Strain and gender differences in the behavior of mouse lines commonly used in transgenic studies. Physiol.
Behav. 72, 271–281 (2001).
173. Ricotti, V. et al. Neurodevelopmental, emotional, and behavioural problems in Duchenne muscular dystrophy in relation to underlying dystrophin gene mutations. Dev. Med. Child Neurol. 58, 77–84 (2016).
174. Pangalila, R. F. et al. Prevalence of fatigue, pain, and affective disorders in adults with duchenne muscular dystrophy and their associations with quality of life. Arch. Phys. Med. Rehabil. 96, 1242–7 (2015).
175. Hendriksen, J., Poysky, J., Schrans, D., Schouten, E. & ALdenkamp, A. Psychosocial Adjustment in Males with Duchenne Muscular Dystrophy: Psychometric Properties and Clinical Utility of a Parent-report
Questionnaire. J. Pediatr. Psychol. 34, 69–78 (2009).
176. Vaillend, C. & Ungerer, A. Behavioral characterization of mdx3cv mice deficient in C-terminal dystrophins. Neuromuscul. Disord. 9, 296–304
(1999).
177. Vaillend, C. et al. Spatial discrimination learning and CA1 hippocampal synaptic plasticity in mdx and mdx3cv mice lacking dystrophin gene products. Neuroscience 86, 53–66 (1998).
&
207–210 (1996).
179. Vaillend, C., Billard, J.-M. & Laroche, S. Impaired long-term spatial and recognition memory and enhanced CA1 hippocampal LTP in the dystrophin-deficient Dmd(mdx) mouse. Neurobiol. Dis. 17, 10–20 (2004).
180. Chang, Q. & Gold, P. E. Switching memory systems during learning: changes in patterns of brain acetylcholine release in the hippocampus and striatum in rats. J. Neurosci. 23, 3001–3005 (2003).
181. Yin, H. H. & Knowlton, B. J. The role of the basal ganglia in habit formation.
Nat. Rev. Neurosci. 7, 464–76 (2006).
182. Lidov, H. G., Byers, T. J., Watkins, S. C. & Kunkel, L. M. Localization of dystrophin to postsynaptic regions of central nervous system cortical neurons. Nature 348, 725–728 (1990).
183. Lidov, H. G. Dystrophin in the nervous system. Brain Pathol. 6, 63–77
(1996).
184. Daoud, F. et al. Role of Mental Retardation-Associated Dystrophin-Gene Product Dp71 in Excitatory Synapse Organization, Synaptic Plasticity and Behavioral Functions. PLoS One 4, e6574 (2009).
185. Doorenweerd, N. et al. Reduced cerebral gray matter and altered white matter in boys with Duchenne muscular dystrophy. Ann. Neurol. 76, 403–11
(2014).
186. Taylor, P. J. et al. Dystrophin gene mutation location and the risk of
cognitive impairment in Duchenne muscular dystrophy. PLoS One 5, e8803
(2010).
187. Bardoni, A. et al. Loss of Dp140 regulatory sequences is associated with cognitive impairment in dystrophinopathies. Neuromuscul. Disord. 10, 194–
199 (2000).
188. Felisari, G. et al. Loss of Dp140 dystrophin isoform and intellectual impairment in Duchenne dystrophy. Neurology 55, 559–64 (2000).
189. Muntoni, F., Mateddu, A. & Serra, G. Passive avoidance behaviour deficit in the mdx mouse. Neuromuscul. Disord. 1, 121–123 (1991).
190. Carretta, D. et al. Spatial analysis reveals alterations of parvalbumin- and calbindin-positive local circuit neurons in the cerebral cortex of mutant mdx mice. Brain Res. 1016, 1–11 (2004).
191. Del Tongo, C., Carretta, D., Fulgenzi, G., Catini, C. & Minciacchi, D.
Parvalbumin-positive GABAergic interneurons are increased in the dorsal hippocampus of the dystrophic mdx mouse. Acta Neuropathol. 118, 803–
812 (2009).
Interneurons are necessary for coordinated activity during reversal learning in orbitofrontal cortex. Biol. Psychiatry 77, 454–464 (2014).
193. Ter Horst, J. P., De Kloet, E. R., Schächinger, H. & Oitzl, M. S. Relevance of stress and female sex hormones for emotion and cognition. Cell. Mol.
Neurobiol. 32, 725–735 (2012).
194. O’Leary, T. P., Savoie, V. & Brown, R. E. Learning, memory and search strategies of inbred mouse strains with different visual abilities in the Barnes maze. Behav. Brain Res. 216, 531–42 (2011).
195. Harrison, F. E., Hosseini, A. H. & McDonald, M. P. Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks.
Behav. Brain Res. 198, 247–251 (2009).
196. Nuechterlein, K. H. et al. Identification of separable cognitive factors in schizophrenia. Schizophr. Res. 72, 29–39 (2004).
197. Castellanos, F. X. & Tannock, R. Neuroscience of attention-deficit/
hyperactivity disorder: the search for endophenotypes. Nat. Rev. Neurosci.
3, 617–628 (2002).
198. Crews, F. T. & Boettiger, C. A. Impulsivity, frontal lobes and risk for addiction. Pharmacol. Biochem. Behav. 93, 237–247 (2009).
199. Steinberg, L. Cognitive and affective development in adolescence. Trends
Cogn. Sci. 9, 69–74 (2005).
200. Robbins, T. W. The 5-choice serial reaction time task: Behavioural
pharmacology and functional neurochemistry. Psychopharmacology (Berl).
163, 362–380 (2002).
201. Bushnell, P. J. & Strupp, B. J. in Methods of Behavior Analysis in
Neuroscience 119–143 (2009).
202. Spear, L. The adolescent brain and age-related behavioural manifestations.
Neuroscience & Biobehavioural Reviews 24, (2000).
203. Laviola, G., Macrì, S., Morley-Fletcher, S. & Adriani, W. Risk-taking behavior in adolescent mice: Psychobiological determinants and early epigenetic influence. Neurosci. Biobehav. Rev. 27, 19–31 (2003).
204. Bradshaw, C. M. & Szabadi, E. Choice between delayed reinforcers in a discrete-trials schedule: The effect of deprivation level. Q. J. Exp. Psychol.
Sect. B 44, 1–16 (2007).
205. Loos, M. et al. Activity and impulsive action are controlled by different genetic and environmental factors. Genes, Brain Behav. 8, 817–828 (2009).
&
Res. 214, 216–24 (2010).
207. Loos, M., Staal, J., Pattij, T., Smit, A. B. & Spijker, S. Independent genetic loci for sensorimotor gating and attentional performance in BXD recombinant inbred strains. Genes. Brain. Behav. 11, 147–56 (2012).
208. Sarter, M. & Bruno, J. P. Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res. Rev. 23, 28–46 (1997).
209. Young, J. W. et al. Reverse translation of the rodent 5C-CPT reveals that the impaired attention of people with schizophrenia is similar to scopolamine-induced deficits in mice. Transl. Psychiatry 3, e324 (2013).
210. Pattij, T. et al. Strain specificity and cholinergic modulation of visuospatial attention in three inbred mouse strains. Genes. Brain. Behav. 6, 579–87
(2007).
211. Siegel, J. A., Benice, T. S., Van Meer, P., Park, B. S. & Raber, J. Acetylcholine receptor and behavioral deficits in mice lacking apolipoprotein E.
Neurobiol. Aging 32, 75–84 (2011).
212. Patel, S., Stolerman, I. P., Asherson, P. & Sluyter, F. Attentional performance of C57BL/6 and DBA/2 mice in the 5-choice serial reaction time task.
Behav. Brain Res. 170, 197–203 (2006).
213. Castellanos, F. X. et al. Varieties of attention-deficit/hyperactivity disorder-related intra-individual variability. Biol. Psychiatry 57, 1416–23 (2005).
214. Di Martino, A. et al. Decomposing intra-subject variability in children with attention-deficit/hyperactivity disorder. Biol. Psychiatry 64, 607–14 (2008).
215. Sanchez-Roige, S., Peña-Oliver, Y. & Stephens, D. N. Measuring impulsivity in mice: the five-choice serial reaction time task. Psychopharmacology
(Berl). 219, 253–70 (2012).
216. Dalley, J. W., Mar, A. C., Economidou, D. & Robbins, T. W. Neurobehavioral mechanisms of impulsivity: fronto-striatal systems and functional
neurochemistry. Pharmacol. Biochem. Behav. 90, 250–60 (2008).
217. Remmelink, E., Smit, A. B., Verhage, M. & Loos, M. Measuring
discrimination- and reversal learning in mouse models within 4 days and without prior food deprivation. Learn. Mem. (Accepted), (2016).
218. Adriani, W. & Laviola, G. Elevated levels of impulsivity and reduced place conditioning with d-amphetamine: two behavioral features of adolescence in mice. Behav Neurosci 117, 695–703 (2003).
219. Pinkston, J. W. & Lamb, R. J. Delay discounting in C57BL/6J and DBA/2J mice: Adolescent-limited and life-persistent patterns of impulsivity. Behav.
Neurosci. 125, 194–201 (2011).
in impulsivity among adolescent and adult Sprague-Dawley rats. Behav.
Neurosci. 126, 735–741 (2012).
221. Lukkes, J. L., Thompson, B. S., Freund, N. & Andersen, S. L. The
developmental inter-relationships between activity, novelty preferences, and delay discounting in male and female rats. Dev. Psychobiol. (2015). doi:10.1002/dev.21368
222. Rubia, K. Functional brain imaging across development. Eur. Child Adolesc.
Psychiatry 22, 719–31 (2013).
223. Sarter, M. & Parikh, V. Choline transporters, cholinergic transmission and cognition. Nat. Rev. Neurosci. 6, 48–56 (2005).
224. Dillon, G. M. et al. Prefrontal cortex lesions and scopolamine impair attention performance of C57BL/6 mice in a novel 2-choice visual discrimination task. Behav. Brain Res. 204, 67–76 (2009).
225. Loos, M., Staal, J., Smit, A. B., De Vries, T. J. & Spijker, S. Enhanced alcohol self-administration and reinstatement in a highly impulsive, inattentive recombinant inbred mouse strain. Front. Behav. Neurosci. 7, 1–10 (2013).
226. Greco, B., Invernizzi, R. W. & Carli, M. Phencyclidine-induced impairment in attention and response control depends on the background genotype of mice: reversal by the mGLU(2/3) receptor agonist LY379268.
Psychopharmacology (Berl). 179, 68–76 (2005).
227. Kim, C. H. et al. The continuous performance test (rCPT) for mice: A novel operant touchscreen test of attentional function. Psychopharmacology
(Berl). 232, 3947–3966 (2015).
228. Hayward, M. D. & Low, M. J. The contribution of endogenous opioids to food reward is dependent on sex and background strain. Neuroscience 144,
17–25 (2007).
229. Gelegen, C., Collier, D. A., Campbell, I. C., Oppelaar, H. & Kas, M. J. H. Behavioral , physiological , and molecular differences in response to dietary restriction in three inbred mouse strains. Am J Physiol Endocrinol Metab 29,
574–581 (2006).
230. Izquierdo, A. et al. Genetic and dopaminergic modulation of reversal learning in a touchscreen-based operant procedure for mice. Behav. Brain
Res. 171, 181–8 (2006).
231. Atalayer, D. & Rowland, N. E. Comparison of C57BL/6 and DBA/2 mice in food motivation and satiety. Physiol. Behav. 99, 679–83 (2010).
&
185 (2002).
233. Cabib, S., Puglisi-Allegra, S. & Ventura, R. The contribution of comparative studies in inbred strains of mice to the understanding of the hyperactive phenotype. Behav. Brain Res. 130, 103–109 (2002).
234. Marks, M. J., O’Connor, M. F., Artman, L. D., Burch, J. B. & Collins, A. C. Chronic scopolamine treatment and brain cholinergic function. Pharmacol.
Biochem. Behav. 20, 771–777 (1984).
235. Begley, C. G. & Ioannidis, J. P. A. Reproducibility in Science: Improving the Standard for Basic and Preclinical Research. Circ. Res. 116, 116–126 (2015).
236. Young, J. W., Powell, S. B., Risbrough, V., Marston, H. M. & Geyer, M. a. Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacol. Ther. 122, 150–202 (2009).
237. Gerlai, R. & Clayton, N. S. Reply. Trends Neurosci. 22, 301–302 (1999).
238. Lustig, C., Kozak, R., Sarter, M., Young, J. W. & Robbins, T. W. CNTRICS final animal model task selection: control of attention. Neurosci. Biobehav.
Rev. 37, 2099–110 (2013).
239. Wilkinson, R. T. Interaction of noise with knowledge of results and sleep deprivation. J. Exp. Psychol. 66, 332–7 (1963).
240. Beck, L. H., Bransome, E. D., Mirsky, A. F., Rosvold, H. E. & Sarason, I. A continuous performance test of brain damage. J. Consult. Psychol. 20, 343–
50 (1956).
241. Chudasama, Y. & Robbins, T. W. Psychopharmacological approaches to modulating attention in the five-choice serial reaction time task: implications for schizophrenia. Psychopharmacology (Berl). 174, 86–98
(2004).
242. Brown, S. B. R. E. et al. Effects of clonidine and scopolamine on multiple target detection in rapid serial visual presentation. Psychopharmacology
(Berl). 233, 341–350 (2016).
243. Loos, M. et al. Within-strain variation in behavior differs consistently between common inbred strains of mice. Mamm. Genome (2015). doi:10.1007/s00335-015-9578-7
244. Salomons, A. R., Arndt, S. S. & Ohl, F. Impact of anxiety profiles on cognitive performance in BALB/c and 129P2 mice. Cogn. Affect. Behav.
Neurosci. 12, 794–803 (2012).
245. Heinrichs, S. C. Mouse feeding behavior: ethology, regulatory mechanisms and utility for mutant phenotyping. Behav. Brain Res. 125, 81–88 (2001).
257–261 (2009).
247. Würbel, H. Behavioral phenotyping enhanced - beyond (environmental) standardization. Genes, Brain Behav. 1, 3–8 (2002).
248. Würbel, H. Behaviour and the standardization fallacy. Nat. Genet. 26, 263
(2000).
249. Staay, F. J. Van Der & Steckler, T. The fallacy of behavioral phenotyping without standardisation. Genes, Brain Behav. 9–13 (2002).
250. Gerlai, R. Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci. 19, 177–181 (1996).
251. Branchi, I. & Ricceri, L. Refining learning and memory assessment in laboratory rodents. An ethological perspective. Ann. Ist. Super. Sanita 40,
231–236 (2004).
252. Vorhees, C. V & Williams, M. T. Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 1, 848–58
(2006).
253. Gaskill, B. N., Lucas, J. R., Pajor, E. a & Garner, J. P. Little and often? Maintaining continued performance in an automated T-maze for mice.
Behav. Processes 86, 272–8 (2011).
254. Richardson, C. A. Automated homecage behavioural analysis and the implementation of the three Rs in research involving mice. Altern. to Lab.
Anim. 40, P7-9 (2012).
255. Spruijt, B. M. & Visser, L. de. Advanced behavioural screening: automated home cage ethology. Drug Discov. Today Technol. 3, 231–237 (2006).
256. Wolfer, D. P. et al. Cage enrichment and mouse behaviour. Nature 432,
821–822 (2004).
257. Sandi, C. & Pinelo-Nava, M. T. Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast. 2007, 78970 (2007).
258. Papaleo, F., Lipska, B. K. & Weinberger, D. R. Mouse models of genetic effects on cognition: relevance to schizophrenia. Neuropharmacology 62,
1204–20 (2012).
259. Popoli, M., Yan, Z., McEwen, B. S. & Sanacora, G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat. Rev.
Neurosci. 13, 22–37 (2012).
260. Mozhui, K. et al. Strain differences in stress responsivity are associated with divergent amygdala gene expression and glutamate-mediated neuronal excitability. J Neurosci 30, 5357–5367 (2010).
&
mouse test. Trends Neurosci. 26, 132–6 (2003).
262. Winter, Y. & Schaefers, A. T. U. A sorting system with automated gates permits individual operant experiments with mice from a social home cage.
