The power of automated behavioural homecage technologies in characterizing disease progression in laboratory mice: A review

Applied Animal Behaviour Science

Volumn 163, Issue , 2015, Pages 19-27

  Richardson, Claire A ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Animal welfare; Automated behavioural analysis; Disease; Humane endpoints; Mice; Replacement, reduction, refinement (3Rs)

Indexed keywords

AUTOMATION; BEHAVIORAL ECOLOGY; BIOMARKER; DISEASE INCIDENCE; DISEASE SEVERITY; PATHOGENICITY; PHENOTYPIC PLASTICITY; RODENT;

ANIMALIA; MUS;

EID: 84921027022     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2014.11.018     Document Type: Review

References (85)

1. American College of Laboratory Animal Medicine Public statement: recommendations for the assessment and management of pain in rabbits and rodents. J. Am. Assoc. Lab. Anim. Sci. 2007, 46:97-108.
2. Arras M., Glauser D.L., Jirkof P., Rettich A., Schade B., Cinelli P., Pinschewer D.D., Ackermann M. Multiparameter telemetry as a sensitive screening method to detect vaccine reactogenicity in mice. PLOS ONE 2012, 7:e29726.
3. Ashall V., Millar K. An opportunity to refocus on the 'humane' in experimental endpoints: moving beyond Directive 2010/63/EU. Altern. Lab. Anim. 2013, 41:307-312.
4. Ashall V., Millar K. Endpoint matrix: a conceptual tool to promote consideration of the multiple dimensions of humane endpoints. ALTEX 2014, 31:209-213.
5. Aubert A. Sickness and behaviour in animals: a motivational perspective. Neurosci. Biobehav. Rev. 1999, 23:1029-1036.
6. Baiguera C., Alghisi M., Pinna A., Belluci A., Benarese M., Porrini V., Pellitteri M., Berini G., Fabene P.F., Sigala S., Spillantini M.G., Liou H.-C., Spano P.F., Pizzi M. Late-onset Parkinonsonism in NFκB/c-Rel-deficient mice. Brain 2012, 135:2750-2765.
7. Balci F., Oakeshott S., Lea Shamy J.L., El-Khodor B., Filppov I., Mushlin R., Port R., Connor D., Paintdakhi A., Menalled L., Ramboz S., Howland D., Kwak S., Brunner D. High-throughput automated phenotying of two genetic mouse models of Huntington's disease. PLoS Curr 2013, 5. 10.1371/currents.hd.124aa0d16753f88215776fba102ceb29.
8. Bellmann-Sickert K., Elling C., Madsen A., Little P., Lundgren K., Gerlach L.-O., Bergmann R., Holst B., Schwartz T., Beck-Sickinger A. Long-acting lipidated analogue of human pancreatic polypeptide is slowly released into circulation. J. Med. Chem. 2011, 54:2658-2667.
9. Benkhelifa-Ziyyat S., Besse A., Roda M., Duque S., Astord S., Carcenac R., Marais T., Barkats M. Intramuscular scAAV9-SMN injection mediates widespread gene delivery to the spinal cord and decreases disease severity in SMA mice. Mol. Therapy 2013, 21:282-290.
10. Brodkin J., Frank D., Grippo R., Hausfater M., Guilinello M., Acherholt N., Gutzen C. Validation and implementation of a novel high-throughput behavioral phenotyping instrument for mice. J. Neurosci. Methods 2014, 224:48-57.
11. Broom D.M. Behaviour and welfare in relation to pathology. Appl. Anim. Behav. Sci. 2006, 97:73-83.
12. Codita A., Gumucio A., Lannfelt L., Gellerfors P., Winblad B., Mohammed A.H., Nilsson L.N.G. Impaired behaviour of female tg-ArcSwe APP mice in the IntelliCage: a longitudinal study. Behav. Brain Res. 2010, 215:83-94.
13. Committee on Recognition and Alleviation of Distress in Laboratory Animals Recognition and Alleviation of Distress in Laboratory Animals 2008, National Academies Press, Washington.
14. Cunningham C., Deacon R., Wells H., Boche D., Waters S., Picanco Diniz C., Scott H., Rawlins J., Perry V. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur. J. Neurosci. 2003, 17:2147-2155.
15. Dallman M.F. Stress and sickness decrease food intake and body weight. How does this happen? When does this adaptive response progress to pain and suffering?. Coping with Challenge: Welfare in Animals Including Humans 2000, 216-301. Dahlem University Press, Berlin. D.M. Broom (Ed.).
16. Dantzer R. Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur. J. Pharmacol. 2004, 500:399-411.
17. de Visser L., van den Bos R., 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. 2006, 5:458-466.
18. Deacon R., Raley J., Perry V., Rawlins J. Burrowing into prion disease. Neuroreport 2001, 12:2053-2057.
19. Dell'Omo G., Vannoni E., Vyssotski A.L., Di Bari M.A., Nonno R., Agrimi U., Lipp H.P. Early behavioural changes in mice infected with BSE and scrapie: automated home cage monitoring reveals prion strain differences. Eur. J. Neurosci. 2002, 16:735-742.
20. D'Mello C., Swain M.G. Liver-brain inflammation axis. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 301:749-761.
21. EU Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Off. J. Eur. Union 2010, L276:33-79.
22. Franco N.H., Correia-Neves M., Olsson I.A.S. Animal welfare studies in murine tuberculosis: assessing progress over a 12-year period and the need for further improvement. PLOS ONE 2012, 7(10):e47723.
23. Franco N.H., Correla-Neves M., Olsson I.A.S. How humane is your endpoint? Refining the science-driven approach for termination of animal studies of chronic infection. PLoS Pathog. 2012, 8:e1002399.
24. Gaskill B.N., Gordon C.J., Pajor E.A., Lucas J.R., Davis J.K., Garner J.P. Impact of nesting material on mouse temperature and physiology. Physiol. Behav. 2013, 110-111:87-95.
25. Goulding E.H., Schenk A.K., Juneja P., MacKay A.W., Wade J.M., Tecott L.H. A robust automated system elucidates mouse home cage behavioral structure. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20575-20582.
26. Grillet N., Pattyn A., Contet C., Kieffer B.L., Goridis C., Brunet J.-F. Generation and characterization of Rgs4 mutant mice. Mol. Cell. Biol. 2005, 25:4221-4228.
27. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 1988, 12:123-137.
28. Hawkins P. Recognizing and assessing pain, suffering and distress in laboratory animals: a survey of current practice in the UK with recommendations. Lab. Anim. 2002, 36:378-395.
29. Hawkins P. Progress in assessing animal welfare in relation to new legislation: opportunities for behavioural researchers. J. Neurosci. Methods 2014, 234:135-138.
30. Hawkins P., Morton D.B., Burman O., Dennison N., Honess P., Jennings M., Lane S., Middleton V., Roughan J.V., Wells S., Westwood K. A guide to defining and implementing protocols for the welfare assessment of laboratory animals: eleventh report of the BVAAWF/FRAME/RSPCA/UFAW Joint Working Group on Refinement. Lab. Anim. 2011, 45:1-13.
31. Home Office Annual Statistics of Scientific Procedures on Living Animals, Great Britain 2012, London 2013, 58.
32. Howerton C.L., Garner J.P., Mench J.A. A system utilizing radio frequency identification (RFID) technology to monitor individual rodent behaviour in complex social settings. J. Neurosci. Methods 2012, 209:74-78.
33. Hudson M. The welfare and scientific advantages of non-invasive imaging of animals used in biomedical research. Anim. Welf. 2005, 14:303-317.
34. Jacobsen K.R., Jørgensen P., Pipper C.B., Steffensen A.M., Hau J., Abelson K.S.P. The utility of fecal corticosterone metabolites and animal welfare assessment protocols as predictive parameters of tumor development and animal welfare in a murine xenograft model. In Vivo 2013, 27:189-196.
35. Jirkof P., Leucht K., Cesarovic N., Caj M., Nicholls F., Rogler G., Arras M., Hausmann M. Burrowing is a sensitive behavioural assay for monitoring general wellbeing during dextran sulfate sodium colitis in laboratory mice. Lab. Anim. 2013, 47:274-283.
36. Kalueff A., Touhimaa P. Grooming analysis for neurobehavioural stress research. Brain Res. Protoc. 2004, 13:151-158.
37. Krackow S., Vannoni E., Codita A., Mohammed A.H., Circulli F., Branchi I., Alleva E., Reichelt A., Willuweit A., Voikar V., Colacicco G., Wolfer D.P., Buschmann J.-U.F., Safi K., Lipp H.-P. Consistent behavioural phenotyping differences between inbred strains in the IntelliCage. Genes Brain Behav. 2010, 9:722-731.
38. Kyzar E., Gaikwad S., Roth A., Green J., Pham M., Stewart A., Liang Y., Kobla V., Kalueff A. Towards high-throughput phenotyping of complex patterned behaviors in rodents: focus on mouse self-grooming and its sequencing. Behav. Brain Res. 2011, 225:426-431.
39. Lewejohann L., Hoppmann A.M., Kegel P., Kritzler M., Krüger N., Sachser N. Behavioral phenotyping of a murine model of Alzheimer's disease in a seminaturalistic environment using RFID TRACKING. Behav. Res. Methods 2009, 41:850-856.
40. Lindsay T., Jonas B., Sevcik M., Kubota K., Halvorson K., Ghilardi J., Kuskowski M., Stelow E., Mukherjee P., Gendler S., Wong G., Mantyh P. Pancreatic cancer pain and its correlation with changes with tumor vasculature, macrophage infiltration, neuronal innervation, body weight and disease progression. Pain 2005, 119:233-246.
41. Littin K., Acevedo A., Browne W., Edgar J., Mendl M., Owen D., Sherwin C., Würbel H., Nicol C. Towards humane end points: behavioural changes precede clinical signs of disease in a Huntington's disease model. Proc. R. Soc. B 2008, 275:1856-1874.
42. Mayer J. Using behaviour analysis to recognize pain in small mammals. Lab Anim. Eur. 2007, 7:16-26.
43. McGonigle P., Ruggeri B. Animal models of human disease: challenges in enabling translation. Biochem. Pharmacol. 2014, 87:162-171.
44. Miller A.L., Flecknell P.A., Leach M.C., Roughan J.V. A comparison of a manual and an automated behavioural analysis method for assessing post-operative pain in mice. Appl. Anim. Behav. Sci. 2011, 131:138-144.
45. Miller A.L., Wright-Williams S.L., Flecknell P.A., Roughan J.V. A comparison of abdominal and scrotal approach methods of vasectomy and the influence of analgesic treatment in laboratory mice. Lab. Anim. 2012, 46:304-310.
46. Mochel F., Durant B., Durr A., Schiffmann R. Altered dopamine and serotonin metabolism in motorically asymptomatic R6/2 mice. PLoS ONE 2011, 6:e18336.
47. Mochel F., Durant B., Meng X., O'Callaghan J., Yu H., Brouillet E., Wheeler V.C., Humbert S., Schiffmann R., Durr A. Early alterations of brain cellular energy homeostasis in Huntington disease models. J. Biol. Chem. 2012, 287:1361-1370.
48. Moretti P., Bouwknecht J.A., Teague R., Paylor R., Zoghbi H. Abnormalities of social interactions and home-cage behaviour in a mouse model of Rett syndrome. Hum. Mol. Genet. 2005, 14:205-220.
49. NC3Rs Humane Endpoints 2013, National Centre for the Replacement, Refinement and Reduction of Animals in Research, https://www.nc3rs.org.uk/humane-endpoints (Richardson, C.A. ; 06-2014) (last accessed 14/12/2014).
50. Oakeshott S., Balci F., Filppov I., Murphy C., Port R., Connor D., Paintdakhi A., LeSauter M., Ramboz S., Kwak S., Howland D., Silver R., Brunner D. Circadian abnormalities in motor activity in a BAC transgenic mouse model of Huntington's disease. PLoS Curr. 2011, 3:RRN1225.
51. Ognibene E., Middei S., Daniele S., Adriani W., Ghiradi O., Capriolo A., Laviola G. Aspects of spatial memory and behavioral disinhibition in Tg2576 transgenic mice as a model of Alzheimer's disease. Behav. Brain Res. 2005, 156:225-232.
52. Olsson I.A.S., Westlund K. More than numbers matter: the effects of social factors on behavior and welfare of laboratory rodents and non-human primates. Appl. Anim. Behav. Sci. 2007, 103:229-254.
53. Olsson I., Nevison C., Patteron-Kane E., Sherwin C., Van de Weerd H., Würbel H. Understanding behaviour: the relevance of ethological approaches in laboratory animal science. Appl. Anim. Behav. Sci. 2003, 81:245-264.
54. Olsson I.A.S., Hansen A.K., Sandøe P. Animal welfare and the refinement of neuroscience research methods - a case study of Huntington's disease models. Lab. Anim. 2008, 42:277-283.
55. Paumier K., Sukoff Rizzo S., Berger Z., Chen Y., Gonzales C., Kaftan E., Li L., Lotarski S., Monaghan M., Shen W., Stolyar P., Vasilyev D., Zaleska M., Hirst W., Dunlop J. Behavioral characterization of A53T mice reveals early and late stage deficits related to Parkinson's disease. PLOS ONE 2013, 8:e70274.
56. Richardson C. Automated homecage behavioural analysis and the implementation of the three Rs in research involving mice. Perspect. Lab. Anim. Sci. 2012, 40:7-9.
57. Richter H., Ambrée O., Lewejohann L., Herring A., Keyvani K., Paulus W., Palme R., Touma C., Schäbitz W.-R., Sachser N. Wheel-running in a transgenic mouse model of Alzheimer's disease: protection or symptom?. Behav. Brain Res. 2008, 190:74-84.
58. Roughan J.V., Wright-Williams S.L., Flecknell P.A. Automated analysis of postoperative behaviour: assessment of HomeCageScan as a novel method to rapidly identify pain and analgesic effects in mice. Lab. Anim. 2009, 43:17-26.
59. Rudenko O., Tkach V., Berezin V., Bock E. Detection of early behavioral markers of Huntington's disease in R6/2 mice employing an automated social home cage. Behav. Brain Res. 2009, 203:188-199.
60. Russell W.M.S., Burch R.L. The Principles of Humane Experimental Technique 1959, Methuen, London.
61. Schaefer A.T., Claridge-Chang A. The surveillance state of behavioral automation. Curr. Opin. Neurobiol. 2012, 22:170-176.
62. Spruijt B.M., DeVisser L. Advanced behavioural screening: automated home cage ethology. Drug Discov. Today: Technol. 2006, 3:231-237.
63. Spruijt B.M., van Hooff J.A., Gispen W.H. Ethology and neurobiology of grooming behavior. Physiol. Rev. 1992, 72:825-852.
64. Steele A.D., Hetz C., Yi C., Jackson W.S., Borkowski A.W., Yuan J., Wollmann R.H., Lindquist S. Prion pathogensis is independent of caspase-12. Prion 2007, 1:243-247.
65. 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. 2007, 104:1983-1988.
66. Steele A.D., King O.D., Jackson W.S., Hetz C., Borkowski A.W., Thielen P., Wollmann R., Lindquist S. Diminishing apoptosis by deletion of Bax or overexpression of BCL-2 does not protect against infectious prion toxicity in vivo. J. Neurosci. 2007, 27:13022-13027.
67. Steele A.D., Hutter G., Jackson W.S., Heppner F.L., Borkowski A.W., King O.D., Raymond G.J., Aguzzi A., Lindquist D.M. Heat shock factor 1 regulates lifespan as distinct from disease onset in prion disease. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:13626-13631.
68. Talavera E.J., Arcaya J.-L., Giraldoth D., Suárez J., Bonilla E. Decrease in spontaneous motor activity and in brain lipid peroxidation in manganese and melatonin treated mice. Neurochem. Res. 1999, 24:705-708.
69. Tecott L.H., Nestler E.J. Neurobehavioral assessment in the information age. Nat. Neurosci. 2004, 7:462-466.
70. Too L., Ball H., McGregoe I., Hunt N. A novel automated test battery reveals enduring behavioural alterations an cognitive impairments in survivors of murine pneumococcal meningitis. Brain Behav. Immun. 2014, 35:107-124.
71. Torres-Lista V., Giménez-Llort L. Impairment of nesting behaviour in 3xTg-AD mice. Behav. Brain Res. 2013, 247:153-157.
72. Urban R., Scherrer G., Goulding E.H., Tecott L.H., Basbaum A. Behavioral indices of ongoing pain are largely unchanged in male mice with tissue or nerve-induced mechanical hypersensitivity. Pain 2011, 152:990-1000.
73. van der Burg J.M.M., Bacos K., Wood N.I., Lindqvist A., Wierup N., Woodman B., Wamsteeker J.I., Smith R., Deierborg T., Kuhar M.J., Bates G.P., Mulder H., Erlanson-Albertsson C., Morton A.J., Brundin P., Petersén Å., Björkqvist M. Increased metabolism in the R6/2 mouse model of Huntington's disease. Neurobiol. Dis. 2008, 29:41-51.
74. van der Worp H.B., Howells D.W., Sena E.S., Porritt M., Rewell S., O'Collins V., Macleod M.R. Can animal models of disease reliably inform human studies?. PLoS Med. 2010, 7:e1000245.
75. van Loo P.L.P., Everse L.A., Bernsen M.R., Baumans V., Hellebrekers L.J., Kruitwagon C.L.J.J., den Otter W. Analgesics in mice used in cancer research: reduction of discomfort?. Lab. Anim. 1997, 31:318-325.
76. Voikar V., Colacicco G., Gruber O., Vannoni E., Lipp H.P., Wolfer D.P. Conditioned response suppression in the IntelliCage: assessment of mouse strain difference and effects of hippocampal and striatal lesions on acquisition and retention of memory. Behav. Brain Res. 2010, 213:304-312.
77. Weary D.M., Huzzey J.M., von Keyserlingk M.A.G. Using behaviour to predict and identify ill health in animals. J. Anim. Sci. 2009, 87:770-777.
78. Weissbrod A., Shapiro A., Vasserman G., Edry L., Dayan M., Yitzhaky A., Hertzberg L., Feinerman O., Kimchi T. Automated long-term tracking of social behavioural phenotyping of animal colonies within a semi-natural environment. Nat. Commun. 2013, 4:2018.
79. Wesson D., Wilson D. Age and gene overexpression interact to abolish nesting behavior in Tg2576 amyloid precursor protein (APP) mice. Behav. Brain Res. 2011, 216:408-413.
80. Whittaker A., Howarth G. Use of spontaneous behaviour measures to assess pain in laboratory rats and mice: how are we progressing?. Appl. Anim. Behav. Sci. 2014, 151:1-12.
81. Winter Y., Schaefers A.T.U. A sorting system with automated gates permits individual operant experiments with mice from a social home cage. J. Neurosci. Methods 2011, 196:276-280.
82. Wong D., Makowska I.J., Weary D.M. Rat aversion to isoflurane versus carbon dioxide. Biol. Lett. 2013, 9. 10.1098/rsbl.2012.1000.
83. Wood N.I., Goodman A.O.G., van der Burg J.M.M., Gazeau V., Brundin P., Björkqvist M., Petersén Å., Tabrizi S.J., Barker R.A., Morton A.J. Increased thirst and drinking in Huntington's disease and the R6/2 mouse. Brain Res. Bull. 2008, 76:70-79.
84. Wright-Williams S.L., Flecknell P.A., Roughan J.V. Comparative effects of vasectomy surgery and buprenorphine treatment on faecal cortisone concentrations and behaviour assessed by manual and automated analysis methods in C57 and C3H mice. Lab. Anim. 2013, 8:e75948.
85. Zarringhalam K., Ka M., Kook Y.H., Terranova J.I., Suh Y., King O.D., Um M. An open system for automatic home-cage behavioural analysis and its application to male and female mouse models of Huntington's disease. Behav. Brain Res. 2012, 229:216-225.