An open-source toolbox for automated phenotyping of mice in behavioral tasks

Frontiers in Behavioral Neuroscience

Volumn 8, Issue OCT, 2014, Pages

  Patel, Tapan P ^a   Gullotti, David M ^a   Hernandez, Pepe ^b   O’Brien, W Timothy ^b   Capehart, Bruce P ^c   Morrison, Barclay ^d   Bass, Cameron ^e   Eberwine, James E ^b   Abel, Ted ^b   Meaney, David F ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NONE   (United States)

^e Duke University   (United States)

Author keywords

Automated behavior; Barnes maze; Blast induced traumatic brain injury; Elk 1 knockout; Social interaction; Spatial object recognition

Indexed keywords

TRANSCRIPTION FACTOR ELK 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASSOCIATIVE MEMORY; AUTOMATION; BEHAVIOR DISORDER; BLAST INJURY; CONTROLLED STUDY; ELEVATED ZERO MAZE TEST; GENE DELETION; GENERALIZED ANXIETY DISORDER; INTERMETHOD COMPARISON; MOTOR COORDINATION; MOUSE; NONHUMAN; NOVEL OBJECT RECOGNITION TEST; OPEN FIELD TEST; OPEN SOURCE TOOLBOX; PHENOTYPE; SCORING SYSTEM; SOCIAL INTERACTION; SPATIAL MEMORY; TRAUMATIC BRAIN INJURY;

EID: 84907765929     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00349     Document Type: Article

References (47)

1. Abel, T., Nguyen, P. V., Barad, M., Deuel, T. A., Kandel, E. R., and Bourtchouladze, R. (1997). Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88, 615-626. doi: 10.1016/S0092-8674(00)81904-2
2. Balderas, I., Rodriguez-Ortiz, C. J., Salgado-Tonda, P., Chavez-Hurtado, J., McGaugh, J. L., and Bermudez-Rattoni, F. (2008). The consolidation of object and context recognition memory involve different regions of the temporal lobe. Learn. Mem. 15, 618-624. doi: 10.1101/lm.1028008
3. Barker, G. R., and Warburton, E. C. (2011). When is the hippocampus involved in recognition memory? J. Neurosci. 31, 10721-10731. doi: 10.1523/JNEUROSCI.6413-10.2011
4. Barrett, L. E., Sul, J. Y., Takano, H., Van Bockstaele, E. J., Haydon, P. G., and Eberwine, J. H. (2006). Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor. Nat. Methods 3, 455-460. doi: 10.1038/nmeth885
5. Besnard, A., Galan-Rodriguez, B., Vanhoutte, P., and Caboche, J. (2011). Elk-1 a transcription factor with multiple facets in the brain. Front. Neurosci. 5:35. doi: 10.3389/fnins.2011.00035
6. Bonasera, S. J., Schenk, A. K., Luxenberg, E. J., and Tecott, L. H. (2008). A novel method for automatic quantification of psychostimulant-evoked route-tracing stereotypy: application to Mus musculus. Psychopharmacology (Berl.) 196, 591-602. doi: 10.1007/s00213-007-0994-6
7. Bourtchuladze, R., Frenguelli, B., Blendy, J., Cioffi, D., Schutz, G., and Silva, A. J. (1994). Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell 79, 59-68. doi: 10.1016/0092-8674(94)90400-6
8. Broadbent, N. J., Squire, L. R., and Clark, R. E. (2004). Spatial memory, recognition memory, and the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 101, 14515-14520. doi: 10.1073/pnas.0406344101
9. Carbonell, W. S., and Mandell, J. W. (2003). Transient neuronal but persistent astroglial activation of ERK/MAP kinase after focal brain injury in mice. J. Neurotrauma 20, 327-336. doi: 10.1089/089771503765172282
10. Casadesus, G., Shukitt-Hale, B., and Joseph, J. A. (2001). Automated measurement of age-related changes in the locomotor response to environmental novelty and home-cage activity. Mech. Ageing Dev. 122, 1887-1897. doi: 10.1016/S0047-6374(01)00324-4
11. Cesari, F., Rennekampff, V., Vintersten, K., Vuong, L. G., Seibler, J., Bode, J., et al. (2004). Elk-1 knock-out mice engineered by Flp recombinase-mediated cassette exchange. Genesis 38, 87-92. doi: 10.1002/gene.20003
12. Chen, S. A., O'dell, L. E., Hoefer, M. E., Greenwell, T. N., Zorrilla, E. P., and Koob, G. F. (2006). Unlimited access to heroin self-administration: independent motivational markers of opiate dependence. Neuropsychopharmacology31, 2692-2707. doi: 10.1038/sj.npp.1301008
13. Choleris, E., Thomas, A. W., Kavaliers, M., and Prato, F. S. (2001). A detailed ethological analysis of the mouse open field test: effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neurosci. Biobehav. Rev. 25, 235-260. doi: 10.1016/S0149-7634(01)00011-2
14. Clifford, S., Young, R., and Williamson, P. (2007). Assessing the early characteristics of autistic disorder using video analysis. J. Autism Dev. Disord. 37, 301-313. doi: 10.1007/s10803-006-0160-8
15. Davenport, N. D., Lim, K. O., Armstrong, M. T., and Sponheim, S. R. (2012). Diffuse and spatially variable white matter disruptions are associated with blast-related mild traumatic brain injury. Neuroimage 59, 2017-2024. doi: 10.1016/j.neuroimage.2011.10.050
16. Defensor, E. B., Pearson, B. L., Pobbe, R. L., Bolivar, V. J., Blanchard, D. C., and Blanchard, R. J. (2011). A novel social proximity test suggests patterns of social avoidance and gaze aversion-like behavior in BTBR T+ tf/J mice. Behav. Brain Res. 217, 302-308. doi: 10.1016/j.bbr.2010.10.033
17. Goldstein, L. E., Fisher, A. M., Tagge, C. A., Zhang, X. L., Velisek, L., Sullivan, J. A., et al. (2012). Chronic traumatic encephalopathy in blast-exposed military veterans and a blast neurotrauma mouse model. Sci. Transl. Med. 4, 134ra160. doi: 10.1126/scitranslmed.3003716
18. Goulding, E. H., Schenk, A. K., Juneja, P., Mackay, A. W., Wade, J. M., and Tecott, L. H. (2008). A robust automated system elucidates mouse home cage behavioral structure. Proc. Natl. Acad. Sci. U.S.A. 105, 20575-20582. doi: 10.1073/pnas.0809053106
19. Gullotti, D. M., Beamer, M., Panzer, M. B., Chen, Y. C., Patel, T. P., Yu, A., et al. (2014). Significant head accelerations can influence immediate neurological impairments in a murine model of blast-induced traumatic brain injury. J. Biomech. Eng. 136, 091004. doi: 10.1115/1.4027873
20. Jacobson, L. H., Bettler, B., Kaupmann, K., and Cryan, J. F. (2007). Behavioral evaluation of mice deficient in GABA(B(1)) receptor isoforms in tests of unconditioned anxiety. Psychopharmacology (Berl.) 190, 541-553. doi: 10.1007/s00213-006-0631-9
21. Jhuang, H., Garrote, E., Mutch, J., Yu, X., Khilnani, V., Poggio, T., et al. (2010). Automated home-cage behavioural phenotyping of mice. Nat. Commun. 1, 68. doi: 10.1038/ncomms1064
22. Joachims, T. (1999). "Making large-scale support vector machine learning practical," in Advances in Kernel Methods, eds B. Schölkopf, C. J. C. Burges, and A. J. Smola (Cambridge: MIT Press), 169-184.
23. Kabra, M., Robie, A. A., Rivera-Alba, M., Branson, S., and Branson, K. (2013). JAABA: interactive machine learning for automatic annotation of animal behavior. Nat. Methods 10, 64-67. doi: 10.1038/nmeth.2281
24. Karlsson, R. M., Holmes, A., Heilig, M., and Crawley, J. N. (2005). Anxiolytic-like actions of centrally-administered neuropeptide Y, but not galanin, in C57BL/6J mice. Pharmacol. Biochem. Behav. 80, 427-436. doi: 10.1016/j.pbb.2004.12.009
25. Levin, H. S., Wilde, E., Troyanskaya, M., Petersen, N. J., Scheibel, R., Newsome, M., et al. (2010). Diffusion tensor imaging of mild to moderate blast-related traumatic brain injury and its sequelae. J. Neurotrauma 27, 683-694. doi: 10.1089/neu.2009.1073
26. Mac Donald, C., Johnson, A., Cooper, D., Malone, T., Sorrell, J., Shimony, J., et al. (2013). Cerebellar white matter abnormalities following primary blast injury in US military personnel. PLoS ONE 8:e55823. doi: 10.1371/journal.pone.0055823
27. Magnuson, J., Leonessa, F., and Ling, G. S. (2012). Neuropathology of explosive blast traumatic brain injury. Curr. Neurol. Neurosci. Rep. 12, 570-579. doi: 10.1007/s11910-012-0303-6
28. Markow, T. A., and Hanson, S. J. (1981). Multivariate analysis of Drosophila courtship. Proc. Natl. Acad. Sci. U.S.A. 78, 430-434. doi: 10.1073/pnas.78.1.430
29. Millecamps, M., Jourdan, D., Leger, S., Etienne, M., Eschalier, A., and Ardid, D. (2005). Circadian pattern of spontaneous behavior in monarthritic rats: a novel global approach to evaluation of chronic pain and treatment effectiveness. Arthritis Rheum. 52, 3470-3478. doi: 10.1002/art.21403
30. Morris, J. F., Sul, J. Y., Kim, M. S., Klein-Szanto, A. J., Schochet, T., Rustgi, A., et al. (2013). Elk-1 phosphorylated at threonine-417 is present in diverse cancers and correlates with differentiation grade of colonic adenocarcinoma. Hum. Pathol. 44, 766-776. doi: 10.1016/j.humpath.2012.08.001
31. Otani, N., Nawashiro, H., Fukui, S., Nomura, N., and Shima, K. (2002). Temporal and spatial profile of phosphorylated mitogen-activated protein kinase pathways after lateral fluid percussion injury in the cortex of the rat brain. J. Neurotrauma 19, 1587-1596. doi: 10.1089/089771502762300247
32. Park, E., Eisen, R., Kinio, A., and Baker, A. J. (2013). Electrophysiological white matter dysfunction and association with neurobehavioral deficits following low-level primary blast trauma. Neurobiol. Dis. 52, 150-159. doi: 10.1016/j.nbd.2012.12.002
33. Phillips, R. G., and Ledoux, J. E. (1992). Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285. doi: 10.1037/0735-7044.106.2.274
34. Prut, L., and Belzung, C. (2003). The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur. J. Pharmacol. 463, 3-33. doi: 10.1016/S0014-2999(03)01272-X
35. Raghupathi, R., Muir, J. K., Fulp, C. T., Pittman, R. N., and McIntosh, T. K. (2003). Acute activation of mitogen-activated protein kinases following traumatic brain injury in the rat: implications for posttraumatic cell death. Exp. Neurol. 183, 438-448. doi: 10.1016/S0014-4886(03)00166-3
36. Rutten, K., Reneerkens, O. A., Hamers, H., Sik, A., McGregor, I. S., Prickaerts, J., et al. (2008). Automated scoring of novel object recognition in rats. J. Neurosci. Methods 171, 72-77. doi: 10.1016/j.jneumeth.2008.02.006
37. Sananbenesi, F., Fischer, A., Schrick, C., Spiess, J., and Radulovic, J. (2002). Phosphorylation of hippocampal Erk-1/2, Elk-1, and p90-Rsk-1 during contextual fear conditioning: interactions between Erk-1/2 and Elk-1. Mol. Cell. Neurosci. 21, 463-476. doi: 10.1006/mcne.2002.1188
38. Sharma, A., Callahan, L. M., Sul, J. Y., Kim, T. K., Barrett, L., Kim, M., et al. (2010). A neurotoxic phosphoform of Elk-1 associates with inclusions from multiple neurodegenerative diseases. PLoS ONE 5:e9002. doi: 10.1371/journal.pone.0009002
39. Simon, P., Dupuis, R., and Costentin, J. (1994). Thigmotaxis as an index of anxiety in mice. Influence of dopaminergic transmissions. Behav. Brain Res. 61, 59-64. doi: 10.1016/0166-4328(94)90008-6
40. Sponheim, S. R., McGuire, K. A., Kang, S. S., Davenport, N. D., Aviyente, S., Bernat, E. M., et al. (2011). Evidence of disrupted functional connectivity in the brain after combat-related blast injury. Neuroimage 54 Suppl. 1, S21-S29. doi: 10.1016/j.neuroimage.2010.09.007
41. Steele, A. D., Jackson, W. S., King, O. D., and Lindquist, S. (2007). 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, 1983-1988. doi: 10.1073/pnas.0610779104
42. Tamborini, P., Sigg, H., and Zbinden, G. (1989). Quantitative analysis of rat activity in the home cage by infrared monitoring. Application to the acute toxicity testing of acetanilide and phenylmercuric acetate. Arch. Toxicol. 63, 85-96. doi: 10.1007/BF00316429
43. Tang, X., Orchard, S. M., and Sanford, L. D. (2002). Home cage activity and behavioral performance in inbred and hybrid mice. Behav. Brain Res. 136, 555-569. doi: 10.1016/S0166-4328(02)00228-0
44. Tang, X., and Sanford, L. D. (2005). Home cage activity and activity-based measures of anxiety in 129P3/J, 129X1/SvJ and C57BL/6J mice. Physiol. Behav. 84, 105-115. doi: 10.1016/j.physbeh.2004.10.017
45. Vekovischeva, O. Y., Verbitskaya, E. V., Aitta-Aho, T., Sandnabba, K., and Korpi, E. R. (2007). Multimetric statistical analysis of behavior in mice selected for high and low levels of isolation-induced male aggression. Behav. Processes 75, 23-32. doi: 10.1016/j.beproc.2007.01.006
46. Vianna, M. R., Alonso, M., Viola, H., Quevedo, J., De Paris, F., Furman, M., et al. (2000). Role of hippocampal signaling pathways in long-term memory formation of a nonassociative learning task in the rat. Learn. Mem. 7, 333-340. doi: 10.1101/lm.34600
47. Yang, S. H., Bumpass, D. C., Perkins, N. D., and Sharrocks, A. D. (2002). The ETS domain transcription factor Elk-1 contains a novel class of repression domain. Mol. Cell. Biol. 22, 5036-5046. doi: 10.1128/MCB.22.14.5036-5046.2002