Structured evaluation of rodent behavioral tests used in drug discovery research

Frontiers in Behavioral Neuroscience

Volumn 8, Issue JULY, 2014, Pages

  Hånell, Anders ^a,b   Marklund, Niklas ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal behavior; Mice; Phenotyping; Rats; Translational medicine

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANXIETY; ARTICLE; COGNITION; CONTROLLED STUDY; DEPRESSION; DRUG DEVELOPMENT; ELEVATED PLUS MAZE TEST; EXPERIMENTAL BEHAVIORAL TEST; INTERNAL VALIDITY; MOTIVATION; NONHUMAN; OPEN FIELD TEST; REPRODUCIBILITY; RODENT; SENSORIMOTOR FUNCTION; SOCIAL INTERACTION; SUBSTANCE ABUSE; VALIDITY;

EID: 84904692829     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00252     Document Type: Article

References (143)

1. Ache, B. W., and Young, J. M. (2005). Olfaction: diverse species, conserved principles. Neuron 48, 417-430. doi: 10.1016/j.neuron.2005.10.022
2. Balkaya, M., Kröber, J. M., Rex, A., and Endres, M. (2013). Assessing post-stroke behavior in mouse models of focal ischemia. J. Cereb. Blood Flow Metab. 33, 330-338. doi: 10.1038/jcbfm.2012.185
3. Barnum, C. J., Blandino, P., and Deak, T. (2008). Social status modulates basal IL-1 concentrations in the hypothalamus of pair-housed rats and influences certain features of stress reactivity. Brain Behav. Immun. 22, 517-527. doi: 10.1016/j.bbi. 2007.10.004
4. Bertoglio, L. J., and Carobrez, A. P. (2002). Behavioral profile of rats submitted to session 1-session 2 in the elevated plus-maze during diurnal/nocturnal phases and under different illumination conditions. Behav. Brain Res. 132, 135-143. doi: 10.1016/s0166-4328(01)00396-5
5. Birrell, J. M., and Brown, V. J. (2000). Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 20, 4320-4324.
6. Blizard, D. A., Weinheimer, V. K., Klein, L. C., Petrill, S. A., Cohen, R., and McClearn, G. E. (2006). "Return to home cage" as a reward for maze learning in young and old genetically heterogeneous mice. Comp. Med. 56, 196-201.
7. Braun, A. A., Skelton, M. R., Vorhees, C. V., and Williams, M. T. (2011). Comparison of the elevated plus and elevated zero mazes in treated and untreated male sprague-dawley rats: effects of anxiolytic and anxiogenic agents. Pharmacol. Biochem. Behav. 97, 406-415. doi: 10.1016/j.pbb.2010.09.013
8. Brooks, S. P., and Dunnett, S. B. (2009). Tests to assess motor phenotype in mice: a user's guide. Nat. Rev. Neurosci. 10, 519-529. doi: 10.1038/nrn2652
9. Bruce-Keller, A. J., Umberger, G., McFall, R., and Mattson, M. P. (1999). Food restriction reduces brain damage and improves behavioral outcome following excitotoxic and metabolic insults. Ann. Neurol. 45, 8-15. doi: 10.1002/1531-8249(199901)45:1<8::aid-art4>3.3.co;2-m
10. Brunner, D., Nestler, E., and Leahy, E. (2002). In need of high-throughput behavioral systems. Drug Discov. Today 7, S107-S112. doi: 10.1016/s1359-6446(02)02423-6
11. Burn, C. C. (2008). What is it like to be a rat? Rat sensory perception and its implications for experimental design and rat welfare. Appl. Anim. Behav. Sci. 112, 1-32. doi: 10.1016/j.applanim.2008.02.007
12. Button, K. S., Ioannidis, J. P. A., Mokrysz, C., Nosek, B. A., Flint, J., Robinson, E. S. J., et al. (2013). Power failure: why small sample size undermines the reliability of neuroscience. Nat. Rev. Neurosci. 14, 365-376. doi: 10.1038/nrn3475
13. Caligioni, C. S. (2009). Assessing reproductive status/stages in mice. Curr. Protoc. Neurosci. Appendix 4, Appendix 4I. doi: 10.1002/0471142301.nsa04is48
14. Cancedda, L., Putignano, E., Sale, A., Viegi, A., Berardi, N., and Maffei, L. (2004). Acceleration of visual system development by environmental enrichment. J. Neurosci. 24, 4840-4848. doi: 10.1523/jneurosci.0845-04.2004
15. Casarrubea, M., Sorbera, F., Santangelo, A., and Crescimanno, G. (2012). The effects of diazepam on the behavioral structure of the rat's response to pain in the hot-plate test: anxiolysis vs. pain modulation. Neuropharmacology 63, 310-321. doi: 10.1016/j.neuropharm.2012.03.026
16. Castelhano-Carlos, M. J., and Baumans, V. (2009). The impact of light, noise, cage cleaning and in-house transport on welfare and stress of laboratory rats. Lab. Anim. 43, 311-327. doi: 10.1258/la.2009.0080098
17. Chen, S.-K., Tvrdik, P., Peden, E., Cho, S., Wu, S., Spangrude, G., et al. (2010). Hematopoietic origin of pathological grooming in Hoxb8 mutant mice. Cell 141, 775-785. doi: 10.1016/j.cell.2010.03.055
18. Chesler, E. J., Wilson, S. G., Lariviere, W. R., Rodriguez-Zas, S. L., and Mogil, J. S. (2002). Influences of laboratory environment on behavior. Nat. Neurosci. 5, 1101-1102. doi: 10.1038/nn1102-1101
19. Chia, R., Achilli, F., Festing, M. F. W., and Fisher, E. M. C. (2005). The origins and uses of mouse outbred stocks. Nat. Genet. 37, 1181-1186. doi: 10.1038/ ng1665
20. Clause, A., Nguyen, T., and Kandler, K. (2011). An acoustic startle-based method of assessing frequency discrimination in mice. J. Neurosci. Methods 200, 63-67. doi: 10.1016/j.jneumeth.2011.05.027
21. Clifton, P. G. (2000). Meal patterning in rodents: psychopharmacological and neuroanatomical studies. Neurosci. Biobehav. Rev. 24, 213-222. doi: 10.1016/s0149-7634(99)00074-3
22. Cook, M. N., Crounse, M., and Flaherty, L. (2002). Anxiety in the elevated zeromaze is augmented in mice after repeated daily exposure. Behav. Genet. 32, 113-118. doi: 10.1023/A:1015249706579
23. Costa-Pinto, F. A., Cohn, D. W. H., Sa-Rocha, V. M., Sa-Rocha, L. C., and PalermoNeto, J. (2009). Behavior: a relevant tool for brain-immune system interaction studies. Ann. N Y Acad. Sci. 1153, 107-119. doi: 10.1111/j.1749-6632.2008. 03961.x
24. Crabbe, J. C., and Morris, R. G. M. (2004). Festina lente: late-night thoughts on high-throughput screening of mouse behavior. Nat. Neurosci. 7, 1175-1179. doi: 10.1038/nn1343
25. Crabbe, J. C., Wahlsten, D., and Dudek, B. C. (1999). Genetics of mouse behavior: interactions with laboratory environment. Science 284, 1670-1672. doi: 10. 1126/science.284.5420.1670
26. Crawley, J., and Goodwin, F. K. (1980). Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol. Biochem. Behav. 13, 167-170. doi: 10.1016/0091-3057(80)90067-2
27. Cryan, J. F., Mombereau, C., and Vassout, A. (2005). The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci. Biobehav. Rev. 29, 571-625. doi: 10.1016/j. neubiorev.2005.03.009
28. D'Ausilio, A. (2012). Arduino: a low-cost multipurpose lab equipment. Behav. Res. Methods 44, 305-313. doi: 10.3758/s13428-011-0163-z
29. Dalal, S. J., Estep, J. S., Valentin-Bon, I. E., and Jerse, A. E. (2001). Standardization of the whitten effect to induce susceptibility to Neisseria gonorrhoeae in female mice. Contemp. Top. Lab. Anim. Sci. 40, 13-17.
30. Davis, J. F., Krause, E. G., Melhorn, S. J., Sakai, R. R., and Benoit, S. C. (2009). Dominant rats are natural risk takers and display increased motivation for food reward. Neuroscience 162, 23-30. doi: 10.1016/j.neuroscience.2009. 04.039
31. Deacon, R. (2012). Assessing burrowing, nest construction and hoarding in mice. J. Vis. Exp. e2607. doi: 10.3791/2607
32. Deacon, R. (2013). The successive alleys test of anxiety in mice and rats. J. Vis. Exp. e2705. doi: 10.3791/2705
33. de Visser, L., van den Bos, R., Kuurman, W. W., Kas, M. J. H., and Spruijt, B. M. (2006). Novel approach to the behavioural characterization of inbred mice: automated home cage observations. Genes Brain Behav. 5, 458-466. doi: 10. 1111/j.1601-183x.2005.00181.x
34. Dews, P. B., Estes, W. K., Morse, W. H., Quine, W. V., and Herrnstein, R. J. (1994). Memorial minute for B. F. Skinner. Behav. Anal. 17, 2-5.
35. Diamond, M. E., von Heimendahl, M., Knutsen, P. M., Kleinfeld, D., and Ahissar, E. (2008). "Where" and "what" in the whisker sensorimotor system. Nat. Rev. Neurosci. 9, 601-612. doi: 10.1038/nrn2411
36. Dunham, N. W., and Miya, T. S. (1957). A note on a simple apparatus for detecting neurological deficit in rats and mice. J. Am. Pharm. Assoc. Am. Pharm. Assoc. (Baltim) 46, 208-249. doi: 10.1002/jps.3030460322
37. Ekmark-Lewén, S., Lewén, A., Meyerson, B. J., and Hillered, L. (2010). The multivariate concentric square field test reveals behavioral profiles of risk taking, exploration and cognitive impairment in mice subjected to traumatic brain injury. J. Neurotrauma 27, 1643-1655. doi: 10.1089/neu.2009.0953
38. Emond, M., Faubert, S., and Perkins, M. (2003). Social conflict reduction program for male mice. Contemp. Top. Lab. Anim. Sci. 42, 24-26.
39. Engelmann, M., Ebner, K., Landgraf, R., and Wotjak, C. T. (2006). Effects of Morris water maze testing on the neuroendocrine stress response and intrahypothalamic release of vasopressin and oxytocin in the rat. Horm. Behav. 50, 496-501. doi: 10.1016/j.yhbeh.2006.04.009
40. Espejo, E. F., and Mir, D. (1994). Differential effects of weekly and daily exposure to the hot plate on the rat's behavior. Physiol. Behav. 55, 1157-1162. doi: 10. 1016/0031-9384(94)90404-9
41. Festing, M. F. W., and Altman, D. G. (2002). Guidelines for the design and statistical analysis of experiments using laboratory animals. ILAR J. 43, 244-258. doi: 10. 1093/ilar.43.4.244
42. Filli, L., and Schwab, M. E. (2012). The rocky road to translation in spinal cord repair. Ann. Neurol. 72, 491-501. doi: 10.1002/ana.23630
43. Fonio, E., Golani, I., and Benjamini, Y. (2012). Measuring behavior of animal models: faults and remedies. Nat. Methods 9, 1167-1170. doi: 10.1038/nmeth. 2252
44. Foster, J. A., and McVey Neufeld, K.-A. (2013). Gut-brain axis: how the microbiome influences anxiety and depression. Trends Neurosci. 36, 305-312. doi: 10.3410/f. 718013229.793477291
45. Freund, J., Brandmaier, A. M., Lewejohann, L., Kirste, I., Kritzler, M., Krüger, A., et al. (2013). Emergence of individuality in genetically identical mice. Science 340, 756-759. doi: 10.1126/science.1235294
46. Gilmour, G., Arguello, A., Bari, A., Brown, V. J., Carter, C., Floresco, S. B., et al. (2013). Measuring the construct of executive control in schizophrenia: defining and validating translational animal paradigms for discovery research. Neurosci. Biobehav. Rev. 37, 2125-2140. doi: 10.1016/j.neubiorev.2012.04.006
47. Gray, P. H. (1973). Comparative psychology and ethology: a saga of twins reared apart. Ann. N Y Acad. Sci. 223, 49-53. doi: 10.1111/j.1749-6632.1973. tb41417.x
48. Guccione, L., Djouma, E., Penman, J., and Paolini, A. G. (2013). Calorie restriction inhibits relapse behaviour and preference for alcohol within a two-bottle free choice paradigm in the alcohol preferring (iP) rat. Physiol. Behav. 110C-111C, 34-41. doi: 10.1016/j.physbeh.2012.11.011
49. Hall, C. S. (1934). Emotional behavior in the rat. I. Defecation and urination as measures of individual differences in emotionality. J. Comp. Psychol. 18, 385-403. doi: 10.1037/h0071444
50. Harrison, F. E., Hosseini, A. H., and McDonald, M. P. (2009). Endogenous anxiety and stress responses in water maze and Barnes maze spatial memory tasks. Behav. Brain Res. 198, 247-251. doi: 10.1016/j.bbr.2008.10.015
51. Hopkins, M. E., and Bucci, D. J. (2010). Interpreting the effects of exercise on fear conditioning: the influence of time of day. Behav. Neurosci. 124, 868-872. doi: 10.1037/a0021200
52. Horner, A. E., Heath, C. J., Hvoslef-Eide, M., Kent, B. A., Kim, C. H., Nilsson, S. R. O., et al. (2013). The touchscreen operant platform for testing learning and memory in rats and mice. Nat. Protoc. 8, 1961-1984. doi: 10.1038/nprot. 2013.122
53. Huberman, A. D., and Niell, C. M. (2011). What can mice tell us about how vision works? Trends Neurosci. 34, 464-473. doi: 10.1016/j.tins.2011.07.002
54. Hurst, J. L., and West, R. S. (2010). Taming anxiety in laboratory mice. Nat. Methods 7, 825-826. doi: 10.1038/nmeth.1500
55. Jacob, H. J., Lazar, J., Dwinell, M. R., Moreno, C., and Geurts, A. M. (2010). Gene targeting in the rat: advances and opportunities. Trends Genet. 26, 510-518. doi: 10.1016/j.tig.2010.08.006
56. Johansen, J. P., Cain, C. K., Ostroff, L. E., and LeDoux, J. E. (2011). Molecular mechanisms of fear learning and memory. Cell 147, 509-524. doi: 10.1016/j.cell. 2011.10.009
57. Jones, N. (2012). Science in three dimensions: the print revolution. Nature 487, 22-23. doi: 10.1038/487022a
58. Kääriäinen, T. M., Käenmäki, M., Forsberg, M. M., Oinas, N., Tammimäki, A., and Männistö, P. T. (2011). Unpredictable rotational responses to L-dopa in the rat model of Parkinson's disease: the role of L-dopa pharmacokinetics and striatal dopamine depletion. Basic Clin. Pharmacol. Toxicol. 110, 162-170. doi: 10. 1111/j.1742-7843.2011.00782.x. [Epub ahead of print].
59. 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
60. Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M., and Altman, D. G. (2010). Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 8:e1000412. doi: 10.1371/journal.pbio. 1000412
61. Kim, D.-E., Kim, J.-Y., Nahrendorf, M., Lee, S.-K., Ryu, J. H., Kim, K., et al. (2011). Direct thrombus imaging as a means to control the variability of mouse embolic infarct models: the role of optical molecular imaging. Stroke 42, 3566-3573. doi: 10.1161/strokeaha.111.629428
62. Krackow, S., Vannoni, E., Codita, A., Mohammed, A. H., Cirulli, F., Branchi, I., et al. (2010). Consistent behavioral phenotype differences between inbred mouse strains in the IntelliCage. Genes Brain Behav. 9, 722-731. doi: 10.1111/j.1601-183x.2010.00606.x
63. Krzywinski, M., and Altman, N. (2013). Points of significance: importance of being uncertain. Nat. Methods 10, 809-810. doi: 10.1038/nmeth.2613
64. Lathe, R. (2004). The individuality of mice. Genes Brain Behav. 3, 317-327. doi: 10. 1111/j.1601-183X.2004.00083.x
65. Lenzlinger, P. M., Shimizu, S., Marklund, N., Thompson, H. J., Schwab, M. E., Saatman, K. E., et al. (2005). Delayed inhibition of Nogo-A does not alter injury-induced axonal sprouting but enhances recovery of cognitive function following experimental traumatic brain injury in rats. Neuroscience 134, 1047-1056. doi: 10.1016/j.neuroscience.2005.04.048
66. Lewejohann, L., Hoppmann, A. M., Kegel, P., Kritzler, M., Krüger, A., and Sachser, N. (2009). Behavioral phenotyping of a murine model of Alzheimer's disease in a seminaturalistic environment using RFID tracking. Behav. Res. Methods 41, 850-856. doi: 10.3758/BRM.41.3.850
67. Liu, D., Diorio, J., Day, J. C., Francis, D. D., and Meaney, M. J. (2000). Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat. Neurosci. 3, 799-806. doi: 10.1038/77702
68. Lo, E. H. (2008). Experimental models, neurovascular mechanisms and translational issues in stroke research. Br. J. Pharmacol. 153(Suppl. 1), S396-S405. doi: 10.1038/sj.bjp.0707626
69. Loane, D. J., and Faden, A. I. (2010). Neuroprotection for traumatic brain injury: translational challenges and emerging therapeutic strategies. Trends Pharmacol. Sci. 31, 596-604. doi: 10.1016/j.tips.2010.09.005
70. Macleod, M. R., Fisher, M., O'Collins, V., Sena, E. S., Dirnagl, U., Bath, P. M. W., et al. (2009). Good laboratory practice: preventing introduction of bias at the bench. Stroke 40, e50-e52. doi: 10.1161/STROKEAHA.108.525386
71. Mandillo, S., Tucci, V., Hölter, S. M., Meziane, H., Banchaabouchi, M. A., Kallnik, M., et al. (2008). Reliability, robustness and reproducibility in mouse behavioral phenotyping: a cross-laboratory study. Physiol. Genomics 34, 243-255. doi: 10. 1152/physiolgenomics.90207.2008
72. Mao, J. (2009). Translational pain research: achievements and challenges. J. Pain 10, 1001-1011. doi: 10.1016/j.jpain.2009.06.002
73. Maren, S. (2008). Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. Eur. J. Neurosci. 28, 1661-1666. doi: 10.1111/j.1460-9568.2008.06485.x
74. Martens, K. M., Vonder Haar, C., Hutsell, B. A., and Hoane, M. R. (2013). The dig task: a simple scent discrimination reveals deficits following frontal brain damage. J. Vis. Exp. e50033. doi: 10.3791/50033
75. Martin, B., Ji, S., Maudsley, S., and Mattson, M. P. (2010). "Control" laboratory rodents are metabolically morbid: why it matters. Proc. Natl. Acad. Sci. U S A 107, 6127-6133. doi: 10.1073/pnas.0912955107
76. McCall, R. B., Lester, M. L., and Corter, C. M. (1969). Caretaker effect in rats. Dev. Psychol. 1, 771. doi: 10.1037/h0028199
77. McCoy, G. W. (1909). A preliminary report on tumors found in wild rats. J. Med. Res. 21, 285-296.
78. McNamara, K. C. S., Lisembee, A. M., and Lifshitz, J. (2010). The whisker nuisance task identifies a late-onset, persistent sensory sensitivity in diffuse brain-injured rats. J. Neurotrauma 27, 695-706. doi: 10.1089/neu.2009.1237
79. Meaney, M. J. (2001). Maternal care, gene expression and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci. 24, 1161-1192. doi: 10.1146/annurev.neuro.24.1.1161
80. Merlot, E., Moze, E., Bartolomucci, A., Dantzer, R., and Neveu, P. J. (2004). The rank assessed in a food competition test influences subsequent reactivity Frontiers in Behavioral Neuroscience www.frontiersin.org July 2014 {pipe} Volume 8 {pipe} Article to immune and social challenges in mice. Brain Behav. Immun. 18, 468-475. doi: 10.1016/j.bbi.2003.11.007
81. Meyerson, B. J., Augustsson, H., Berg, M., and Roman, E. (2006). The Concentric square field: a multivariate test arena for analysis of explorative strategies. Behav. Brain Res. 168, 100-113. doi: 10.1016/j.bbr.2005.10.020
82. Meziane, H., Ouagazzal, A. M., Aubert, L., Wietrzych, M., and Krezel, W. (2007). Estrous cycle effects on behavior of C57BL/6J and BALB/cByJ female mice: implications for phenotyping strategies. Genes Brain Behav. 6, 192-200. doi: 10. 1111/j.1601-183x.2006.00249.x
83. Moscarello, J. M., and LeDoux, J. E. (2013). Active avoidance learning requires prefrontal suppression of amygdala-mediated defensive reactions. J. Neurosci. 33, 3815-3823. doi: 10.1523/JNEUROSCI.2596-12.2013
84. Muheim, R., Edgar, N. M., Sloan, K. A., and Phillips, J. B. (2006). Magnetic compass orientation in C57BL/6J mice. Learn. Behav. 34, 366-373. doi: 10.3758/ bf03193201
85. Nadler, J. J., Moy, S. S., Dold, G., Trang, D., Simmons, N., Perez, A., et al. (2004). Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav. 3, 303-314. doi: 10.1111/j.1601-183x.2004.00071.x
86. Neelakantan, H., and Walker, E. A. (2012). Temperature-dependent enhancement of the antinociceptive effects of opioids in combination with gabapentin in mice. Eur. J. Pharmacol. 686, 55-59. doi: 10.1016/j.ejphar.2012.04.042
87. Nithianantharajah, J., and Hannan, A. J. (2006). Enriched environments, experience-dependent plasticity and disorders of the nervous system. Nat. Rev. Neurosci. 7, 697-709. doi: 10.1038/nrn1970
88. O'Connor, C., Heath, D. L., Cernak, I., Nimmo, A. J., and Vink, R. (2003). Effects of daily versus weekly testing and pre-training on the assessment of neurologic impairment following diffuse traumatic brain injury in rats. J. Neurotrauma 20, 985-993. doi: 10.1089/089771503770195830
89. Ohl, F., and Keck, M. E. (2003). Behavioural screening in mutagenised mice-in search for novel animal models of psychiatric disorders. Eur. J. Pharmacol. 480, 219-228. doi: 10.1016/j.ejphar.2003.08.108
90. Pellow, S., and File, S. E. (1986). Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol. Biochem. Behav. 24, 525-529. doi: 10.1016/0091-3057(86)90552-6
91. Petrovich, G. D., Ross, C. A., Mody, P., Holland, P. C., and Gallagher, M. (2009). Central, but not basolateral, amygdala is critical for control of feeding by aversive learned cues. J. Neurosci. 29, 15205-15212. doi: 10.1523/JNEUROSCI.3656-09. 2009
92. Porsolt, R. D., Bertin, A., and Jalfre, M. (1977). Behavioral despair in mice: a primary screening test for antidepressants. Arch. Int. Pharmacodyn. Ther. 229, 327-336.
93. Prendergast, B. J., Onishi, K. G., and Zucker, I. (2014). Female mice liberated for inclusion in neuroscience and biomedical research. Neurosci. Biobehav. Rev. 40, 1-5. doi: 10.1016/j.neubiorev.2014.01.001
94. Prusky, G. T., Alam, N. M., Beekman, S., and Douglas, R. M. (2004). Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest. Ophthalmol. Vis. Sci. 45, 4611-4616. doi: 10.1167/iovs.04-0541
95. Quatrale, R. P., and Laden, K. (1968). Solute and water secretion by the eccrine sweat glands of the rat. J. Invest. Dermatol. 51, 502-504. doi: 10.1038/jid. 1968.81
96. Ramos, A., Pereira, E., Martins, G. C., Wehrmeister, T. D., and Izídio, G. S. (2008). Integrating the open field, elevated plus maze and light/dark box to assess different types of emotional behaviors in one single trial. Behav. Brain Res. 193, 277-288. doi: 10.1016/j.bbr.2008.06.007
97. Rampon, C., Tang, Y. P., Goodhouse, J., Shimizu, E., Kyin, M., and Tsien, J. Z. (2000). Enrichment induces structural changes and recovery from nonspatial memory deficits in CA1 NMDAR1-knockout mice. Nat. Neurosci. 3, 238-244. doi: 10.1038/72945
98. Richter, S. H., Garner, J. P., Auer, C., Kunert, J., and Würbel, H. (2010). Systematic variation improves reproducibility of animal experiments. Nat. Methods 7, 167-168. doi: 10.1038/nmeth0310-167
99. Rosenzweig, M. R., Riley, D. A., and Krech, D. (1955). Evidence for echolocation in the rat. Science 121:600. doi: 10.1126/science.121.3147.600
100. Rousson, V. (2011). Assessing inter-rater reliability when the raters are fixed: two concepts and two estimates. Biom. J. 53, 477-490. doi: 10.1002/bimj.201000066
101. Russell, W. M. S., and Burch, R. L. (1959). The Principles of Humane Experimental Technique. Wheathampstaed: Universities Federation for Animal Welfare.
102. Ryan, B. C., and Vandenbergh, J. G. (2002). Intrauterine position effects. Neurosci. Biobehav. Rev. 26, 665-678. doi: 10.1016/s0149-7634(02)00038-6
103. Samoilov, V. O. (2007). Ivan petrovich pavlov(1849-1936). J. Hist. Neurosci. 16, 74-89. doi: 10.1080/09647040600793232
104. Savonenko, A. V., Melnikova, T., Hiatt, A., Li, T., Worley, P. F., Troncoso, J. C., et al. (2012). Alzheimer's therapeutics: translation of preclinical science to clinical drug development. Neuropsychopharmacology 37, 261-277. doi: 10.1038/npp. 2011.211
105. Schaefers, A. T. U., and Winter, Y. (2011). Rapid task acquisition of spatial-delayed alternation in an automated T-maze by mice. Behav. Brain Res. 225, 56-62. doi: 10.1016/j.bbr.2011.06.032
106. Schallert, T. (2006). Behavioral tests for preclinical intervention assessment. NeuroRx 3, 497-504. doi: 10.1016/j.nurx.2006.08.001
107. Schallert, T., Fleming, S. M., Leasure, J. L., Tillerson, J. L., and Bland, S. T. (2000). CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39, 777-787. doi: 10.1016/s0028-3908(00)00005-8
108. Schallert, T., Woodlee, M. T., and Fleming, S. M. (2002). "Disentangling multiple types of recovery from brain injury recovery of function, " in Pharmacology of Cerebral Ischemia, eds J. Krigelstein and S. Klumpp (Stuttgart: Medpharm Scientific Publishers), 201-216.
109. Schallert, T., Woodlee, M. T., and Fleming, S. M. (2003). Experimental focal ischemic injury: behavior-brain interactions and issues of animal handling and housing. ILAR J. 44, 130-143. doi: 10.1093/ilar.44.2.130
110. Schmitt, U., and Hiemke, C. (1998). Strain differences in open-field and elevated plus-maze behavior of rats without and with pretest handling. Pharmacol. Biochem. Behav. 59, 807-811. doi: 10.1016/s0091-3057(97)00502-9
111. Sena, E., van der Worp, H. B., Howells, D., and Macleod, M. (2007). How can we improve the pre-clinical development of drugs for stroke? Trends Neurosci. 30, 433-439. doi: 10.1016/j.tins.2007.06.009
112. Shemesh, Y., Sztainberg, Y., Forkosh, O., Shlapobersky, T., Chen, A., and Schneidman, E. (2013). High-order social interactions in groups of mice. Elife 2:e00759. doi: 10.7554/eLife.00759
113. Shepherd, J. K., Grewal, S. S., Fletcher, A., Bill, D. J., and Dourish, C. T. (1994). Behavioural and pharmacological characterisation of the elevated "zero-maze" as an animal model of anxiety. Psychopharmacology (Berl) 116, 56-64. doi: 10. 1007/bf02244871
114. Shimamura, M., Kuratani, K., and Kinoshita, M. (2007). A new automated and high-throughput system for analysis of the forced swim test in mice based on magnetic field changes. J. Pharmacol. Toxicol. Methods 55, 332-336. doi: 10. 1016/j.vascn.2006.11.003
115. Shrout, P. E., and Fleiss, J. L. (1979). Intraclass correlations: uses in assessing rater reliability. Psychol. Bull. 86, 420-428. doi: 10.1037/0033-2909.86.2.420
116. Sorge, R. E., Martin, L. J., Isbester, K. A., Sotocinal, S. G., Rosen, S., Tuttle, A. H., et al. (2014). Olfactory exposure to males, including men, causes stress and related analgesia in rodents. Nat. Methods 11, 629-632. doi: 10.1038/nmeth.2935
117. Staples, L. G. (2010). Predator odor avoidance as a rodent model of anxiety: learning-mediated consequences beyond the initial exposure. Neurobiol. Learn. Mem. 94, 435-445. doi: 10.1016/j.nlm.2010.09.009
118. Strauss, M. E., and Smith, G. T. (2009). Construct validity: advances in theory and methodology. Annu. Rev. Clin. Psychol. 5, 1-25. doi: 10.1146/annurev.clinpsy. 032408.153639
119. Steensma, D. P., Kyle, R. A., and Shampo, M. A. (2010). Abbie Lathrop, the "mouse woman of Granby": rodent fancier and accidental genetics pioneer. Mayo Clin. Proc. 85:e83. doi: 10.4065/mcp.2010.0647
120. Thierry, B. (2010). Darwin as a student of behavior. C. R. Biol. 333, 188-196. doi: 10.1016/j.crvi.2009.12.007
121. Turner, J. G., Parrish, J. L., Hughes, L. F., Toth, L. A., and Caspary, D. M. (2005). Hearing in laboratory animals: strain differences and nonauditory effects of noise. Comp. Med. 55, 12-23.
122. van der Staay, F. J., and Steckler, T. (2002). The fallacy of behavioral phenotyping without standardisation. Genes Brain Behav. 1, 9-13. doi: 10.1046/j.1601-1848. 2001.00007.x
123. van Driel, K. S., and Talling, J. C. (2005). Familiarity increases consistency in animal tests. Behav. Brain Res. 159, 243-245. doi: 10.1016/j.bbr.2004.11.005
124. Võikar, V., Polus, A., Vasar, E., and Rauvala, H. (2005). Long-term individual housing in C57BL/6J and DBA/2 mice: assessment of behavioral consequences. Genes Brain Behav. 4, 240-252. doi: 10.1111/j.1601-183x.2004.00106.x
125. Vorhees, C. V., and Williams, M. T. (2006). Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 1, 848-858. doi: 10.1038/nprot.2006.116
126. Wahlsten, D., Metten, P., and Crabbe, J. C. (2003a). A rating scale for wildness and ease of handling laboratory mice: results for 21 inbred strains tested in two laboratories. Genes Brain Behav. 2, 71-79. doi: 10.1034/j.1601-183x.2003. 00012.x
127. Wahlsten, D., Metten, P., Phillips, T. J., Boehm, S. L., Burkhart-Kasch, S., Dorow, J., et al. (2003b). Different data from different labs: lessons from studies of gene-environment interaction. J. Neurobiol. 54, 283-311. doi: 10.1002/neu. 10173
128. Wahlsten, D., Rustay, N. R., Metten, P., and Crabbe, J. C. (2003c). In search of a better mouse test. Trends Neurosci. 26, 132-136. doi: 10.1016/s0166-2236(03)00033-x
129. Walczak, J.-S., and Beaulieu, P. (2006). Comparison of three models of neuropathic pain in mice using a new method to assess cold allodynia: the double plate technique. Neurosci. Lett. 399, 240-244. doi: 10.1016/j.neulet.2006.01.058
130. Wang, F., Zhu, J., Zhu, H., Zhang, Q., Lin, Z., and Hu, H. (2011). Bidirectional control of social hierarchy by synaptic efficacy in medial prefrontal cortex. Science 334, 693-697. doi: 10.1126/science.1209951
131. Whishaw, I. Q., Coles, B. L., and Bellerive, C. H. (1995). Food carrying: a new method for naturalistic studies of spontaneous and forced alternation. J. Neurosci. Methods 61, 139-143. doi: 10.1016/0165-0270(95)00035-s
132. Whitten, W. K. (1956). Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J. Endocrinol. 13, 399-404. doi: 10.1677/joe.0. 0130399
133. Winter, Y., and Schaefers, A. T. U. (2011). A sorting system with automated gates permits individual operant experiments with mice from a social home cage. J. Neurosci. Methods 196, 276-280. doi: 10.1016/j.jneumeth.2011.01.017
134. Wöhr, M., Houx, B., Schwarting, R. K. W., and Spruijt, B. (2008). Effects of experience and context on 50-kHz vocalizations in rats. Physiol. Behav. 93, 766-776. doi: 10.1016/j.physbeh.2007.11.031
135. Wöhr, M., Roullet, F. I., and Crawley, J. N. (2011). Reduced scent marking and ultrasonic vocalizations in the BTBR T+tf/J mouse model of autism. Genes. Brain. Behav. 10, 35-43. doi: 10.1111/j.1601-183x.2010.00582.x
136. Wood, E. R., Dudchenko, P. A., and Eichenbaum, H. (1999). The global record of memory in hippocampal neuronal activity. Nature 397, 613-616. doi: 10. 1038/17605
137. Würbel, H. (2002). Behavioral phenotyping enhanced-beyond (environmental) standardization. Genes. Brain. Behav. 1, 3-8. doi: 10.1046/j.1601-1848.2001. 00006.x
138. Wynne, C. D. L. (2004). The perils of anthropomorphism. Nature 428:606. doi: 10. 1038/428606a
139. Yang, M., and Crawley, J. N. (2009). Simple behavioral assessment of mouse olfaction. Curr. Protoc. Neurosci. Chapter 8:Unit 8.24. doi: 10.1002/0471142301. ns0824s48
140. Yezierski, R. P., and Vierck, C. J. (2011). Should the hot-plate test be reincarnated? J. Pain 12, 936-937; author reply938-939. doi: 10.1016/j.jpain.2011. 05.003
141. Young, J. W., Meves, J. M., and Geyer, M. A. (2013). Nicotinic agonist-induced improvement of vigilance in mice in the 5-choice continuous performance test. Behav. Brain Res. 240, 119-133. doi: 10.1016/j.bbr.2012.11.028
142. Yousuf, S., Atif, F., Sayeed, I., Wang, J., and Stein, D. G. (2013). Post-stroke infections exacerbate ischemic brain injury in middle-aged rats: immunomodulation and neuroprotection by progesterone. Neuroscience 239, 92-102. doi: 10.1016/j. neuroscience.2012.10.017
143. Yu, Z. F., and Mattson, M. P. (1999). Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism. J. Neurosci. Res. 57, 830-839. doi: 10.1002/(sici)1097-4547(19990915)57:6<830::aid-jnr8>3.3.co;2-u