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      Towards large scale automated cage monitoring – Diurnal rhythm and impact of interventions on in-cage activity of C57BL/6J mice recorded 24/7 with a non-disrupting capacitive-based technique

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          Abstract

          Background and aims

          Automated recording of laboratory animal’s home cage behavior is receiving increasing attention since such non-intruding surveillance will aid in the unbiased understanding of animal cage behavior potentially improving animal experimental reproducibility.

          Material and methods

          Here we investigate activity of group held female C57BL/6J mice ( mus musculus) housed in standard Individually Ventilated Cages across three test-sites: Consiglio Nazionale delle Ricerche (CNR, Rome, Italy), The Jackson Laboratory (JAX, Bar Harbor, USA) and Karolinska Insititutet (KI, Stockholm, Sweden). Additionally, comparison of female and male C57BL/6J mice was done at KI. Activity was recorded using a capacitive-based sensor placed non-intrusively on the cage rack under the home cage collecting activity data every 250 msec, 24/7. The data collection was analyzed using non-parametric analysis of variance for longitudinal data comparing sites, weekdays and sex.

          Results

          The system detected an increase in activity preceding and peaking around lights-on followed by a decrease to a rest pattern. At lights off, activity increased substantially displaying a distinct temporal variation across this period. We also documented impact on mouse activity that standard animal handling procedures have, e.g. cage-changes, and show that such procedures are stressors impacting in-cage activity.

          These key observations replicated across the three test-sites, however, it is also clear that, apparently minor local environmental differences generate significant behavioral variances between the sites and within sites across weeks. Comparison of gender revealed differences in activity in the response to cage-change lasting for days in male but not female mice; and apparently also impacting the response to other events such as lights-on in males. Females but not males showed a larger tendency for week-to-week variance in activity possibly reflecting estrous cycling.

          Conclusions

          These data demonstrate that home cage monitoring is scalable and run in real time, providing complementary information for animal welfare measures, experimental design and phenotype characterization.

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          Most cited references29

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          Genetics of mouse behavior: interactions with laboratory environment.

          Strains of mice that show characteristic patterns of behavior are critical for research in neurobehavioral genetics. Possible confounding influences of the laboratory environment were studied in several inbred strains and one null mutant by simultaneous testing in three laboratories on a battery of six behaviors. Apparatus, test protocols, and many environmental variables were rigorously equated. Strains differed markedly in all behaviors, and despite standardization, there were systematic differences in behavior across labs. For some tests, the magnitude of genetic differences depended upon the specific testing lab. Thus, experiments characterizing mutants may yield results that are idiosyncratic to a particular laboratory.
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            Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies.

            Choosing the best genetic strains of mice for developing a new knockout or transgenic mouse requires extensive knowledge of the endogenous traits of inbred strains. Background genes from the parental strains may interact with the mutated gene, in a manner which could severely compromise the interpretation of the mutant phenotype. The present overview summarizes the literature on a wide variety of behavioral traits for the 129, C57BL/6, DBA/2, and many other inbred strains of mice. Strain distributions are described for open field activity, learning and memory tasks, aggression, sexual and parental behaviors, acoustic startle and prepulse inhibition, and the behavioral actions of ethanol, nicotine, cocaine, opiates, antipsychotics, and anxiolytics. Using the referenced information, molecular geneticists can choose optimal parental strains of mice, and perhaps develop new embryonic stem cell progenitors, for new knockouts and transgenics to investigate gene function, and to serve as animal models in the development of novel therapeutics for human genetic diseases.
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              Estrous cycle effects on behavior of C57BL/6J and BALB/cByJ female mice: implications for phenotyping strategies.

              Systematic behavioral phenotyping of genetically modified mice is a powerful method with which to identify the molecular factors implicated in control of animal behavior, with potential relevance for research into neuropsychiatric disorders. A number of such disorders display sex differences, yet the use of female mice in phenotyping strategies has been a rare practice because of the potential variability related to the estrous cycle. We have now investigated the behavioral effects of the estrous cycle in a battery of behavioral tests in C57BL/6J and BALB/cByJ inbred strains of mice. Whereas the performance of BALB/cByJ female mice varied significantly depending on the phase of the estrous cycle in the open field, tail flick and tail suspension tests, the behavior of C57BL/6J females, with the exception of the tail suspension performance, remained stable across all four phases of the estrous cycle in all of the tests including open field, rotarod, startle reflex and pre-pulse inhibition, tail flick and hot plate. We also found that irrespective of the estrous cycle, the behavior of C57BL/6J females was different from that of BALB/cByJ groups in all of the behavioral paradigms. Such strain differences were previously reported in male comparisons, suggesting that the same inter-group differences can be revealed by studying female or male mice. In addition, strain differences were evident even for behaviors that were susceptible to estrous cycle modulations, although their detection might necessitate the constitution of large experimental groups.
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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: Project administrationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Project administrationRole: Writing – review & editing
                Role: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: SupervisionRole: Writing – original draft
                Role: ConceptualizationRole: SupervisionRole: Writing – original draft
                Role: ConceptualizationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                4 February 2019
                2019
                : 14
                : 2
                : e0211063
                Affiliations
                [1 ] Departments of Neuroscience, Karolinska Institutet, Stockholm, Sweden
                [2 ] Tecniplast SpA, Buguggiate (Va), Italy
                [3 ] The Jackson Laboratory, Bar Harbor, Maine, United States of America
                [4 ] National Research Council, CNR-Campus International Development (EMMA-INFRAFRONTIER-IMPC), Monterotondo Scalo, Rome, Italy
                Kent State University, UNITED STATES
                Author notes

                Competing Interests: The authors declare no conflict of interest. Tecniplast SPA (Via I Maggio 6, 21020 Buguggiate (Va), Italy) is a commercial company selling the DVC system. However, this does not alter the authors' adherence to all the PLOS ONE policies on sharing data and materials. We have read the journal's policy and the authors of this manuscript have no competing interests.

                Author information
                http://orcid.org/0000-0001-5037-7461
                Article
                PONE-D-18-24438
                10.1371/journal.pone.0211063
                6361443
                30716111
                de5ec7f2-22b7-4551-a7d3-c5cb85106a13
                © 2019 Pernold et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 19 August 2018
                : 2 January 2019
                Page count
                Figures: 10, Tables: 4, Pages: 20
                Funding
                The work at CNR was supported by Infrafrontier-I3 project under EU contract Grant Agreement Number 312325 of the EC FP7 Capacities Specific Programme at CNR Institute of Cell Biology and Neurobiology and intramural funding to EM. The work at JAX was funded by The Jackson Laboratory. The work at KI was funded by Karolinska Institutet. DVCTM equipment at CNR, JAX and KI, respectively, was made available by Tecniplast SpA. F. Iannello, M. Rigamonti and G. Rosati are employed by Tecniplast SpA. Tecniplast SpA provided support in the form of salaries for authors FI, MR and GR, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Rodents
                Mice
                Physical Sciences
                Materials Science
                Material Properties
                Capacitance
                Research and Analysis Methods
                Bioassays and Physiological Analysis
                Electrophysiological Techniques
                Membrane Electrophysiology
                Electrode Recording
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                Behavior
                Animal Behavior
                Social Sciences
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                Animal Behavior
                Biology and Life Sciences
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                Collective Animal Behavior
                Social Sciences
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                Behavior
                Animal Behavior
                Collective Animal Behavior
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Collective Animal Behavior
                Custom metadata
                All raw data have been deposited at Dryad.org with DOI: doi: 10.5061/dryad.s437221

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