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Research ArticleNew Research, Disorders of the Nervous System

An Automated Home-Cage System to Assess Learning and Performance of a Skilled Motor Task in a Mouse Model of Huntington’s Disease

Cameron L. Woodard, Federico Bolaños, James D. Boyd, Gergely Silasi, Timothy H. Murphy and Lynn A. Raymond
eNeuro 7 September 2017, 4 (5) ENEURO.0141-17.2017; DOI: https://doi.org/10.1523/ENEURO.0141-17.2017
Cameron L. Woodard
1Department of Psychiatry, Kinsmen Laboratory of Neurological Research, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
2Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
3Graduate Program in Neuroscience, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
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Federico Bolaños
1Department of Psychiatry, Kinsmen Laboratory of Neurological Research, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
2Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
3Graduate Program in Neuroscience, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
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James D. Boyd
1Department of Psychiatry, Kinsmen Laboratory of Neurological Research, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
2Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
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Gergely Silasi
4Department of Cellular and Molecular Medicine, Faculty of Medicine, University of Ottawa, Ottawa, Ontario K1H 8M5, Canada
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Timothy H. Murphy
1Department of Psychiatry, Kinsmen Laboratory of Neurological Research, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
2Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
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Lynn A. Raymond
1Department of Psychiatry, Kinsmen Laboratory of Neurological Research, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
2Djavad Mowafaghian Centre for Brain Health, University of British Columbia, Vancouver, British Columbia V6T 1Z3, Canada
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  • Figure 1.
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    Figure 1.

    Apparatus for home-cage assessment of skilled motor learning. A, A small opening on one side of the home-cage allows 24-h access to a chamber containing a metal lever and water spout. Microchipped animals are identified by an RFID reader on entrance into the chamber, allowing for individual tracking and assessment of group-housed animals. B, The lever is restricted in its horizontal movement by two metal posts, and held in starting position by a small counterweight. In the first phase of testing, the mouse must pull the lever backwards 12° from its starting position to receive a water drop. C, A top-down view of the lever position range. In the second phase of testing, the mouse must first pull the lever back to the center (red line), and then hold it within a central goal position range (shaded area) to receive a water drop. The length of time the lever must be held for changes dynamically based on the individual animal’s success rate.

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    Figure 2.

    Acquisition and performance of lever-pull task in phase 1. A, Number of animals to reach the performance criteria of 200 trials performed in phase 1. An overall lower proportion of YAC128 animals acquired the task as assessed by this cutoff. B, Average weight over the course of testing as a percentage of baseline. Although six-month-old animals remained at their baseline weight, two-month-old WT and YAC128 animals and four-month-old YAC128 animals gained weight over 14 d in the lever-cage (asterisks indicate significant increase as compared to baseline weight). C, No significant differences between WT and YAC128 were seen in the number of trials performed per day; however, animals in both genotypes performed less daily trials with increasing age. D, Time spent in the chamber per day was also not significantly different between genotypes; however, both WT and YAC128 animals were much higher on this measure at two months old than at other ages. E, F, Sample lever traces from two four-month-old animals (WT and YAC128, respectively) in phase 1. Each line represents one trial. Numbers of animals (WT/YAC128) used for weight, trial frequency, and time in chamber analysis are n = 17/13 at two months old, n = 14/16 at four months old, and n = 18/12 at six months old. All data are presented as mean ± SEM. ns = not significant; *p < 0.5; **p < 0.01; ***p < 0.001; ****p < 0.0001.

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    Figure 3.

    Distribution of trials throughout the light/dark cycle. A, Raster plots show the distribution of trials through the day for representative four-month-old WT and YAC128 animals on the fifth day of testing (each line represents one trial). B, The average percentage of all trials performed during the dark phase of testing was significantly higher in WT than in YAC128 mice, suggesting a disruption of normal circadian rhythms in these animals. C-E, Trials were split into 1-h bins for each animal, and the percentage of trials occurring in each bin was calculated and graphed for two-, four-, and six-month-old age groups. A significant interaction between genotype and the hour of day was observed for four- and six-month-old, but not two-month-old, animals. Numbers of animals (WT/YAC128) used for analysis are n = 17/13 at two months old, n = 14/16 at four months old, and n = 18/12 at six months old. All data are presented as mean ± SEM. ns = not significant; *p < 0.5; **p < 0.01; ***p < 0.001; ****p < 0.0001.

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    Figure 4.

    Performance of the task during phase 2. A-C, Progression to the maximum required hold duration over the first 500 trials of phase 2 is plotted for two-, four-, and six-month-old age groups. At the end of each 25-trial bin, success rate was calculated over these trials to determine whether the animal met the threshold for their required hold duration to increase. Data are plotted as the required lever hold duration reached at the end of each 25-trial bin. YAC128 mice at two months old, but not other ages, had a significantly slower progression over the first 500 trials as compared to WT controls. D. The majority of animals reached the maximum hold duration within one week, and no significant differences were observed between genotypes. E, Success rate of animals over the first 500 trials of phase 2 is plotted for each age group. Two-month-old YAC128 animals had the lowest average success rate over this period, although no significant main or interaction effects were found. Numbers of animals (WT/YAC128) used for analysis are n = 15/12 at two months old, n = 11/14 at four months old, and n = 16/12 at six months old. All data are presented as mean ± SEM. ns = not significant; *p < 0.5; **p < 0.01; ***p < 0.001; ****p < 0.0001.

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    Figure 5.

    Kinematic measures of lever-pull trials at maximum hold duration. A, B, Lever position traces of 100 successful trials are shown for representative six-month-old WT and YAC128 mice who reached the maximum required lever hold duration. A tendency to overshoot the goal zone (dotted white lines) is seen in this YAC128 animal. C, D, Averaged lever position traces for the same two animals (error bars represent SD). E, Average maximum displacement of the lever for all trials at the 800-ms hold duration is shown for WT and YAC128 animals. The shaded region represents the point at which a trial is initiated when pulled backwards (12 ± 1° from starting position), and the dotted lines represent the range it must be held within to receive a reward. A significant age effect was found, but not a significant genotype or interaction effect. F, The average slope of the lever position trace from 200 to 800 ms after trial initiation was also calculated. An interaction between age and genotype was observed, and six-month-old YAC128 animals had a larger negative slope on average, indicating a progressive release of their hold on the lever. G, The average speed of the lever over all trials at maximum hold duration. Although a significant interaction effect was seen, post hoc testing found no genotype differences in any of the age groups. Numbers of animals (WT/YAC128) used for analysis are n = 13/11 at two months old, n = 10/13 at four months old, and n = 14/9 at six months old. All data are presented as mean ± SEM except where indicated. ns = not significant; *p < 0.5; **p < 0.01; ***p < 0.001; ****p < 0.0001.

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    Table 1.

    Animals excluded from analysis

    Animals initially available for testingDid not reach criteria in phase 1Did not reach maximum hold durationCage crash or malfunctionExcessive weight loss
    Two months old20 WT/21 YAC1280 WT/4 YAC1280 WT/1 YAC1287 WT/5 YAC1280 WT/0 YAC128
    Four months old19 WT/19 YAC1282 WT/2 YAC1282 WT/1 YAC1285 WT/3 YAC1280 WT/0 YAC128
    Six months old25 WT/19 YAC1281 WT/4 YAC1281 WT/0 YAC1289 WT/5 YAC1280 WT/1 YAC128
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    Table 2.

    Statistical table of all analyses

    Data structureType of testTest values and power
    Fig. 2AN/AFisher’s exact testp = 0.0386
    Fig. 2B, two monthsAll but one group normally distributed (D7 WT)Repeated measures two-way ANOVA with Bonferroni post hoc testsDays in cage: F(2,56) = 20.11, p < 0.0001; genotype: F(1,28) = 0.0007, p = 0.9798; interaction: F(2,56) = 0.0260, p = 0.9743
    Fig. 2B, four monthsAll groups normally distributedRepeated measures two-way ANOVA with Bonferroni post hoc testsDays in cage: F(2,56) = 6.050, p = 0.0042; genotype: F(1,28) = 0.08113, p = 0.7779; interaction: F(2,56) = 0.4340, p = 0.6501
    Fig. 2B, six monthsAll groups normally distributedRepeated measures two-way ANOVA with Bonferroni post hoc testsDays in cage: F(2,56) = 3.936, p = 0.0252; genotype: F(1,28) = 0.2267, p = 0.6376; interaction: F(2,56) = 0.3738, p = 0.6898
    Fig. 2C (log transform)All but one group (six-month YAC128) normally distributed, equal variancesTwo-way ANOVAAge: F(2,84) = 4.803, p = 0.0106; genotype: F(1,84) = 0.1089, p = 0.7422; interaction: F(2,84) = 0.5332, p = 0.5887
    Fig. 2D, two monthsNormal distribution, equal variancesStudent’s t testt(28) = 0.7433, p = 0.4635
    Fig. 2D, four monthsNon-normal distributionMann-Whitney testU = 94, p = 0.4659
    Fig. 2D, six monthsNon-normal distributionMann-Whitney testU = 107, p = 0.9665
    Fig. 2D, WTNon-normal distributionKruskal-Wallis Test with Dunn’s post hoc testsH = 15.22, p = 0.0005
    Fig. 2D, YAC128Non-normal distributionKruskal-Wallis Test with Dunn’s post hoc testsH = 13.50, p = 0.0012
    Fig. 3BGroups normally distributed, equal variancesTwo-way ANOVAAge: F(2,84) = 2.945, p = 0.0580; genotype: F(1,84) = 4.772, p = 0.0317; interaction: F(2,84) = 0.2492, p = 0.7800
    Fig. 3CGroups normally distributedRepeated measures two-way ANOVAHour of day: F(23,644) = 86.51, p < 0.0001; genotype: F(1,28) = -0.3218, p > 0.9999; interaction: F(23,644) = 0.7632, p = 0.7788
    Fig. 3DGroups normally distributedRepeated measures two-way ANOVA with Bonferroni post hoc testsHour of day: F(23,598) = 56.36, p < 0.0001; genotype: F(1,26) = 0.0, p > 0.9999; interaction: F(23,598) = 2.296, p = 0.0006
    Fig. 3EGroups normally distributedRepeated measures two-way ANOVA with Bonferroni post hoc testsHour of day: F(23,644) = 43.87, p < 0.0001; genotype: F(1,28) = 0.8750, p = 0.3576; interaction: F(23,644) = 1.911, p = 0.0066
    Fig. 4AGroups normally distributedRepeated measures two-way ANOVA with Bonferroni post hoc testsTrial number: F(20,500) = 70.42, p < 0.0001; genotype: F(1, 25) = 6.367, p = 0.0184; interaction: F(20,500) = 5.321, p < 0.0001
    Fig. 4BGroups normally distributedRepeated measures two-way ANOVATrial number: F(20,460) = 115.8, p < 0.0001; genotype: F(1,23) = 0.02924, p = 0.8657; interaction: F(20,460) = 0.6740, p = 0.8528
    Fig. 4CGroups normally distributedRepeated measures two-way ANOVATrial number: F(20,520) = 115.7, p < 0.0001; genotype: F(1,26) = 0.2737, p = 0.6053; interaction: F(20,520) = 1.336, p = 0.1497
    Fig. 4DN/AFisher’s exact testp = 0.7292
    Fig. 4EGroups normally distributed, equal variancesTwo-way ANOVAAge: F(2,74) = 2.753, p = 0.0703; genotype: F(1,74) = 2.002, p = 0.1613; interaction: F(2,74) = 1.504, p = 0.2290
    Fig. 5EGroups normally distributed, equal variancesTwo-way ANOVA with Bonferroni post hoc testsAge: F(2,64) = 3.193, p = 0.0477; genotype: F(1,64) = 2.798, p = 0.0993; interaction: F(2,64) = 2.522, p = 0.0883
    Fig. 5FAll but one group (two-month YAC128) normally distributed, equal variancesTwo-way ANOVA with Bonferroni post hoc testsAge: F(2,64) = 0.8329, p = 0.4395; genotype: F(1,64) = 3.837, p = 0.0545; interaction: F(2,64) = 6.309, p = 0.0032
    Fig. 5GGroups normally distributed, equal variancesTwo-way ANOVA with Bonferroni post hoc testsAge: F(2,64) = 1.188, p = 0.3113; genotype: F(1,64) = 2.193, p = 0.1435; interaction: F(2,64) = 3.381, p = 0.0402
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An Automated Home-Cage System to Assess Learning and Performance of a Skilled Motor Task in a Mouse Model of Huntington’s Disease
Cameron L. Woodard, Federico Bolaños, James D. Boyd, Gergely Silasi, Timothy H. Murphy, Lynn A. Raymond
eNeuro 7 September 2017, 4 (5) ENEURO.0141-17.2017; DOI: 10.1523/ENEURO.0141-17.2017

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An Automated Home-Cage System to Assess Learning and Performance of a Skilled Motor Task in a Mouse Model of Huntington’s Disease
Cameron L. Woodard, Federico Bolaños, James D. Boyd, Gergely Silasi, Timothy H. Murphy, Lynn A. Raymond
eNeuro 7 September 2017, 4 (5) ENEURO.0141-17.2017; DOI: 10.1523/ENEURO.0141-17.2017
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