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Research ArticleMethods/New Tools, Novel Tools and Methods

Sleep in Populations of Drosophila Melanogaster

Chang Liu, Paula R. Haynes, Nathan C. Donelson, Shani Aharon and Leslie C. Griffith
eNeuro 13 August 2015, 2 (4) ENEURO.0071-15.2015; https://doi.org/10.1523/ENEURO.0071-15.2015
Chang Liu
Department of Biology, National Center for Behavioral Genomics and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454-9110
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Paula R. Haynes
Department of Biology, National Center for Behavioral Genomics and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454-9110
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Nathan C. Donelson
Department of Biology, National Center for Behavioral Genomics and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454-9110
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Shani Aharon
Department of Biology, National Center for Behavioral Genomics and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454-9110
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Leslie C. Griffith
Department of Biology, National Center for Behavioral Genomics and Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts 02454-9110
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  • Figure 1.
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    Figure 1.

    Diagrams of DAM2 and LAM25H systems. A, DAM2 apparatus. Left, Side view of DAM2 sleep tube (5 × 65 mm) for individual fly recording showing location of infrared beams and food. Right, Cross-section of the tube with the orientation of the two infrared beams. B, LAM25H apparatus. Left, Side view of LAM25H vial (25 × 95 mm) for population recording showing location of infrared beams and food. Right, Cross-section of the vial with the orientation of the nine infrared beams. Dark blue bars and light blue bars indicate transmitters and receivers. Red arrow lines indicate how pairs of infrared beam sensors work, as well as the coverage of the cross-sectional area.

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    Figure 2.

    Populations of flies exhibit sleep patterns distinct from individual flies. A, Individual fly sleep for males and females. B, Sleep in populations of males and females. C, Quantification of total sleep from A and B. Individual males slept more than females. In populations males slept longer during the day, but less at night. D, Activity levels during wake periods. Males had more beam breaks than females in populations. E, Number of sleep episodes. Individual females had more sleep episodes than males, but populations were indistinguishable. F, Mean episode length. Females had shorter episodes than individual males, but no significant difference was detected in populations. G, Sleep Latency. Individual male flies took shorter time to fall asleep after light transitions than individual female flies, but no significant difference was found between populations of males and females. n = 32 for individuals and n = 8 groups for populations. Statistically similar groups are marked by the same letter, with different letters indicating significant differences between groups. F, female; M, male; ZT, Zeitgeber time.

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    Figure 3.

    Populations exhibit homeostatic rebound sleep after mechanical sleep deprivation. A, Sleep profiles of individual female flies (n = 48 and n = 43 for non-SD and SD, respectively) were recorded using DAM2. B, Sleep profiles of groups of 50 female flies (n = 16 groups for both non-SD and SD) were captured using LAM25H. Red bar indicates the sleep deprivation period in both experiments. In B, the absence of data points for the SD groups during the SD period is because of the need to remove the population vials from the monitor during shaking (see Materials and Methods). C, Quantification of recovery day sleep. Day time sleep increased significantly on the recovery day after 12 h of sleep deprivation by mechanical shaking. Sleep changes were normalized to the baseline day. Δ Total sleep: total sleep changes. ZT, Zeitgeber time; SD, sleep deprivation. ***p < 0.0001; n.s., no significant difference.

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    Figure 4.

    Suppression of sleep by starvation generates rebound sleep in populations. Sleep patterns generated by starvation in female (A) and male (B) flies in populations. C, Total daytime and nighttime sleep changes are plotted as mean ± SEM. Male flies’ sleep was reduced significantly during the day and night, but female flies’ sleep was significantly suppressed only in the night. Red bar indicates the starvation period. Twenty-four hour starvation-induced sleep loss was compensated after feeding on the recovery day. Δ Total sleep: total sleep changes. n = 8 for all conditions. ***p < 0.0001; n.s., no significant difference. ZT, Zeitgeber time; F, female; M, male.

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    Figure 5.

    amn1 Mutant flies housed in populations show a fragmented sleep pattern, similar to that of amn1 individuals. Sleep profiles of amn1 mutant flies compared with wild-type Canton S flies in individuals (A) and populations (B), respectively. C, Quantification of data. amn1 mutant flies slept less than wild-type flies in population as well as individuals. D, Activity during waking. Populations of mutant flies were hyperactive during the light period but hypoactive in the dark compared with controls; however, no difference was detected in individual flies. E, Number of sleep episodes. Sleep episodes increased significantly in populations of amn1 mutant flies compared with controls at night consistent with individuals, but exhibited the opposite phenotype during light period. F, Episode length. Populations of mutant flies did not show significant difference in sleep episode length where individual mutant flies decreased dramatically compared to wild-type. G, Latency. amn1 mutant flies exhibited similar latency compared to wild type flies at night in both individuals and populations. n = 8 groups for both wild-type and amn1 populations. n = 31 and n = 32, respectively, for wild-type and amn1 individuals. ZT, Zeitgeber time.

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    Figure 6.

    Populations of flies sleep better with complete food. Sleep profiles for populations of females (A) and males (B) on different food. C, Quantification of total sleep. Both female and male populations of flies slept significantly longer when on standard fly food compared with sucrose during the day, but there was no statistically significant difference during the night. D, Activity while awake. Complete food significantly increased activity levels during daytime wake periods in males, and at night in females. E, Number of sleep episodes. F, Sleep bout length. Females, but not males, had significantly consolidated sleep at night, i.e., fewer but longer sleep episodes. G, Latency. Females fell asleep faster on the complete food than on the sucrose agar food, whereas males exhibited similar latency on both food media. n = 8 groups for all conditions. ZT, Zeitgeber time; F, female; M, male.

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    Figure 7.

    Sleep is affected by population size and social behavior. A, Sleep profiles for female populations of different sizes. B, Sleep profiles for populations of males and females (1:1 ratio of sexes). C, Quantification of total sleep. Total sleep was decreased significantly with increasing number of flies and mixed populations with the same number of total flies exhibit lower sleep than populations of female flies. D, Activity while awake. Increasing the number of flies increases population activity. E, Number of sleep episodes. The number of episodes scales with population size in opposite directions for female only and mixed populations. F, Sleep latency does not change significantly with population size. n = 5–6 groups for all conditions. ZT, Zeitgeber time.

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    Figure 8.

    The ratio of male–female flies in mixed populations affect total sleep. Two experiments were done to test the effects of changes in sex ratio. A, Different ratios from 0 to 100% male were tested. Data are quantified in B. C, Small changes in ratios around the extremes were tested. Data are quantified in D. Mixed populations of flies had generally lower sleep than female or male same sex populations. Small changes in the number of males or females affected sleep most significantly at the extremes. To view sleep profiles clearly, error bars were omitted from A and C. n = 5–7 groups for all conditions. ZT, Zeitgeber time.

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    Figure 9.

    Olfactory input modulates sleep amount by influencing social interactions. Sleep profiles of individual female (A) or male (B) flies. C, Quantification of data. Orco2 mutants slept significantly less than w controls during the day, and male Orco2 mutants slept longer than w males at night. No significant difference was detected between individual female Orco2 mutants and w. n = 30–32 for all genotypes. Population sleep profiles for female (D), male (E), and 1:1 mixed-sex populations (F). G, Quantification of data. Total sleep in populations of Orco2 mutant flies was similar to w controls within the male and female groups during the day and night. However, mixed female and male populations of Orco2 mutants exhibited drastically elevated sleep compared with w controls during the night. n = 5–6 groups for all genotypes. ZT, Zeitgeber time; F, female; M, male.

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Tables

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    Table 1.

    Two-way ANOVA

    Source of variation
    Group (inhividual vs population)Gender (female vs male)Interaction
    DataDFn, DFdFpFpFp
    Fig. 2CTotal sleepLP1,76123.7<0.000186.91<0.00010.026340.8715
    DP1,7631.3<0.00014.8760.030247.18<0.0001
    DActivityLP1,764077<0.0001138.6<0.000196.81<0.0001
    DP1,76162.6<0.000137.59<0.000118.87<0.0001
    EEpisodesLP1,7654.01<0.00010.54250.46377.2930.0085
    DP1,76136.5<0.00016.3030.01420.00051160.982
    FEpisode LengthLP1,7624.88<0.00017.440.00795.6830.0196
    DP1,7614.440.00030.38280.53790.58380.4472
    GLatencyLP1,7634.82<0.000124.25<0.00010.0088890.9251
    DP1,7620.44<0.000124.45<0.00013.3260.0721
    Group (individual vs population)Genotype (CS vs amn)Interaction
    DFn, DFdFP valueFP valueFP value
    Fig. 5CTotal sleepLP1,75137.1<0.000140.04<0.00013.4230.0682
    DP1,7515.680.000223.11<0.00016.5230.0127
    DActivityLP1,751109<0.0001381.8<0.0001349<0.0001
    DP1,7547.74<0.000113.60.000415.010.0002
    EEpisodesLP1,7515.460.00022.3760.127441.79<0.0001
    DP1,75329.4<0.000138.07<0.00010.011360.9154
    FEpisode LengthLP1,7521.08<0.00017.8870.00637.2760.0086
    DP1,7513.870.00045.4690.0224.2020.0439
    GLatencyLP1,7524.08<0.000113.030.00062.6350.1088
    DP1,758.5880.00450.30530.58222/1330.1483
    Gender (female vs male)Food (complete vs sucrose agar)Interaction
    Fig. 6CTotal sleepLP1, 282.3330.1379127.2<0.000133.64<0.0001
    DP1, 2870.01<0.000153.7<0.00010.075860.785
    DActivityLP1, 28120.1<0.000152.35<0.000149.79<0.0001
    DP1, 283.4790.072711.210.00234.7780.0373
    EEpisodesLP1, 281.560.2222.6440.11510.76030.3907
    DP1, 2815.580.000560.54<0.000141.7<0.0001
    FEpisode LengthLP1, 285.1650.030923.54<0.00010.87250.3583
    DP1, 2850.2<0.000155.13<0.000142.32<0.0001
    GLatencyLP1, 281.5810.21942.69<0.0018.790.0061
    DP1, 2815.490.000534.96<0.000126.79<0.0001
    Gender (female vs mixed)Size (10 vs 50 vs 100)Interaction
    Fig. 7CTotal sleep24h1,26/2,26/2,26123.8<0.0001150.2<0.00018.4810.0015
    DActivity24h1,26/2,26/2,2682.69<0.000186.37<0.000115.01<0.0001
    EEpisodes24h1,26/2,26/2,26115.4<0.000111.750.0002116.8<0.0001
    FLatency24h1,26/2,26/2,263.2490.05503.8070.06192.8590.0754
    Gender (female vs male)Genotype (w vs Orco2)Interaction
    Fig. 9CTotal sleepLP1,21252.2<0.000156.03<0.00010.10740.7436
    DP1,2134.61<0.00010.47480.492111.130.0011
    gender (female vs male. vs Mixed)genotype (w vs Orco2)interaction
    GTotal sleepLP2,26/1,26/2,26281.4<0.00014.9920.03434.8840.0158
    DP2,26/1,26/2,26117.2<0.0001218.9<0.000180.17<0.0001
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    Table 2.

    Multi-comparisons after Two-way ANOVA

    Total SleepActivityEpisodeMean Episode LengthLatency
    LPDPLPDPLPDPLPDPLPDP
    Fig. 2ParametricParametricParametricParametricNonparametricNonparametricParametricNonparametricNonparametricNoparametric
    Female individual vs male individual<0.0001<0.00010.03390.04940.00280.2822<0.00010.15570.0002<0.0001
    Female individual vs female population<0.00010.3704<0.0001<0.00010.13930.0010.19410.01550.30770.0576
    Female individual vs male population0.2067<0.0001<0.0001<0.00010.02690.00730.21510.0016>0.9999<0.0001
    Male individual vs female population<0.00010.0379<0.0001<0.0001<0.0001<0.0001<0.0001<0.0001<0.0001>0.9999
    Male individual vs male population<0.0001<0.0001<0.0001<0.0001<0.0001<0.0001<0.0001<0.00010.00160.1597
    Female population vs male population<0.0001<0.0001<0.0001<0.0001>0.9999>0.99990.8482>0.9999>0.99990.1533
    Fig. 5ParametricNonparametricParametricParametricParametricParametricNonparametricNonparametricNonparametricNonparametric
    CS population vs amn1 population0.01430.0246<0.00010.00030.00010.0008>0.9999>0.99990.4977>0.9999
    CS population vs CS individual<0.00010.9612<0.0001<0.0001<0.0001<0.0001<0.0001<0.00010.05880.0105
    CS population vs amn1 individual0.0006>0.9999<0.0001<0.00010.0007<0.00010.09990.1171>0.99990.0791
    amn1 population vs CS individual<0.0001<0.0001<0.00010.07540.1481<0.0001<0.0001<0.0001<0.00010.3603
    amn1 population vs amn1 individual<0.00010.0107<0.00010.07540.1481<0.00010.04020.00430.0123>0.9999
    CS individual vs amn1 individual<0.00010.01580.34280.8361<0.0001<0.0001<0.00010.00010.046>0.9999
    Fig. 6ParametricNonparametricParametricParametricParametricParametricNonparametricNonparametricNonparametric
    Complete female vs complete male<0.00010.0363<0.00010.8222N/A<0.00010.3520.0394>0.9999>0.9999
    Complete female vs sugar-agar female<0.00010.07910.90010.0032N/A<0.00010.00160.0109<0.00010.0002
    Complete female vs sugar-agar male<0.0001<0.00010.02990.6616N/A<0.00010.1516<0.00010.00120.7302
    Complete male vs sugar-agar female<0.0001>0.9999<0.00010.0048N/A0.03360.0002>0.99990.01480.0056
    Complete male vs sugar-agar male0.00120.1409< 0.00010.6616N/A0.35740.03880.5590.0911> 0.9999
    Sugar-agar female vs sugar-agar male0.00530.06810.02990.031N/A0.16610.0909>0.9999>0.99990.0535
    Fig. 7Parametric (24 h)Parametric (24 h)Parametric (24 h)DP
    50 female vs 10 female<0.00010.0759<0.0001N/A
    50 female vs 100 female0.00350.01970.9473N/A
    50 female vs male+female 50<0.0001<0.0001<0.0001N/A
    50 female vs male+female 100.02470.34990.0056N/A
    50 female vs male+female 100<0.0001<0.0001<0.0001N/A
    10 female vs 100 female<0.0001<0.0001<0.0001N/A
    10 female vs male+female 50<0.0001<0.00010.9473N/A
    10 female vs male+female 100.00660.3499<0.0001N/A
    10 female vs male+female 100<0.0001<0.0001<0.0001N/A
    100 female vs male+female 500.00070.0157<0.0001N/A
    100 female vs male+female 10<0.00010.00070.0056N/A
    100 female vs male+female 1000.0001<0.0001<0.0001N/A
    male+female 50 vs male+female 10<0.0001<0.00010.0001N/A
    male+female 50 vs male+female 1000.01230.0005<0.0001N/A
    male+female 10 vs male+female 100<0.0001<0.0001<0.0001N/A
    Fig. 9CParametricNonparametric
    w female vs w male<0.00010.3464
    w female vs Orco female<0.0001>0.9999
    w female vs Orco male<0.0001<0.0001
    w male vs Orco female0.00010.0219
    w male vs Orco male<0.00010.0173
    Orco female vs Orco male<0.0001<0.0001
    Fig. 9GParametricParametric
    w female vs w male< 0.00010.3837
    w female vs w male+female0.8275<0.0001
    w female vs Orco female0.52870.0043
    w female vs Orco male<0.00010.0012
    w female vs Orco male+female0.17660.061
    w male vs w male+female<0.0001<0.0001
    w male vs Orco female<0.00010.1477
    w male vs Orco male0.05450.061
    w male vs Orco male+female<0.00010.5044
    w male+female vs Orco female0.5287<0.0001
    w male+female vs Orco male<0.0001<0.0001
    w male+female vs Orco male+female0.1105<0.0001
    Orco female vs Orco male<0.00010.6037
    Orco female vs Orco male+female0.01560.5044
    Orco male vs Orco male+female<0.00010.3319
    • View popup
    Table 3.

    t Test and nonparametric

    DataTestdft/Up
    Fig. 3CNon-SD individual vs SD individual LPUnpaired t test896.903<0.0001
    Non-SD population vs SD population LPMann–Whitney test303<0.0001
    Non-SD individual vs SD individual DPMann–Whitney test897910.0554
    Non-SD population vs SD population DPMann–Whitney test3041.50.0007
    Fig. 4CFemale nonstarved vs starved LP on starvation dayUnpaired t test140.77640.4504
    Male nonstarved vs starved LP on starvation dayUnpaired t test146.179<0.0001
    Female nonstarved vs starved DP on starvation dayUnpaired t test148.153<0.0001
    Male nonstarved vs starved DP on starvation dayUnpaired t test146.526<0.0001
    Female nonstarved vs starved LP on recovery dayUnpaired t test148.27<0.0001
    Male nonstarved vs starved LP on recovery dayUnpaired t test144.52<0.0001
    Female nonstarved vs starved DP on recovery dayUnpaired t test140.33690.7412
    Male nonstarved vs starved DP on recovery dayUnpaired t test140.00610.9952
    • View popup
    Table 4.

    One-way ANOVA and nonparametric test

    DataTestDFn, DFdFp
    Fig. 8B24 hOne-way ANOVA4, 2742.35<0.0001
    No. of groupsNo. of total values
    Fig. 8BLPKruskal–Wallis test5320.0002approximate p value
    DPKruskal–Wallis test5320.0001approximate p value
    Fig. 8D24 hKruskal–Wallis test664<0.0001approximate p value
    LPKruskal–Wallis test664<0.0001approximate p value
    DPKruskal–Wallis test664<0.0001approximate p value
    • View popup
    Table 5.

    Multiple-comparisons following one-way ANOVA and nonparametric test

    24 hLPDP
    Datan1n2Mean (rank) differencesAdjusted p valueMean rank differencesAdjusted p valueMean rank differencesAdjusted p value
    Holm–Sidak's testDunn's testDunn's test
    Fig. 8BFemale vs male 100%66−92.420.3864−6.833>0.99996>0.9999
    Female vs male 50%67388.2<0.000111.310.302117.790.0065
    Female vs male 77%67427.3<0.000112.60.157919.50.0019
    Female vs male 33%66435.2<0.000111.830.288719.830.0025
    Male 100% vs male 50%67480.6<0.000118.140.005111.790.2393
    Male 100% vs male 77%67519.7<0.000119.430.00213.50.0969
    Male100% vs male 33%66527.6<0.000118.670.005713.830.1064
    Male 50% vs male 77%7739.070.78161.286>0.99991.714>0.9999
    Male 50% vs male 33%7646.980.78160.5238>0.99992.048>0.9999
    Male 77% vs male 33%767.9050.8861−0.7619>0.99990.3333>0.9999
    Dunn's testDunn's testDunn's test
    Fig. 8DFemale vs 100% male88−240.1486−44.5<0.0001230.2018
    Female vs 4% male8125.667>0.9999-5.5>0.99998.167>0.9999
    Female vs 10% male812220.14411.167>0.999939.17<0.0001
    Female vs 90% male8123.333>0.9999−22.170.136133.50.0012
    Female vs 96% male812-9.667>0.9999-31.830.002723.830.0754
    100% male vs 4% male81229.670.007239<0.0001−14.83>0.9999
    100% male vs 10% male81246<0.000145.67<0.000116.170.8556
    100% male vs 90% male81227.330.019422.330.128510.5>0.9999
    100% male vs 96% male81214.33>0.999912.67>0.99990.8333>0.9999
    4% male vs 10% male121216.330.47386.667>0.9999310.0007
    4% male vs 90% male1212−2.333>0.9999−16.670.424125.330.0128
    4% male vs 96% male1212−15.330.6539−26.330.007915.670.5883
    10% male vs 90% male1212−18.670.2104−23.330.032-5.667>0.9999
    10% male vs 96% male1212−31.670.0005−330.0002−15.330.6539
    90% male vs 96% male1212−13>0.9999−9.667>0.9999−9.667>0.9999
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Sleep in Populations of Drosophila Melanogaster
Chang Liu, Paula R. Haynes, Nathan C. Donelson, Shani Aharon, Leslie C. Griffith
eNeuro 13 August 2015, 2 (4) ENEURO.0071-15.2015; DOI: 10.1523/ENEURO.0071-15.2015

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Sleep in Populations of Drosophila Melanogaster
Chang Liu, Paula R. Haynes, Nathan C. Donelson, Shani Aharon, Leslie C. Griffith
eNeuro 13 August 2015, 2 (4) ENEURO.0071-15.2015; DOI: 10.1523/ENEURO.0071-15.2015
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Novel Tools and Methods

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  • A Toolbox of Criteria for Distinguishing Cajal–Retzius Cells from Other Neuronal Types in the Postnatal Mouse Hippocampus
  • Assessment of Spontaneous Neuronal Activity In Vitro Using Multi-Well Multi-Electrode Arrays: Implications for Assay Development
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eNeuro eISSN: 2373-2822

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