Research ArticleDEVELOPMENTAL NEUROSCIENCE

Early-life sleep disruption increases parvalbumin in primary somatosensory cortex and impairs social bonding in prairie voles

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Science Advances  30 Jan 2019:
Vol. 5, no. 1, eaav5188
DOI: 10.1126/sciadv.aav5188
  • Fig. 1 Experimental design.

    Summary of experiments conducted on (A) juvenile prairie voles only and (B) adult prairie voles that underwent ELSD or control conditions. RIA, radioimmunoassay; IHC, immunohistochemistry.

  • Fig. 2 Sleep measures during shaker or baseline conditions in juvenile prairie voles.

    (A and B) Sample hypnograms showing 30 min of either baseline (A) or ELSD (B) sleep patterns in prairie voles indicate brief arousals at regular intervals on the shaker. (C) Experimental design: EEG/EMG signals were collected from juvenile voles both on and off the shaker for 24 hours. (D) Total sleep time was moderately reduced. (E) REM sleep was reduced by approximately 25%. (F) Sleep was fragmented as evidenced by increased sleep-to-wake transitions (inset: NREM-to-wake and REM-to-wake transition). (G) Average sleep bout duration for both NREM and REM sleep was reduced on the shaker. W, wake; NR, NREM sleep; R, REM sleep. #P < 0.05 but not significant after Bonferroni correction, *P < 0.05, **P < 0.01, ***P < 0.001. Bar height is the mean; error bars ± SEM (n = 9).

  • Fig. 3 No change in nonsleep measures during ELSD.

    Prairie vole litters were either housed on the shaker (A) or left undisturbed for seven consecutive days from P14 to P21. P14 and P21 were partial shaker days (indicated by angled text). (B) Duration of parental care during ELSD protocol (checkerboard bars) was not different from controls (solid bars). (C) Weight at time of weaning was similar for both conditions (n = 13 to 22 per group) as were (D) circulating corticosterone levels (n = 5 to 9 per group). Symbols are individual animals. Fill colors indicate breeder pairs as an example of genetic heterogeneity and litter counterbalancing across groups within the prairie vole colony. Bar height is mean; error bars ± SEM.

  • Fig. 4 ELSD increased PV-ir in adult male S1 barrel cortex.

    (A) Experimental design: Brain tissue from control and ELSD adults was collected and processed for PV-ir in the barrel region of the S1 cortex. (B) ELSD animals showed increased PV-ir, (left: collapsed across sex; inset: data points for each sex). (C) Representative image of S1 cortex in an adult male control and ELSD prairie vole. Error bars ± SEM (n = 8 to 13 per group); *P < 0.05; **P < 0.01.

  • Fig. 5 NORT and light/dark box test in adults.

    (A) Experimental design: Control and ELSD prairie voles underwent NORT and light/dark box testing as adults. (B) ELSD animals did not show a preference to interact with the novel object during the test phase (one sample t test, test value = 0.5: *P < 0.05), dashed line indicates no preference, and (C) males spent less time interacting with objects (novel + familiar) overall during test (n = 7 to 13). (D) There were no significant differences in time spent in the dark portion of a light/dark box, one possible indicator of anxiety in rodents. Bar height is mean; error bars ± SEM (n = 12 to 29 per group). *P < 0.05, **P < 0.01.

  • Fig. 6 Partner preference test for pair bond formation.

    (A) Experimental design: ELSD and control prairie voles were tested for partner preference after 24 hours of cohabitation with an opposite sex animal. (B) ELSD reduced total huddling time (partner + stranger; inset: individual data points by sex). (C) ELSD males did not show a huddling partner preference. (D) Total aggression was lower in females, and (E) both ELSD and control males displayed selective aggression toward the stranger. Bar height is mean; error bars ± SEM (n = 13 to 20 per group). *P < 0.05, **P < 0.01.

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/1/eaav5188/DC1

    Supplementary Methods

    Fig. S1. Power spectral analysis of EEG signal during ELSD compared to baseline.

    Fig. S2. Mean percentage of nursing subtypes was not different between sleep-disrupted dams or controls.

    Fig. S3. PV-ir in the mPFC.

    Fig. S4. PV-ir in laminar bins within the S1 cortex.

    Fig. S5. Time with objects during NORT acquisition and locomotor activity in light/dark box was not different between groups.

    Fig. S6. Olfactory social recognition test.

    Table S1. Repeated measures MANOVA statistics on EEG power within relevant frequency bands on the shaker compared to baseline.

    Table S2. Target parental behaviors analyzed in this study.

    Table S3. Laminar distribution of PV-ir within S1 cortex of ELSD adult males compared to controls: T statistics and P values at each bin level.

  • Supplementary Materials

    This PDF file includes:

    • Supplementary Methods
    • Fig. S1. Power spectral analysis of EEG signal during ELSD compared to baseline.
    • Fig. S2. Mean percentage of nursing subtypes was not different between sleep-disrupted dams or controls.
    • Fig. S3. PV-ir in the mPFC.
    • Fig. S4. PV-ir in laminar bins within the S1 cortex.
    • Fig. S5. Time with objects during NORT acquisition and locomotor activity in light/dark box was not different between groups.
    • Fig. S6. Olfactory social recognition test.
    • Table S1. Repeated measures MANOVA statistics on EEG power within relevant frequency bands on the shaker compared to baseline.
    • Table S2. Target parental behaviors analyzed in this study.
    • Table S3. Laminar distribution of PV-ir within S1 cortex of ELSD adult males compared to controls: T statistics and P values at each bin level.

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