Early-life sleep disruption impairs subtle social behaviors during pair bond formation in prairie voles: A computer vision study

Early life sleep disruption (ELSD) has been shown to have long lasting effects on social behavior in adult prairie voles (Microtus ochrogaster), including impaired expression of pair bond behavior during partner preference testing (e.g., reduced huddling with a pair bonded partner). However, due to the limitations of manual behavior tracking, the behavioral effects of ELSD across the entire time course of pair bond formation have not yet been described, hindering our ability to trace mechanisms. Here, we used computer vision to precisely track multiple behaviors during opposite-sex cohabitation of prairie voles. Male-female pairs were allowed to interact through a mesh divider in the home cage for 72 h, providing variables of body direction, distance-to-divider, and locomotion speed, with temporal resolution as high as the video frame rate (20-25 Hz). We found that control males displayed periodic, stereotyped patterns of body orientation towards females during pair bond formation. In contrast, ELSD males showed reduced duration and ultradian periodicity of these body orientation behaviors towards females. Furthermore, in both sexes, ELSD altered stereotypical spatial and temporal patterns of locomotion seen in control animals that typically varied across days of cohabitation and light/dark periods. This study highlights the utility of computer vision in deep characterization of subtle behaviors and allows a more comprehensive behavioral assessment of the profound and persistent effects of ELSD on later life social behavior. Our findings may shed light on causal mechanisms underlying human neurodevelopmental disorders featuring sleep disruption and social deficits, such as autism spectrum disorder.