(3) (25%) Early in mammalian development, slecp predominates over wakefulness, with both non-rapid eye movement (NREM) and rapid eye movement (REM) sleep at their lifetime maximums. This period of life corresponds to a time of rapid cortical changes and has led to the hypothesis that the endogenous neural activation characteristic of REM sleep in particular may be critical for normal maturation of the central nervous system (1-4).
Sleep deprivation studies in both young felines and juvenile rodents have identified core functions of sleep in the early development of the visual system (3, 5--7). motor systems (8-10), refinement of sensorimotor integration (11), and organization of spinal reflexes (12). Early-life sleep may also be necessary for the maturation of the neurobiological systems that underlie complex social behaviors (13): Previous works in both Drosophila (13, 14) and rats (15--17) suggest that early-lifc sleep disruption (ELSD) results in long-lasting changes in species-specific sociosexual behavior (e.g., courting and mating). However, the role of early-life sleep in the development of specific brain circuits that underlie complex social behaviors such as pair bond formation and expression remains largely unexplored.
In mice and rats, inhibitory GABAergic synapses within the barrel fields of the primary somatosensory (S1) cortex undergo marked remodeling in the second and third postnatal weeks (18, 19), with normal whisking behavior emerging between postnatal days (P) 12 and 15 (20). The somatosensory system is crucial for the expression n of rodent social behaviors (21). Both neonatal damage to the somatosensory cortex (22) and the deprivation of sensory stimuli to the whiskers alter the development of play behavior (23), which can influence the adult expression of social behavior (24. 25).
Proper synchronization of excitatory and inhibitory processes, essential to normal neural functioning throughout the neocortex (26), is dependent on fast-spiking parvalbumin (PV)-expressing inhibitory interneurons (27). These interneurons are involved in generating electroencephalographic (EEG) oscillations within the y frequency band (20 to 100 Hz) (28, 29) associated with cortical activation present during wake and REM sleep (30). Direct activation of PV interneurons in the barrel cortex of mice selectively amplifies EEG oscillations within the y frequency band (28). and aberrant EEG y band oscillations are a feature of many neuropsychiatric disorders (31).
PV intemeuron development is especially vulnerable to atypical experience during early development because of its activity-dependent postnatal maturation (32) and has been shown to be sensitive to REM sleep deprivation in kittens (5). In the rat and mouse, PV immuno oreactivity (PV-ir) in the cerebral cortex develops rapidly between P12 and P21 (33, 34) and may represent a time period in rodents whereby social neural networks are sensitive to environn mental insults such as ELSD. Notably, PV disruption in the cortex has been linked to abnormal social behavior in mice (35).
To investigate how sleep shapes the neural system's underlying social development, we disrupted sicep carly in life in the highly social prairie vole (Microtus ochrogaster). Prairie voles are socially monogamous rodents that form lifelong pair bonds with opposite sex individuals. In the wild, prairie voles engage in a number of affiliative social behaviors common to humans, including biparental care (36) and extended opposite sex cohabitation (assessed in the laboratory using the partner preference test) (37). We hypothesized that REM ELSD that occurs within a sensitive period of PV development in the cortex of rodents would have long-lasting effects on PV-ir and social bonding in the prairie vole.
In this series of studies, we first validated a method of ELSD in juvenile prairie voles using a laboratory orbital shaker while undergoing chronic in vivo sleep EEG/electromyographic (EMG) recordings. EEG/EMG signals were used to determine sleep measures during ELSD compared to baseline, as well as relative EEG power during sleep stages. Prairie vole pups underwent ELSD for I weck during their third postnatal week in development (P14 to P21), when social behaviors with littermates are starting to emerge (38) and when PV-ir is maturing in the neocortex. Brain tissue was collected from adult animals and processed for PV-ir in the S1 cortexas a first probe into the neocortical excitation/inhibition tuning necessary for appropriate social development. Behaviorally, adult prairic voles were tested for pair bond formation, novel object recognition, and anxiety-related bebavior to examine the role of early-life sleep on the development of complex behaviors known to involve the somatosensory system (i.e., sensory intcgration of environmental cues).
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