Sleep-dependent sensorimotor processing and network connectivity in the infant rat

Early sensory experiences play a critical role in the activity-dependent development of the sensorimotor system. The sources of sensory input to the neonatal nervous system involve external stimulation (exafference) and sensory feedback arising from self-generated movements (reafference). In the perinatal period, reafference from twitches of the limbs and facial muscles during active (REM) sleep is a powerful driver of neural activity across the entire neuraxis. Thus, sleep-related twitches are thought to contribute to the activity-dependent development of sensorimotor networks. In this dissertation, we first aimed to identify a motor pathway for the generation of twitching. Using newborn rats at postnatal day (P) 8, we provide evidence that the red nucleus (RN; source of the rubrospinal tract) is involved in the production of twitching. In addition, we show that reafference from twitches drives neural activity in the RN, therefore suggesting that the RN is an important site for sensorimotor integration. Also, in the RN of P8 rats, twitch-related reafference triggers theta (4–7 Hz) oscillations. By P12, theta oscillations are expressed continuously and exclusively across bouts of active sleep. Synchronized neuronal oscillations comprise a fundamental mechanism by which distant neural structures establish and express functional connectivity. Thus, we next hypothesized that sleep-dependent theta oscillatory activity enables the expression of network connectivity between the RN and associated neural networks, such as the hippocampus. Simultaneous recordings from the hippocampus and RN at P12 show that theta oscillations in both structures are synchronized, co-modulated, and mutually interactive exclusively during active sleep. Lastly, we test the hypothesis that twitches drive synchronized oscillatory activity across functionally related sensory structures at early ages when the occurrence of oscillations largely depends on sensory input. Focusing on the cortico-hippocampal network at P8, we demonstrate that, unlike periods of wake-related movements or behavioral quiescence, twitching promotes coupled oscillatory activity at Beta2 frequency (~20-30 Hz). Altogether, the findings in this dissertation suggest that one of the functions of active sleep in early infancy is to provide a context for sensorimotor processing and for synchronizing activity within and between forebrain and brainstem structures. Consequently, any condition or manipulation that restricts active sleep can deprive the infant animal of substantial sensory experience, potentially resulting in atypical developmental trajectories.