Abstract
Early stages of sensorimotor system development in mammals are characterized by the occurrence of spontaneous movements. Whether and how these movements support correlated activity in developing sensorimotor spinal cord circuits remains unknown. Here we show highly correlated activity in sensory and motor zones in the spinal cord of neonatal rats in vivo. Both during twitches and complex movements, movement-generating bursts in motor zones are followed by bursts in sensory zones. Deafferentation does not affect activity in motor zones and movements, but profoundly suppresses activity bursts in sensory laminae and results in sensorimotor uncoupling, implying a primary role of sensory feedback in sensorimotor synchronization. This is further supported by largely dissociated activity in sensory and motor zones observed in the isolated spinal cord in vitro. Thus, sensory feedback resulting from spontaneous movements is instrumental for coordination of activity in developing sensorimotor spinal cord circuits.
Highlights
Stages of sensorimotor system development in mammals are characterized by the occurrence of spontaneous movements
These behavioural observations and model predictions of spinal cord circuit function are supported by results obtained for higher sensorimotor stations, where sensory feedback from spontaneous twitches and reflexive responses was shown to trigger internally generated thalamocortical spindle-burst and early gamma oscillations (EGOs)[11,12,13,14,17,18,28]
Recordings of neuronal activity in cortex of neonatal rats revealed that different types of spontaneous movements evoke cardinally different cortical responses: while twitches and startles occurring during sleep were followed by excitation of neurons in primary motor cortex and hippocampus, complex, long-lasting movements occurring during awake states were not associated with cortical activation[30]
Summary
Stages of sensorimotor system development in mammals are characterized by the occurrence of spontaneous movements. Current knowledge on the function of the neonatal rodent spinal cord in relation to early movements is mainly based on behavioural and network modelling approaches[9,24,25,26] These studies suggest important roles of sensory feedback resulting from spontaneous movements in tuning sensorimotor connectivity. We find that the isolated spinal cord in vitro displays spontaneous bursting activities in sensory and motor zones, their spatiotemporal dynamics poorly matches that of the spinal cord in vivo, even after deafferentation These findings provide, for the first time, a description of sensorimotor spinal cord dynamics in relation to neonatal twitches and complex movements, indicate supraspinal mechanisms of inhibition of cortical activation during complex movements, and show that sensory feedback from twitches creates conditions for a reversed-type of Hebbian learning, with the activity in movement-generating networks preceding the afferent input, which supports the Schouenborg’s model of motordirected somatosensory imprinting
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