POPULATION CODING OF LOCOMOTION BY SENSORY AFFERENT NEURONS IN THE AWAKE MOUSE

Mammalian locomotion arises from the coordinated interaction between motor commands generated by spinal interneurons, and sensory feedback originating from the periphery. Peripheral sensory neurons continuously signal joint position, limb movement, and mechanical deformation of the skin, providing a rich representation of locomotion. However, how large populations of sensory neurons encode and contribute to distinct locomotor phases remains unclear. Here, we addressed this by performing in vivo two-photon calcium imaging of the fourth lumbar dorsal root ganglion in awake, locomoting, spine-fixed mice. To image diverse populations of sensory neurons, we used systemic viral delivery in postnatal day 5 pups to drive broad GCaMP7s expression. Adult mice underwent surgical implantation of a spinal post for fixation, and a glass coverslip over the dorsal root ganglion to provide chronic optical access to sensory neurons. Following habituation to spine-fixed locomotion on a running wheel, neural activity was measured during self-generated movement while hindlimb position was recorded using multiple behavioral imaging cameras. Population recordings across peripheral sensory neurons, whilst mice either walked or ran on a running wheel, revealed coordinated activity in response to self-generated behavioral events. Sensory neuron activity showed bidirectional response properties with both increased and decreased fluorescence across movement bouts. Presumed tactile events whereby the mouse was not locomoting but instead pressing the hindpaw into the surface of the running wheel, also led to salient neural responses across the population. Our results reveal that peripheral sensory afferent populations provide a mixed representation of movement and tactile information during self-generated locomotion.