Long ascending propriospinal neurons are heterogenous and subject to spinal cord injury induced anatomic plasticity

Abstract

Long ascending propriospinal neurons (LAPNs) are a subset of spinal interneurons that provide direct connectivity between distant spinal segments. Here, we focus specifically on an anatomically defined population of “inter-enlargement” LAPNs with cell bodies at L2/3 and terminals at C5/6. Previous studies showed that silencing LAPNs in awake and freely moving animals disrupted interlimb coordination of the hindlimbs, forelimbs, and heterolateral limb pairs. Surprisingly, despite a proportion of LAPNs being anatomically intact post- spinal cord injury (SCI), silencing them improved locomotor function but only influenced coordination of the hindlimb pair. Given the functional significance of LAPNs pre- and post-SCI, we characterized their anatomy and SCI-induced anatomical plasticity. This detailed anatomical characterization revealed three morphologically distinct subsets of LAPNs that differ in soma size, neurite complexity and/or neurite orientation. Following a mild thoracic contusive SCI there was a marked shift in neurite orientation in two of the LAPN subsets to a more dorsoventral orientation, and collateral densities decreased in the cervical enlargement but increased just caudal to the injury epicenter. These post-SCI anatomical changes potentially reflect maladaptive plasticity and an effort to establish new functional inputs from sensory afferents that sprout post-SCI to achieve circuitry homeostasis.