Small sensory spinal lesions that affect hand function in monkeys greatly alter primary afferent and motor neuron connections in the cord. Issue 17 (16th August 2022)

• Record Type: Journal Article
• Authors: Fisher, Karen M.; Garner, Joseph P.; Darian‐Smith, Corinna
• Is Part Of: Journal of comparative neurology. Volume 530:Issue 17(2022)
• Page Start: 3039
• Page End: 3055
• Publication Date: 2022-08-16
• Subjects: dorsal column lesion -- dorsal root lesion -- motor neuron -- nonhuman primate -- somatosensory -- spinal cord injury; Comparative neurobiology -- Periodicals; Neurology -- Periodicals; 616
• DOI: 10.1002/cne.25395
• Languages: English
• ISSNs: 0021-9967

Abstract

Abstract: Small sensory spinal injuries induce plasticity across the neuraxis, but little is understood about their effect on segmental connections or motor neuron (MN) function. Here, we begin to address this at two levels. First, we compared afferent input distributions from the skin and muscles of the digits with corresponding MN pools to determine their spatial relationship, in both the normal state and 4–6 months after a unilateral dorsal root/dorsal column lesion (DRL/DCL), affecting digits 1–3. Second, we looked at specific changes to MN inputs and membrane properties that likely impact functional recovery. Monkeys received a targeted unilateral DRL/DCL, and 4–6 months later, cholera toxin subunit B (CT‐B) was injected bilaterally into either the distal pads of digits 1–3, or related intrinsic hand muscles, to label inputs to the cord, and corresponding MNs. In controls (unlesioned side), cutaneous and proprioceptive afferents from digits 1–3 showed different distribution patterns but similar rostrocaudal spread within the dorsal horn from C1 to T2. In contrast, MNs were distributed across just two segments (C7–8). Following the lesion, sensory inputs were significantly diminished across all 10 segments, though this did not alter MN distributions. Afferent and monoamine inputs, as well as KCC2 cotransporters, were also significantly altered on the cell membrane of CT‐B labeled MNs postlesion. In contrast, inhibitory neurotransmission and perineuronal net integrity were not altered at this prechronic timepoint. Our findings indicate that even a small sensory injury can significantly impact sensory and motor spinal neurons and provide new insight into the complex process of recovery. Abstract : The segmental organization of primate spinal cord differs depending on modality, and these modalities are differentially affected by spinal cord injury. Sensory inputs from the hand have a widespread input range which span 10 segments of cervical and thoracic cord. These inputs are drastically reduced by a dorsal root/dorsal column lesion (DRL/DCL) affecting digits 1‐3 of one hand. In contrast, digit related motor neurons (MNs) have a tight distribution across only 2 spinal segments, and their numbers are unaffected by a DRL/DCL. However, individual synaptic inputs to motor neurons are altered which means that even focal sensory injuries to the spinal cord can have a profound effect on motor output.