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bioRxiv · 10.1101/2025.09.06.674676

Plasticity in thoracic paravertebral sympathetic postganglionic neurons after high spinal cord transection

Li, Y.·Pusuluri, K.·Halder, M.·Sokoloff, A.·Prinz, A. A.·Hochman, S.
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Abstract

Various pre-sympathetic descending brain circuits recruit spinal cord preganglionic neurons to encode central sympathetic drive via their synaptic actions onto sympathetic postganglionic neurons (SPNs) - the final sympathetic output neurons. Thoracic paravertebral ganglia SPNs (tSPNs) provide distributed control over body tissue systems via functional subpopulations. High thoracic spinal cord injuries (SCIs) compromise descending excitatory drive to SPNs, causing dysautonomias including hypotension. In adult mice, we tested whether the SCI-induced chronic reduction in tSPN activity leads to homeostatic increases in their excitability. tSPN excitability spanned a >10 fold range in both sham and SCI populations, governed by a strong linear (ohmic) relationship between cell resistance and threshold depolarizing current (rheobase), with a clear trend towards increased excitability after SCI. Dendritic length was reduced, as was measured cell capacitance in Neuropeptide Y expressing (NPY+) tSPNs (putative vasoconstrictors), which represent >40% of tSPNs. NPY+ tSPNs also had changes in active membrane properties including an increased repetitive firing output gain ({uparrow}f-I slope), which modelling attributed to reduced delayed rectifier currents (IK). After SCI, spontaneous quantal excitatory synaptic frequency increased overall (226%) and in the NPY+ tSPN subpopulation (300%); their temporal summation recruited spiking in 10.5% of sham and 22.2% of SCI recordings. Computational modeling showed that spontaneous synaptic activity was particularly effective at recruiting spiking after SCI. Overall, tSPNs, including in vasoconstrictors, appear to undergo CNS-independent compensatory increases in excitability after SCI. The alterations further contribute to observed central and peripheral changes that limit hypoactivity and hypotension but exaggerate reflex responses. Significance StatementRecruited by preganglionic neurons located in thoracolumbar spinal cord, sympathetic postganglionic neurons (SPNs) represent the final step in sympathetic neural homeostatic control of target organs. The dramatic reductions or complete loss of brain pre-sympathetic drive in higher level spinal cord injuries (SCIs) contribute to emergent dysautonomias. Given the crucial role of SPNs in maintaining organismal homeostasis, we undertook comprehensive studies to test whether thoracic SPNs undergo homeostatic compensatory increases in their cellular excitability weeks after a high thoracic SCI. We observed changes consistent with increased cellular and synaptic excitability including in SPN vasoconstrictors, whose increased output gain, could mitigate hypotension but also strengthen hypertensive responses generated by afferent-driven exaggerated preganglionic drive (e.g. autonomic dysreflexia).

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Li, Y., Pusuluri, K., Halder, M., Sokoloff, A., Prinz, A. A., Hochman, S.. 2025-09-11. Plasticity in thoracic paravertebral sympathetic postganglionic neurons after high spinal cord transection. https://doi.org/10.1101/2025.09.06.674676

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