Abstract

Various presympathetic 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 supraspinal control of SPNs, causing dysautonomias including hypotension. In adult mice of either sex, we tested whether SCI-induced chronic loss of supraspinal control of tSPN activity leads to homeostatic increases in 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). The substantial variability obscured SCI-induced intrinsic plasticity. Dendritic length was reduced, as was measured cell capacitance in neuropeptide Y-expressing (NPY⁺) tSPNs (putative vasoconstrictors), which represent >40% of tSPNs. NPY⁺ tSPNs had changes in active membrane properties including an increased repetitive firing output gain (↑f–I slope), which modeling attributed to reduced delayed rectifier currents (I_K). After SCI, spontaneous quantal excitatory synaptic frequency increased overall (226%) including 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 vasoconstrictors, appear to undergo compensatory increases in excitability following high thoracic SCI. These alterations would further contribute to observed central and peripheral changes that limit hypotension but also exaggerate hyper-reflexic responses.