Identification and characterization of two functionally distinct groups of spinal cord-projecting paraventricular nucleus neurons with sympathetic-related activity

Activation of spinal cord-projecting neurons of the hypothalamic paraventricular nucleus (PVN) has been implicated in a host of sympathetic nervous system functions. Here, we report two distinct activity patterns among electrophysiologically identified PVN spinal neurons that may contribute to the varied functional responses elicited by PVN activation. Extracellular single-unit recording was performed in anesthetized rats, and PVN neurons were antidromically identified by electrical stimulation of the spinal cord (T1-3 or T10-12). Axonal conduction velocity was determined for each identified neuron and revealed two distinct groups of cells, designated Group I (n=19) and Group II (n=34). Conduction velocity was significantly (P<0.01) different between Group I (3.67±0.29 m/s) and Group II (0.45±0.01 m/s) cells and indicates that axons of Group I cells are larger and/or more heavily myelinated than those of Group II, which appear to be unmyelinated. The majority of Group I (15/19: 79%) and Group II (23/34: 68%) cells discharged spontaneously. Basal firing rates were significantly different between groups (Group I: 2.7±0.85 versus Group II: 1.8±0.64 spikes s^-1; P<0.05). Spike-triggered averaging of renal sympathetic nerve activity revealed sympathetic-related discharge among a majority of Group I (11/15:73%) and Group II (17/23: 74%) neurons. In addition, seven of 11 Group I cells showed cardiac-related discharge. Pulse-rhythmic discharge was not detectable in any Group II cells tested (n=17). Among 11 Group I cells tested for barosensitivity, discharge in eight (73%) was graded by changes in mean arterial pressure. None of the 16 Group II cells tested for arterial pressure sensitivity responded. We conclude that the PVN spinal pathway is comprised of at least two functionally distinct cell types. The response profile and activity patterns of Group I cells suggest involvement in regulating vasomotor components of sympathetic outflow. By comparison, the activity of Groups II cells suggests a possible role in non-vasomotor sympathetic control.