Pelvic Nerve Input Mediates Descending Modulation of Homovisceral Processing in the Thoracolumbar Spinal Cord of the Rat

Abstract

Colonic afferents project to the lumbosacral and thoracolumbar spinal cord via the pelvic and hypogastric/lumbar colonic nerves, respectively. Both spinal regions process inflammatory colonic stimuli. The role of thoracolumbar segments in processing acute colorectal pain is questionable, however, because the lumbosacral spinal cord appears sufficient to process reflex responses to acute pain. Here, we show that activity in pelvic nerve colonic afferents actively modulates thoracolumbar dorsal horn neuron processing of the same colonic stimulus through a supraspinal loop: homovisceral descending modulation. Dorsal horn neurons were recorded in the rat thoracolumbar spinal cord after acute or chronic pelvic neurectomy and cervical cold block. Acute pelvic neurectomy or lidocaine inhibition of lumbosacral dorsal roots facilitated the excitatory response of thoracolumbar dorsal horn neurons to colorectal distention (CRD) and decreased the percentage of neurons inhibited by CRD, suggesting colonic input over the pelvic nerve inhibits thoracolumbar processing of the same stimulus. Ectopic activity developed in the proximal pelvic nerve after chronic neurectomy reactivating the inhibitory circuit, inhibiting thoracolumbar neurons. Cervical cold block alleviated the inhibition in intact or chronic neurectomized rats. However, the facilitated response after acute pelvic neurectomy was inhibited by cervical cold block, exposing an underlying descending facilitation. Inhibiting pelvic nerve input after cervical cold block had minimal effect. These data demonstrate that input over the pelvic nerve modulates the response of thoracolumbar spinal neurons to CRD by a supraspinal loop and that increasing thoracolumbar processing increases visceral hyperalgesia.