Pelvic visceral input into the nucleus gracilis is largely mediated by the postsynaptic dorsal column pathway

Abstract

1. The purpose of this study was to investigate a proposed role for the postsynaptic dorsal column (PSDC) pathway in mediating visceral nociceptive input into the dorsal column (DC) nuclei. 2. In one group of animals, the hypogastric nerves were sectioned, thereby restricting colorectal input into the cord to pelvic afferent pathways known to coverage on lower lumbar and sacral segments. Extracellular recording were made from 41 nucleus gracilis (NG) cells that responded to colorectal distension (CRD). Results reported are from 15 NG cells that were tested before and after the administration of morphine into the sacral cord by microdialysis. 3. The responses of 11 NG cells to CRD were dramatically reduced by morphine infused into the sacral cord through a microdialysis fiber. This reduction was reversed by an intravenous injection of naloxone. Microdialysis administration of 6-cyano-7-nitro-quinoxaline-2,3-dione (CNQX) or a lesion of the DC also abolished the responses of the NG cells to CRD. 4. Four NG cells that responded to CRD showed an increase in their background activity approximately 25 min after an injection of mustard oil (MO). This increase in activity was counteracted by morphine or by a lesion of the DC. 5. In a second group of animals, recordings were made from 28 PSDC cells in the L0-S1 segments of the cord. These units were antidromically activated by stimulation of the upper cervical fasciculus gracilis. The projections of five PSDC neurons into the NG were traced with the use of antidromic mapping. Results are reported for the responses of 12 PSDC cells to CRD and to cutaneous stimuli before and after morphine administration into the sacral cord by microdialysis. 6. Morphine given spinally reduced the responses of 12 PSDC cells to CRD. This reduction was reversed by an intravenous injection of naloxone. CNQX administered spinally also abolished the responses to CRD of the PSDC cells tested. 7. Four other PSDC cells were studied before and after an injection of MO into the colon. Their background activity started to increase within 25 min after the injection. Morphine suppressed this increase in background activity and this effect of morphine was reversed by naloxone. 8. The responses of NG cells to cutaneous stimuli were not significantly affected by morphine in the dose used. On the other hand, morphine significantly reduced the responses of PSDC cells to noxious cutaneous stimuli although this effect was not as dramatic as that on responses to visceral stimuli. 9. From the results of the studies described in this and the companion paper, we conclude that there is an important pelvic visceral nociceptive pathway involving PSDC neurons that synapse in the NG. The NG in turn activates neurons in the ventral posterolateral (VPL) nucleus of the thalamus. We presume that activation of VPL neurons by noxious visceral stimulation contributes to visceral pain sensation and thus that pelvic visceral pain depends largely on activity in the DC-medial lemniscus system.

Nerve injury-induced tactile allodynia is present in the absence of FOS labeling in retrogradely labeled post-synaptic dorsal column neurons

“…The profile found in the present study is consistent with previous observations (Zhang et al 1999;Ossipov et al 2002;Todd, 2002;Gardell et al 2003). Earlier electrophysiologic studies indicated that transmission of visceral nociception to the n. gracilis is mediated through the PSDC neurons (Palecek et al, 2003;Al-Chaer et al 1996a). Furthermore, morphine abolished the responses of PSDC neurons to visceral or somatic nociceptive stimuli, but not to innocuous tactile stimuli, suggesting the possibility that modulation of the PSDC pathway by spinal morphine is mediated through opioid receptors at presynaptic sites or on interneurons (al-Chaer et al, 1996a;Willis et al 1999).…”

“…It is well established that noxious pelvic visceral stimuli may activate PSDC neurons (al-Chaer et al, 1996a(al-Chaer et al, ,1996bPalecek et al, 2002), and that noxious visceral stimuli evokes enhanced FOS expression in PSDC cells (Palecek et al, 2003). In the current investigation, ligation of the ureter caused marked increases in spinal FOS expression.…”

“…It is well established that the PSDC neurons mediate visceral pain (Al-Chaer et al 1996a,b;Hirshberg et al 1996;Houghton et al 1997;Nauta et al 1997;Houghton et al 2001). For example, the physiologic responses of PSDC neurons to colorectal distension are opioid-sensitive and behavioral responses to noxious visceral stimuli are blocked by lesions of the dorsal columns (Al-Chaer et al 1996a;Houghton et al 2001;Palecek et al 2002). The distribution of PSDC neuronal cell bodies coincides with the terminations of Aβ fibers, but not C-fibers, to include laminae III to lamina VI of the dorsal horn and the central canal, and they could receive tactile sensory inputs from the periphery Bennett et al 1984;Giesler et al 1984;Wang et al 1999;Todd, 2002).…”

Degenerative Myelopathy in 18 Pembroke Welsh Corgi Dogs

“…These sensory pathways have been identified in the dorsal funiculus of the lumbosacral and thoracolumbar spinal cord of dogs. 1,2,34 Other more noxious visceral sensations are transmitted in the spinothalamic tract. Lesions found in the dorsal funiculus of dogs in this study could be contributing to a lack of visceral sensory feedback to brain centers.…”

Restoration of spontaneous exploratory behaviors with an intrathecal NMDA receptor antagonist or a PKC inhibitor in rats with acute pancreatitis

“…Non-NMDA or NMDA receptor antagonists produce antinociceptive effects in other visceral pain models in animals (Al-Chaer et al, 1996;Coutinho et al, 1996;Ide et al, 1997;Kolhekar and Gebhart, 1994;Zhang et al, 2000).…”