Origins of Spinal Ascending Pathways that Reach Central Areas Involved in Visceroception and Visceronociception in the Rat

Abstract

The location of spinal cells projecting rostrally to central areas that process visceroception and visceronociception were studied in rat using the retrograde transport of a protein - gold complex. Origins of afferents to the nucleus tractus solitarius (the spinosolitary tract), the parabrachial area (the spinoparabrachial tract), the hypothalamus (the spinohypothalamic tract) and the amygdala (the spinoamygdalar tract) were studied at thoracic, lumbar and sacral levels, where spinal visceroceptive areas are concentrated. All of the afore-mentioned pathways have common origins in the lateral spinal nucleus and in the reticular formation of the neck of the dorsal horn at all the levels studied, and also in the dorsal grey commissure and adjacent areas at sacral levels. The spinosolitary and the spinoparabrachial tracts are dense pathways, both of which are also characterized by afferents from the superficial layers of the dorsal horn at all the levels studied and from cells lying in close proximity to some autonomic spinal areas. These autonomic areas are the central autonomic nucleus (dorsal commissural nucleus) of lamina X at thoracolumbar levels and the parasympathetic column at sacral levels; some projections from the intermediolateral cell column at thoracic levels were also noted. Projections from all these autonomic structures to the parabrachial area have not yet been recognized. Thus, the origin of the spinoparabrachial tract closely resembles that of the spinomesencephalic tract that reaches the periaquaductal grey and adjacent areas. The spinohypothalamic and the spinoamygdalar tracts are smaller pathways. Direct spinal connections to the amygdala have not been reported previously. Both the hypothalamus and amygdala receive projections from lamina VII cells at low thoracic and upper lumbar levels in a pattern that resembles that of the preganglionic cells of the intercalated nucleus. Hypothalamic projections from the sacral parasympathetic area were also noted. The use of c-fos as a functional marker to identify spinal neurons that are activated by noxious visceral stimulation suggests that both the spinoparabrachial and the spinosolitary tracts contribute significantly to the central transmission of visceronoceptive messages. Most of the visceronociceptive ascending projections in these pathways issued from lamina I cells. The results presented here confirm previous observations regarding the spinosolitary and the spinohypothalamic tracts and also demonstrate, for the first time, the complex origin of the spinoparabrachial tract and the existence of direct spinal afferents to the amygdala. These findings suggest that rostral transmission and central integration of visceral inputs require several parallel routes. The spinosolitary and spinoparabrachial tracts clearly play a role in conveying information regarding visceronociception.

Transneuronal Labeling of a Nociceptive Pathway, the Spino-(Trigemino-)Parabrachio-Amygdaloid, in the Rat

“…Therefore, although some lamina I input to the Ce may be relayed by other structures, such as the nucleus of the solitary tract (Menétrey and Basbaum, 1987), the elPB seems to relay most of these afferents. This is consistent with previous reports that spinal and trigeminal afferents (either directly to the amygdala or to relay nuclei other than the nucleus of the solitary tract) originate predominantly from deep layers of the dorsal horn in the rat (Menétrey and de Pommery, 1991).…”

“…To our knowledge, these islets of Ce-projecting cells have not been described previously. Finally, in the spinal cord, we recorded a few Fluoro-gold-labeled cells, mostly contralateral to the injection site, in deep laminae of the dorsal horn, near the central canal, and in the lateral spinal nucleus, confirming a previous report (Menétrey and de Pommery, 1991). Only rarely did we find Fluoro-gold-labeled neurons in lamina I.…”

Anterograde Transneuronal Viral Tracing of Central Viscerosensory Pathways in Rats

“…A separate spinal pathway appears to relay viscerosensory signals through lamina X, medial lamina VII, and the dorsal gray commissure, ascending at the junction of the gracile and cuneate fasciculi (Wang et al, 1999;Willis and Westlund, 2001). This pathway may merge with other ascending sensory pathways that access the forebrain by relaying in the caudal NST and medullary reticular formation (Menetrey and Basbaum, 1987;Potts et al, 2002), although direct spinal inputs to the parabrachial nuclei, hypothalamus, and amygdala also have been demonstrated (Menetrey and De Pommery, 1991). H129 tracing studies using longer survival times in bilaterally vagotomized rats will be necessary to reveal the central features of ascending spinal viscerosensory pathways and the extent to which they converge with ascending vagal sensory pathways.…”

Increased visceral sensitivity to capsaicin after DSS-induced colitis in mice: spinal cord c-Fos expression and behavior

“…Neuronal responses. The superficial lamina of the spinal cord dorsal horn (lamina I/II) and lamina X at the spinal segments T 12/13 to S 1 is known to receive nociceptive input from the colon (26). To test whether a painful stimulus in the colon induces neuronal activation in these areas, we determined the number of c-Fos-positive cells in the superficial lamina of the dorsal horn and in lamina X from spinal segment T 12/13 to S 1 at 2 h after intracolonic instillation of capsaicin or vehicle.…”