Spinal lamina I projection neurons in the rat: Collateral innervation of parabrachial area and thalamus

Abstract

A major ascending nociceptive pathway from spinal lamina I to the mesencephalon has previously been reported in the cat, rat and monkey. In the present paper, we have used single and double retrograde labeling techniques to describe this projection system and its collateralization to the thalamus in the rat. Injections of wheat germ agglutinin-horseradish peroxidase into the pontomesencephalic parabrachial area labeled cell bodies bilaterally in lamina I and deeper laminae of the spinal cord. Bilateral lesions of the dorsolateral funiculi at thoracic levels reduced labeling of lamina I neurons caudal to the lesions. Combined injections of fluorescent retrograde tracers into the lateral thalamus and parabrachial area resulted in double labeling of projection neurons in lamina I, lamina IV–VIII and the lateral spinal nucleus of the cervical and lumbar enlargements. Double-labeled neurons were especially abundant in lamina I. Thus, we have demonstrated a major lamina I projection through the dorsolateral funiculi to the parabrachial area with significant colateralization to the thalamus. Moreover, since more than 80% of retrogradely labeled lamina I spinothalamic tract cells had collaterals to the parabrachial area we have indirectly demonstrated the presence of a dorsolateral funicular pathway for lamina I spinothalamic neurons in the rat. More lamina I neurons were retrogradely labeled from midbrain injections as compared to thalamic injections. The significance of these findings rest on previous work in this and other laboratories and concerns the understanding of spinal nociceptive mechanisms. Lamina I projection neurons are primarily nociceptive-specific in their response properties and have been shown to project to both the midbrain and thalamus via the dorsolateral funiculus in a number of species. The role of this projection system in nociceptive transmission may lie in its ability to distribute precise information to multiple brain stem sites which in turn activate autonomie or affective responses or descending pain modulatory mechanisms.