Inhibition of spinal nociceptive neurons by excitation of cell bodies or fibers of passage at various brainstem sites in the cat

Abstract

The relative contribution of cells of origin and fibers of passage to the inhibition of spinal nociceptive neurons from various brainstem sites is not known. The present study therefore quantitatively compares the descending inhibition produced by focal electrical stimulation which indiscriminatively excites all neuronal elements with the inhibition evoked by glutamate microinjections which selectively excite cell bodies at the same sites within the midbrain periaqueductal gray (PAG) and neighboring lateral reticular formation (LRF) and within the medullary nucleus raphe magnus (NRM). In pentobarbital anesthetized cats extracellular recordings were made from 22 lumbar dorsal horn neurons responding to innocuous mechanical skin stimuli and to noxious radiant heating of the glabrous skin at the ipsilateral hindpaw. Glutamate microinjections (1 μl, 0.5 M) into 6 of 10 sites within the NRM reduced heat-evoked responses in 6 different cats to 69.2 ± 3.8% of control. Electrical stimulation (180–600 μA) at the same sites and two additional sites in the NRM reduced responses to 50.0 ± 8.7% of control. At 4 of 10 sites within the PAG glutamate reduced spinal neuronal responses to heat in 4 different cats to 69.4 ± 6.1% of control. Electrical stimulation at 3 of the same sites and 6 additional sites within the PAG reduced heat-evoked responses to 52.7 ± 3.5% of control. Microinjections of glutamate into the LRF failed to affect heat-evoked responses in any of the 8 experiments tested, while electrical stimulation at 6 of the same sites in the LRF reduced neuronal responses to heat to 52.4 ± 7.1% of control. Thus, fibers of passage are responsible for the descending inhibition produced by electrical stimulation in the reticular formation neighbouring the PAG, while neurons originating in the PAG or in the NRM mediate some but not all of the descending inhibition evoked from these brainstem sites.