CHARACTERIZATION OF DESCENDING FACILITATION AND INHIBITION OF SPINAL NOCICEPTIVE TRANSMISSION FROM THE NUCLEI RETICULARIS-GIGANTOCELLULARIS AND GIGANTOCELLULARIS PARS ALPHA IN THE RAT

1. Descending influences produced by focal electrical stimulation in the nuclei reticularis gigantocellularis (NGC) and gigantocellularis pars alpha (NGC-alpha) on spinal nociceptive transmission and the dorsoventral region of spinal white matter mediating stimulation-produced modulation were examined in pentobarbital sodium-anesthetized, paralyzed rats. Spinal units studied responded to mechanical stimuli and noxious heating (50-degrees-C) of cutaneous receptive fields confined to the glabrous skin of the ipsilateral hind foot. Recording sites were located in laminae I-VI of the L3-L5 spinal segments. 2. Electrical stimulation in the NGC or NGC-alpha produced both facilitation and inhibition of responses of spinal units to noxious heating of the skin. At 33 of 57 stimulation sites in the NGC and NGC-alpha, electrical stimulation produced biphasic effects, facilitating responses at lesser intensities (5-25-mu-A) and inhibiting responses at greater intensities (50-100-mu-A). At 21 other sites in the NGC and NGC-alpha, electrical stimulation (5-100-mu-A) only inhibited, and at 3 sites stimulation (5-100-mu-A) only facilitated responses of spinal units to noxious heating of the skin. 3. Electrical stimulation in the NGC or NGC-alpha contralateral to the spinal recording site produced the same magnitude of facilitation/inhibition or inhibition of spinal nociceptive transmission as did stimulation in the ipsilateral NGC and NGC-alpha. 4. The latencies to descending facilitation and inhibition of spinal nociceptive transmission from the NGC and NGC-alpha were estimated by a cumulative sum technique to be 232 and 80 ms, respectively. 5. Responses of spinal units to graded heating (42-50-degrees-C) of the skin exhibited positively accelerating stimulus-response functions (SRF) throughout the temperature range tested. Electrical stimulation at lesser, "facilitating" intensities produced a parallel, leftward shift of the SRF, whereas stimulation at greater, "inhibitory" intensities significantly decreased the slope of the SRF without affecting the threshold for response. 6. To determine whether activation of cell bodies in the NGC or NGC-alpha were capable of replicating the effects of electrical stimulation, L-glutamate was microinjected into sites where electrical stimulation facilitated at lesser and inhibited at greater intensities the responses of spinal units to 50-degrees-C heating of the skin. L-Glutamate (5 nmol) produced a rapid onset, short-lasting and reproducible facilitation of nociceptive transmission; glutamate microinjection into the same site at a greater dosage (50 nmol) inhibited responses of the same spinal units. 7. Unilateral transection of the dorsolateral funiculus (DLF; contralateral or ipsilateral) significantly decreased the descending inhibition of nociceptive transmission produced by electrical stimulation in the NGC or NGC-alpha. Bilateral transection of the DLFs abolished the inhibitory effect of stimulation, and those greater intensities of stimulation that previously inhibited nociceptive responses of spinal units before bilateral transection of the DLFs now facilitated those responses. The descending facilitation produced by stimulation at low intensities in the NGC or NGC-alpha was not affected by either unilateral (ipsilateral or contralateral) or bilateral DLF transections. 8. These experiments quantitatively evaluated descending facilitation of spinal nociceptive transmission, and the results complement previous behavioral and pharmacological studies. The present results reveal that spinal nociceptive (thermal) transmission is subject to biphasic descending modulation from cell bodies in the NGC and NGC-alpha, that these descending influences are bilateral in the spinal cord and pathways that exert inhibitory influences on spinal dorsal horn units are contained in the DLFs.