Paradoxical inhibition of nociceptive neurons in the dorsal horn of the rat spinal cord during a nociceptive hindlimb reflex.

Nociceptive-specific and multireceptive neurons in the lumbar dorsal horn are excited by noxious stimuli applied to the hindpaw and inhibited by noxious stimuli applied to distant body regions. Given that at least a subset of these neurons are part of the circuit for nociceptive reflexes, inhibition of nociceptive-specific and multireceptive neurons should inhibit nociceptive reflexes. Unfortunately, previous attempts to test this hypothesis have been inconclusive because of methodological differences between electrophysiological and behavioral experiments. The present study overcame this problem by recording neural and reflex activity simultaneously. Rats were anesthetized with halothane and surgically prepared for single-unit recording from the lumbar dorsal horn. Hindpaw heat caused a burst of activity that reliably preceded hindpaw withdrawal in 10 nociceptive-specific and 17 multireceptive neurons. A distant noxious stimulus (tail in 50 degrees C water or ear pinch) inhibited the evoked activity of both nociceptive-specific and multireceptive neurons and simultaneously changed the topography of the hindpaw reflex from flexion to extension without altering reflex latency. The present data are consistent with previous reports of inhibition of nociceptive-specific and multireceptive neurons during application of a distant noxious stimulus. However, inhibition of nociceptive-specific and multireceptive neurons concomitant with a shift in the hindlimb reflex from flexion to extension suggests that these neurons are part of the circuit for flexor reflexes specifically. Presumably, lateral inhibition from the flexor to extensor circuit allows for the release of hindlimb extension when neurons in the flexion circuit are inhibited by a distant noxious stimulus. Such a system reduces the chance of injury by allowing for withdrawal reflexes to a single noxious stimulus and escape reactions, such as running and jumping, to multiple noxious stimuli.