Functional organization of the nociceptive withdrawal reflexes

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Abstract
1. The organization of the nociceptive hind-limb withdrawal reflexes was investigated in 93 halothane/nitrous oxide anesthetized rats. Electromyographical techniques were used to record reflex activity in single motor units. 2. Most of the hindlimb muscles were activated by noxious mechanical stimulation of the skin of the ipsilateral hindlimb. These were the plantar flexors of the digits, the pronators of the paw, the dorsiflexors and the plantar flexors of the ankle, the flexors of the knee, the flexors of the hip and the adductors. By grading the stimulus intensity it was shown that all these muscles received input from cutaneous nociceptors. 3. Noxious stimulation of the skin failed to activate the obturator, knee extensors and m. tibialis posterior and, in most rats tested, m. semimembranosus and m. adductor magnus. The plantar flexors of the ankle, while exhibiting a clear nocireceptive field in all rats tested, had a high threshold and responded much more weakly than the dorsiflexors of the ankle. Thus, responses in muscles which oppose gravity in the standing position were either very weak or absent. 4. The present study shows that each of the activated hindlimb muscles has a highly organized noci-receptive field on the skin, which is related to the withdrawal movement caused by the muscle itself. Each of the muscles normally causes the withdrawal of its receptive field when the foot is on the ground. The skin area most effectively withdrawn, in this situation, corresponds to the most sensitive area of the nocireceptive field. However, with the exception of the plantar flexors of the digits and/or the ankle, each of the hindlimb muscles also withdraws the major parts of their receptive fields when the foot is off the ground. The locations of the noci-receptive fields were independent of the position of the hindlimb. These characteristics of the nociceptive withdrawal reflexes are the basis for their “local sign” (Sherrington 1906). 5. The threshold and the time course of reflex activation were different in different muscles. However, muscles with a similar action; the plantar flexors of the digits, the pronators of the paw, the dorsiflexors of the digits, the flexors of the knee and the adductors, respectively, had similar thresholds and time courses. Furthermore, the threshold and latency of activation of each muscle increased towards the border of its nocireceptive field, reflecting a decreasing sensitivity. These findings explain the progressive recruitment of muscles during increasing strength of noxious stimulation, termed “irradiation” (Sherrington 1906). 6. It is suggested that the nociceptive withdrawal reflexes are organized as separate reflex paths to individual muscles, each of which has a well organized cutaneous nocireceptive field.