Postnatal Development of Spinal Nociceptive Pathways: Evidence for Involvement of Experience-Dependent Mechanisms

The adult organization and postnatal development of the nociceptive withdrawal reflexes (NWR) of single hindlimb muscles were examined in decerebrate spinal rats using electromyography. In adult rats, NWR were found to perform highly organized sensorimotor transformations, with single muscles receiving excitatory cutaneous input from specific receptive fields (RF) whose distribution of sensitivity reflected the muscles' withdrawal action. The neural circuits underlying NWR were shown to be immature at birth, resulting in functionally unadapted reflex responses and unorganized single muscle RF. A progressive refinement of these circuits then occurred, as evidenced by essentially adult-like reflex properties after the third postnatal week. Two lines of evidence were obtained that suggested that the maturation of NWR was dependent on information derived from the interaction between the developing nervous system and the environment. Firstly, near normal single muscle RF were found in adult rats in which a neonatal transection of the plantar nerves had caused the plantar hindpaw innervation to be provided by nerves other than those in normal rats. The central projections of the primary afferents that had taken over the innervation thus appeared to have become appropriately adapted. Secondly, neonatal alteration of a single muscle's movement pattern lead to a corresponding and appropriate change of that muscle's RF organization, suggesting that the cutaneous sensory feed-back ensuing on muscle contraction is instrumental in the postnatal tuning of NWR circuitry. The results suggest that the organization of spinal nociceptive systems is not genetically "hardwired", but partly under epigenetic influence, indicating involvement of experience-dependent mechanisms.