Properties of an adult spinal sensorimotor circuit shaped through early postnatal experience

During development, information about the three-dimensional shape and mechanical properties of the body is laid down in the synaptic connectivity of sensorimotor systems through adaptive mechanisms. This functional adaptation occurs through alteration of connection properties. Here, we characterize the differences between strong and weak connections in the nociceptive withdrawal reflex in adult decerebrate spinal rats, representing the preserved end product of the developmental adaptation process. Stronger excitatory reflex connections from the skin onto a muscle had relatively higher gain in their input-output relations, shorter onset latencies (up to approximately 150 ms) and lower trial-to-trial variability in relation to response amplitude (SD approximately mean(1/2)) than weaker pathways. Although inhibitory and excitatory nociceptive receptive fields of a muscle overlap to some degree, the results indicate that the inhibitory input is not a major determinant of the gain distribution within the excitatory receptive field and vice versa. The N-methyl-D-aspartate (NMDA) receptor antagonist, D-2-amino-5-phosphonovalerate (0.1-1 microg), applied topically on the spinal cord reduced the gain, whereas the response amplitude was mainly reduced by an absolute number by the alpha-amino-3-hydroxy-5-methyl-4-isoxazole-propionic acid receptor antagonist, 6-nitro-7-sulfamoylbenzo(f)quinoxaline-2,3-dione (1-10 microg). The results indicate that NMDA receptors have a critical role in gain regulation in the nociceptive withdrawal reflex system. It is suggested that after normal postnatal experience-dependent adaptation, the number of connections from a given skin site onto the reflex encoding interneurons is a major determinant of the difference in gain.