Alteration in synaptic inputs through C-afferent fibers to substantia gelatinosa neurons of the rat spinal dorsal horn during postnatal development

Abstract

The change in synaptic inputs through primary afferent C- and A-fibers during postnatal development was examined in substantia gelatinosa neurons of a rat spinal cord slice with an attached L5 dorsal root by use of the blind whole-cell patch-clamp technique; the synaptic responses were compared between the slices obtained from immature (postnatal days 21-23) and mature (postnatal days 56-60) male rats. The mono- and/or polysynaptic afferent inputs were monitored by recording glutamatergic excitatory postsynaptic currents and potentials evoked by stimulating C- and A-fibers, the identification of which was based on the values of threshold stimulus intensity and of the conduction velocity of the fibers, determined by intracellular recordings from dorsal root ganglion neurons. Immature substantia gelatinosa neurons received synaptic inputs through Abeta-, Adelta- and C-afferents, with proportions of 51%, 46% and 36%, respectively. In mature substantia gelatinosa neurons, C- and Adelta-afferent inputs were increased in number (to 84% and 86%, respectively), while Abeta-inputs were decreased to 9%. In both immature and mature rats, repetitive stimulation of C-afferents did not elicit any slow responses, which are longer in duration than the monosynaptic excitatory postsynaptic currents, although C-fibers are known to contain not only excitatory amino acids, but also neuropeptides such as substance P, which is thought to be involved in the production of slow responses. These results indicate that both C- and Adelta-afferents innervating substantia gelatinosa neurons are reorganized following maturation, accompanied by a withdrawal or elimination of Abeta-fibers from the substantia gelatinosa, probably due to a competition among the fibers during development. In spite of the developmental increase in C-fiber inputs, mature as well as immature substantia gelatinosa neurons did not display any slow synaptic responses, which appear to be mediated by transmitters other than excitatory amino acids.