SYNAPTIC-INTERACTIONS BETWEEN PRIMARY AFFERENT TERMINALS AND GABA ANDNITRIC OXIDE-SYNTHESIZING NEURONS IN SUPERFICIAL LAMINAE OF THE RAT SPINAL-CORD

The superficial laminae (I and II) of the spinal dorsal horn receive s mall caliber primary afferent fibers responsive to noxious stimulation , and contain local circuit neurons that modulate afferent input. Many of these neurons are GABAergic; about a third of these also synthesiz e nitric oxide. We identified three main morphological types of primar y afferent terminals in superficial laminae after injections of a trac er selective for small caliber afferents into the sciatic nerve of rat s. The relative densities of the three types varied through the dorsov entral extent of laminae I and II. Synaptic contacts of each type with GABA- and nitric oxide synthase (NOS)-containing dendrites and axon t erminals were determined by preembedding and postembedding immunocytoc hemistry. Nonglomerular primary afferent terminals, likely to originat e from peptidergic unmyelinated fibers, were not seen in synaptic cont act with either GABA- or NOS-containing neurons. Primary afferent term inals at the center of type 1 glomeruli (C1) and at the center of type 2 glomeruli (C2) are likely to originate from unmyelinated and small myelinated fibers, respectively. GABAergic terminals contacted more C2 than C1 terminals, suggesting more effective presynaptic inhibition o f C2 terminals. Many GABAergic terminals were also positive for NOS, b ut all GABAergic terminals presynaptic to primary afferent terminals w ere negative for NOS. Only C2 terminals established frequent synapses with NOS-positive dendrites. These results provide morphological evide nce for selective inhibitory gating of input to superficial dorsal hor n, and suggest that the link between noxious input and nitric oxide-sy nthesizing neurons, likely to be involved in nociception, may be provi ded both by direct synaptic contacts of small myelinated fibers onto d orsally extending NOS-positive dendrites, and by unmyelinated fibers v ia an oligosynaptic pathway.