Primary Afferent Stimulation Differentially Potentiates Excitatory and Inhibitory Inputs to Spinal Lamina II Outer and Inner Neurons

Spinal lamina II (substantia gelatinosa) neurons play an important role in processing of nociceptive information from primary afferent nerves. Anatomical studies suggest that neurons in the outer (lamina II(o)) and inner (lamina II(i)) zone of lamina II receive distinct afferent inputs. The functional significance of this preferential afferent termination in lamina II remains unclear. In this study, we examined the differential synaptic inputs to neurons in lamina II(o) and II(i) in response to primary afferent stimulation. Whole cell voltage-clamp recordings were performed on neurons in lamina II(o) and II(i) of the rat spinal cord slice under visual guidance. Capsaicin (1 microM) significantly increased the frequency of glutamatergic miniature excitatory postsynaptic currents (mEPSCs) in all 27 lamina II(o) neurons and significantly increased the amplitude of mEPSCs in 12 of 27 lamina II(o) neurons. However, capsaicin only significantly increased the frequency of mEPSCs in 9 of 22 (40.9%) lamina II(i) neurons and increased the amplitude of mEPSCs in 6 of these 9 neurons. Furthermore, the peak amplitude of EPSCs, evoked by electrical stimulation of the attached dorsal root, in 40 lamina II(o) neurons was significantly greater than that [160.5 +/- 16.7 vs. 87.0 +/- 10.4 (SE) pA] in 37 lamina II(i) neurons. On the other hand, the peak amplitude of evoked inhibitory postsynaptic currents (IPSCs) in 40 lamina II(o) neurons was significantly smaller than that (103.1 +/- 11.6 vs. 258.4 +/- 24.4 pA) in 37 lamina II(i) neurons. In addition, the peak amplitudes of both EPSCs and IPSCs, evoked by direct stimulation of lamina II, were similar in lamina II(o) and II(i) neurons. This study provides new information that stimulation of primary afferents differentially potentiates synaptic inputs to neurons in lamina II(o) and II(i). The quantitative difference in excitatory and inhibitory synaptic inputs to lamina II(o) and II(i) neurons may be important for integration of sensory information from primary afferent nerves.