INTRODUCTION: Spinal lamina I projection neurons (PNs) are key elements of the pain processing system, which relay peripheral input to supraspinal structures generating sensation of pain. The population of PNs is small (~5% of lamina I neurons) but very heterogeneous according to their intrinsic and synaptic properties. AIM(S): Investigate mechanisms of acute nociception encoding and evaluate input-output characteristics of lamina I PNs. METHOD(S): Whole-cell recordings from lamina I PNs retrogradely-labeled via the lateral PB area in an intact spinal cord preparation with attached dorsal roots. RESULTS: We identified a specific group of PNs (16%) with unique properties. In these PNs (SB-PNs), a stimulation of nociceptive afferents evoked gradual strength‑dependent amplification of afferent input expressed as an increase in the number of generated APs. Upon a root stimulation at C‑fiber‑intensity, the SB‑PN group generated more than 80% of spikes of the entire population of PNs, thus, being the major group of PNs codifying acute pain sensation. We have also identified several mechanisms of this nociceptive input amplification. First, SB‑PNs are intensively innervated by the high‑threshold A delta‑ and C‑afferents providing robust and reliable spike generation. Second, the nociceptive input was amplified by intrinsic bursting capabilities of SB PNs. Third, the afferent input was prolonged (to 0.-1.5 s) and potentiated (to -45 mV to -20 mV) by the NMDAR-dependent synaptic component forming intrinsic plateau potentials generated by SB‑PNs. The afferent stimulation increased, for several seconds, spontaneous excitatory drive to SB-PNs that became suprathreshold and evoked series of spikes. CONCLUSIONS: We have described a new type of lamina I PNs efficiently transmitting the main part of primary nociceptive input to supraspinal structures playing an important role in acute pain generation. A complex interplay between synaptic, intrinsic and network activities underlies unique nociceptive encoding features of this group of PNs. FINANCIAL SUPPORT: Supported by IBRO.
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