DELAYED DEPOLARIZATION AND SLOW SODIUM CURRENTS IN CUTANEOUS AFFERENTS

1. Intraaxonal recordings were obtained in vitro from the sural nerve ( SN), the muscle branch of the anterior tibial nerve ( ATN), or the d eefferented ATN (dATN) in 5- to 7-wk-old rats. Whole-nerve sucrose gap recordings were obtained from the SN and the ATN. This allowed study of cutaneous (SN), mixed motor and muscle afferent (ATN), and isolated muscle afferent (dATN) axons. 2. Application of the potassium channel blocking agent 4-aminopyridine( 4-AP) to ATN or dATN resulted in a sl ight prolongation of the action potential. In contrast, a distinct del ayed depolarization followed the axonal action potential in cutaneous afferents (SN) exposed to 4-AP. The delayed depolarization could be in duced by a single whole-nerve stimulus or by injection of constant-cur rent depolarizing pulses into individual axons. The delayed depolariza tion often gave rise to bursts of action potentials and was followed b y a prominent afterhyperpolarization (AHP). 3. In paired-pulse experim ents on single SN axons, the recovery time (half-amplitude of the acti on potential) was 3.06 +/- 1.82 (SE) ms (n = 12). After exposure to 4- AP the recovery time of the delayed depolarization was considerably lo nger (half-recovery time: 99.0 +/- 28.3 ms; n = 15)than that of he act ion potential (18.8 +/- 9.1 ms; n = 16). 4. Application of tetraethyla mmonium (TEA) to cutaneous or muscle afferents alone had little effect on single action potential waveform. However, TEA reduced the amplitu de of the AHP elicited by a single stimulus in cutaneous afferent axon s after exposure to 4-AP and resulted in repetitive spike discharge. 5 . The delayed depolarization and spike burst activity induced by 4-AP in SN was present in Ca2+-free solutions containing 1 mM ethylene glyc ol-bis(beta-aminoethyl ether)-N,N,N'N'-tetraacetic acid and was not bl ocked by Cd2+ (1.0 mM).6. We obtained whole-cell patch-clamp recording s to study Na+ currents from either randomly selected dorsal root gang lion neurons or cutaneous afferent neurons identified by retrograde la beling with Fluoro-Gold. The majority of the randomly selected neurons had a singular kinetically fast Na+ current. In contrast, no identifi ed cutaneous afferent neurons had a singular fast Na+ current. Rather, they had a combination of kinetically separable fast and slow current s or a singular relatively slow Na+ current. 7. These results demonstr ate a difference in the sensitivity of myelinated cutaneous and muscle afferent axons to blockade of a 4-AP-sensitive K+ channel. Cutaneous afferent axons give rise to a prominent depolarizing potential after t he action potential, which is not present in the muscle afferent or mo tor axons. We propose that cutaneous afferent axons have kinetically s low Na+ channels not present in muscle afferent and efferent fibers, w hose activation underlies the delayed depolarization and multiple spik e discharge. The results indicate a difference in the Na+ channel orga nization of myelinated cutaneous versus muscle afferent axons and thei r cell bodies.