Spontaneous activity in afferent and efferent fibers after chronic axotomy: response to potassium channel blockade

Distally propagating spontaneous impulses in acutely and chronically cut rat saphenous nerve were examined to determine (1) the origin(s) of the activity, (2) the fiber types involved, and (3) whether the activity was affected by potassium channel blockade. Under deep pentobarbital anesthesia, six male Sprague-Dawley rats underwent L3 cauda equina section, then unilateral saphenous axotomy. The nerve was then dissected into 30-50 microfilaments and surveyed for spontaneous activity using a modification of the microfilament recording method. Afterward, the nerve was cut back, and a potassium channel blocking agent (gallamine) was administered. The axonal activity was once again surveyed in the same fashion. Twenty-eight rats underwent unilateral saphenous axotomy 1-8 weeks prior to similar recordings, and the neuroma was excised just before microfilament dissection. Spontaneous discharges in these preparations originated from three foci: (1) antidromic activity from in-continuity dorsal root ganglia (DRG), (2) orthodromic activity from sympathetic neurons, and (3) antidromic activation of dichotomizing afferent axons in the peripheral nerve. There was significantly more antidromic activity from DRG in rats with prior axotomies than in control animals (t = 2.38; p less than 0.025), and gallamine produced a significant increase in DRG activity in the chronically lesioned nerve (t = 2.43; p less than 0.005), but not in acutely lesioned controls. However, most of the spontaneous activity in these preparations was from sympathetic efferents. This activity was decreased significantly by chronic axotomy (t = 2.635; p less than 0.01), and it was not affected by potassium channel blockade with gallamine. In two microfilaments, spontaneous antidromic action potentials were observed in conjunction with a clear receptive field on blood vessels in the nearby fascia. Both of these presumably dichotomized axons were found in acutely cut nerve, thus were not the result of retrograde sprouting from a neuroma. It was concluded that (1) chronic axotomy of sensory afferents produced ectopic activity in their respective DRG, (2) gallamine administration increased spontaneous activity from DRG in chronically axotomized rats, (3) ongoing sympathetic efferent activity in rat saphenous nerve was decreased by distal axotomy for up to 8 weeks, and (4) rare branched sensory afferents occasionally exhibit spontaneous activity.