Unusual electrical interactions between neuronal elements of cat spinal cord were examined during the evolution (7-70 days) of proximal paranodally demyelinated axonal enlargements in alpha motor axons induced by beta, beta'-iminodipropionitrile (IDPN) treatment, 50 mg/kg ip, once weekly for up to 5 weeks. The electrical cross talk was observed as early as 7 days of the neuropathy, at which time it occurred in 17.0% of all motoneuron perikaryal recordings. The incidence was greater at 14 (39.1%) and 35 (26.1%) days, without preferential involvement of any motoneuron type. The frequency of recordings from axonal swellings increased from 7 to 35 days but without an increase in cross talk per recording. At 70 days of the neuropathy, L7 ventral root was stimulated repetitively to examine a possible influence of potassium on cross talk. Subsequently, action potentials could be elicited in motoneurons by stimulation of additional other ventral root filaments. These studies are in agreement with the lack of direct electrical apposition between excitable membranes in IDPN neuropathy but suggest support for a role for an accumulation of extracellular potassium, due to paranodal demyelination as the axon enlarges, in the pathogenesis of these aberrant electrical interactions.