Regular afferent activity and structural homogeneity gate ephaptic synchronization in the dorsal column

Abstract

Ephaptic coupling can modify spike timing in closely packed myelinated axons, but its effect on physiologically relevant spike patterns remains unexplored. In this study, we used a biophysically detailed model of ephaptic coupling in parallel myelinated axons to analyze how experimentally motivated low-threshold mechanoreceptor spike patterns – regular, semiregular, and irregular – propagate along dorsal column axonal bundles. Spike trains were generated using a statistical procedure and were simulated under different population compositions, with and without ephaptic coupling, and under homogeneous and heterogeneous structural conditions. In our simulations, the homogeneous architecture of the dorsal column preserved the rhythmicity of regular firing inputs. Through ephaptic coupling, this rhythmicity drove synchronization across the entire population. Importantly, this synchronization remained partial and did not escalate into hypersynchrony. Without a regular component, ephaptic coupling alone produced only weak, unstructured activity. Axon diameter influenced propagation speed without altering qualitative dynamics. Also, results were independent of population size. By contrast, diameter heterogeneity abolished rhythmic organization and consequently disrupted synchronization. Semiregular firing – characterized by intermittent spike omissions that produce a bursting structure – consistently lost its rhythmic organization across all scenarios and converged toward irregular firing, which itself exhibited slightly reduced temporal variability during propagation. These results indicate that ephaptic coupling enhances the salience of temporal coding by allowing only fully preserved rhythmic firing to entrain and, thereby, partly synchronize surrounding spikes in the dorsal column. Semiregular and irregular inputs, by contrast, appear to contribute primarily to rate coding.