Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields

Abstract

Elasmobranch fishes localize weak electric sources at field intensities of < 5 eta V cm-1, but the response dynamics of electrosensory primary afferent neurons to near threshold stimuli in situ are not well characterized. Electrosensory primary afferents in the round stingray, Urolophus halleri, have a relatively high discharge rate, a regular discharge pattern and entrain to 1-Hz sinusoidal peak electric field gradients of < or = 20 eta V cm-1. Peak neural discharge for units increases as a non-linear function of stimulus intensity, and unit sensitivity (gain) decreases as stimulus intensity increases. Average peak rate-intensity encoding is commonly lost when peak spike rate approximately doubles that of resting, and for many units occurs at intensities < 1 microV cm-1. Best neural sensitivity for nearly all units is at 1-2 Hz with a low-frequency slope of 8 dB/decade and a high-frequency slope of -23 dB/decade. The response characteristics of stingray electrosensory primary afferents indicate sensory adaptations for detection of extremely weak phasic fields near 1-2 Hz. We argue that these properties reflect evolutionary adaptations in elasmobranch fishes to enhance detection of prey, communication and social interactions, and possibly electric-mediated geomagnetic orientation.