Getting the news in milliseconds: the role of early novelty detection in active electrosensory exploration

Abstract

The pulse emitting weakly electric fish Gymnotus omarorum shows stereotyped “novelty responses” consisting of a transient acceleration of the rhythm of a self-emitted electric organ discharge that carries electrosensory signals. Here we show that rapid increases in electric image amplitude cause a “novelty detection potential” in the first electrosensory relay. This sign precedes and its amplitude predicts, the amplitude of the subsequent behavioral novelty response. Current source density analyses indicates its origin ar the layers of the electrosensory lobe where the main output neurons occur. Two types of units, referred to as “ON” and “OFF”. were recorded there in decerebrated fish. Firing probability of “OFF” units drastically decreased after a stepwise increase in electric image. By contrast, the very first novel stimuli after the increase evoked a sharp peak in firing rate of “ON” units followed by a very fast adaptation phase that contrasted with the slow adaptation observed in previous recordings of primary afferents. The amplitudes of this peak, the novelty detection potential, and the behavioral novelty responses, show the same dependence on the departure of the newest stimulus intensity from the weighted average of preceding ones suggesting that the signals encoded by “ON” neurons underlay the novelty detection potential, propagates through the hierarchical organization of the electromotor control, and finally contribute to accelerate the electric organ discharge rate. This suggests that detecting novelty at the very early processing stage of electrosensory signals is essential to adapt the electrosensory sampling rate to exploration requirements as they change dynamically.