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

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 re-cordings 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.

Automated summary

This study reveals that weakly electric fish Gymnotus omarorum exhibits novelty detection potential in response to rapid increases in electric image amplitude. This potential occurs in the first electrosensory relay and predicts subsequent behavioral novelty response. Current source density analyses indicate that it originates in specific layers of the electrosensory lobe where the main output neurons are located. Observation of ON and OFF units shows that firing probability of OFF units decreases drastically after the increase in electric image, while ON units exhibit a sharp increase in firing rate followed by rapid adaptation. These findings suggest that the signals encoded by ON neurons contribute to the novelty detection potential, propagate through hierarchical organization, and accelerate the electric organ discharge rate.