Bimodal modulation of background activity in an identified descending interneuron.

In the absence of any obvious input, sensory neurons and interneurons can display resting or spontaneous activity. This is often regarded as noise and removed through trial averaging, although it may reflect history-dependent modulation of tuning or fidelity and, thus, be of functional relevance to downstream interneurons. We investigated the history dependence of spontaneous activity in a pair of identified, bimodal descending interneurons of the stick insect, called contralateral ON-type velocity-sensitive interneurons (cONv). The bilateral pair of cONv conveys antennal mechanosensory information to the thoracic ganglia, where it arborizes in regions containing locomotor networks. Each cONv encodes the movement velocity of the contralateral antenna, but also substrate vibration as induced by discrete tapping events. Moreover, cONv display highly fluctuating spontaneous activity that can reach rates similar to those during antennal movement at moderate velocities. Hence, cONv offer a unique opportunity to study history-dependent effects on spontaneous activity and, thus, encoding fidelity in two modalities. In this work, we studied unimodal and cross-modal effects as well as unilateral and bilateral effects, using bilateral recordings of both cONv neurons, while moving one antenna and/or delivering taps to induce substrate vibration. Tapping could reduce spontaneous activity of both neurons, whereas antennal movement reduced spontaneous activity of the contralateral cONv neuron only. Combination of both modalities showed a cooperative effect for some parameter constellations, suggesting bimodal enhancement. Since both stimulus modalities could cause a reduction of spontaneous activity at stimulus intensities occurring during natural locomotion, we conclude that this should enhance neuronal response fidelity during locomotion.NEW & NOTEWORTHY The spontaneous activity in a pair of identified, descending insect interneurons is reduced depending on stimulus history. At rest, spontaneous activity levels are correlated in both interneurons, indicating a common drive from background activity. Whereas taps on the substrate affect both interneurons, antennal movement affects the contralateral interneuron only. Cross-modal interaction occurs, too. Since spontaneous activity is reduced at stimulus intensities encountered during natural locomotion, the mechanism could enhance neuronal response fidelity during locomotion.