Motor Behavior Selectively Inhibits Hair Cells Activated by Forward Motion in the Lateral Line of Zebrafish

Leon Lagnado,Paul Pichler

doi:10.1016/j.cub.2019.11.020

Abstract

SummaryHow do sensory systems disambiguate events in the external world from signals generated by the animal’s own motor actions? One strategy is to use an “efference copy” of the motor command to inhibit the sensory input caused by active behavior [1]. But does inhibition of self-generated inputs also block transmission of external stimuli? We investigated this question in the lateral line, a sensory system that allows fish and amphibians to detect water currents and that contributes to behaviors such as rheotaxis [2] and predator avoidance [3, 4]. This mechanical sense begins in hair cells grouped into neuromasts dotted along the animal’s body [5]. Each neuromast contains two populations of hair cells, activated by deflection in either the anterior or posterior direction [6], as well as efferent fibers that are active during motor behavior to suppress afferents projecting to the brain [7, 8, 9, 10, 11, 12]. To test how far the efference copy signal modulates responses to external stimuli, we imaged neural and synaptic activity in larval zebrafish during fictive swimming. We find that efferents transmit a precise copy of the motor signal and a single spike in the motor nerve can be associated with ∼50% inhibition of glutamate release. The efference copy signal acted with high selectivity on hair cells polarized to be activated by posterior deflections, as would occur during forward motion. During swimming, therefore, “push-pull” encoding of stimulus direction by afferents of opposite polarity is disrupted while still allowing a subset of hair cells to detect stimuli originating in the external world.

Highlights

Background fluorescence was subtracted manuallyBaseline fluorescence (F) was defined as the average fluorescence in the first 10 s of imaging and preceding the first stimulation interval; the ratio of change in fluorescence (DF) was calculated relative to that value (DF/F) and used for further analysis
Neuromasts Receive an Almost Exact Copy of the Motor Signal Cholinergic efferents entering neuromasts are thought to be coactivated with motor neurons to provide feedforward control of the sensitivity of the lateral line [11, 13], but the quantitative
The Efference Copy Suppresses Both Spontaneous and Stimulus-Evoked Transmission from Hair Cells To what extent does the efference copy signal modulate the output from a neuromast? To investigate this question, we monitored the synaptic output from hair cells by expressing the glutamate sensor iGluSnFR [18] under the control of the Sill promoter [15, 19] (Figures 1B, 1C, 2A, and 2B)

Summary

Introduction

Baseline fluorescence (F) was defined as the average fluorescence in the first 10 s of imaging and preceding the first stimulation interval; the ratio of change in fluorescence (DF) was calculated relative to that value (DF/F) and used for further analysis. Contrast in images was adjusted for presentation purposes. The motor nerve recordings were further digitally filtered (300 Hz high-pass 1kHz low-pass and 50 Hz notch). Spikes were extracted using a custom written procedure that applied a simple threshold to the filtered signal and detected when it was crossed by the signal. This temporal filter was a Gaussian with FWHM = 100 ms.

Methods

Results

Discussion

Conclusion