The impulse response of optic flow-sensitive descending neurons to roll m-sequences.

Richard Leibbrandt,Karin Nordström,Sarah Nicholas

doi:10.1242/jeb.242833

Richard Leibbrandt, Karin Nordström + Show 1 more

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https://doi.org/10.1242/jeb.242833

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Abstract

ABSTRACTWhen animals move through the world, their own movements generate widefield optic flow across their eyes. In insects, such widefield motion is encoded by optic lobe neurons. These lobula plate tangential cells (LPTCs) synapse with optic flow-sensitive descending neurons, which in turn project to areas that control neck, wing and leg movements. As the descending neurons play a role in sensorimotor transformation, it is important to understand their spatio-temporal response properties. Recent work shows that a relatively fast and efficient way to quantify such response properties is to use m-sequences or other white noise techniques. Therefore, here we used m-sequences to quantify the impulse responses of optic flow-sensitive descending neurons in male Eristalis tenax hoverflies. We focused on roll impulse responses as hoverflies perform exquisite head roll stabilizing reflexes, and the descending neurons respond particularly well to roll. We found that the roll impulse responses were fast, peaking after 16.5–18.0 ms. This is similar to the impulse response time to peak (18.3 ms) to widefield horizontal motion recorded in hoverfly LPTCs. We found that the roll impulse response amplitude scaled with the size of the stimulus impulse, and that its shape could be affected by the addition of constant velocity roll or lift. For example, the roll impulse response became faster and stronger with the addition of excitatory stimuli, and vice versa. We also found that the roll impulse response had a long return to baseline, which was significantly and substantially reduced by the addition of either roll or lift.

Highlights

When animals move through the world, their own movements generate widefield optic flow across their eyes
We simulated a cube with 4 m sides, with the hoverfly placed in its center (Fig. 1A, not to scale), containing 2 cm diameter spheres at a density of 100/m3
We found that the time to peak (TTP) and half-width of the roll impulse response (Fig. 3G,H,L,M) was similar to what has been reported for impulse responses to a range of different widefield stimuli in a range of different lobula plate tangential cells (LPTCs), including Eristalis horizontal system (HS) cells (Lee et al, 2015), Drosophila HS cells (Schnell et al, 2014) and blowfly H1 (Roy et al, 2015)

Summary

Introduction

When animals move through the world, their own movements generate widefield optic flow across their eyes. One of the most commonly applied models for motion detection was based on the steering response to widefield motion, R.L., 0000-0003-2442-0782; S.N., 0000-0002-5555-9421; K.N., 0000-00026020-6348 Later work, using receptive field mapping, physiological response properties and dye coupling, showed that VS cells synapse with the DNOVS2 neuron (Suver et al, 2016; Wertz et al, 2008, 2009b), which is called DNp22 (Namiki et al, 2018). Analysis of how the sensory information that passes through the descending neurons is transformed to motor control is a rapidly expanding field (Ache et al, 2019a; Cande et al, 2018; Chen et al, 2018), with population code control of behavior being likely (Ache et al, 2019b; Gonzalez-Bellido et al, 2013; Levi and Camhi, 2000)

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