Neuroethology of Motion Vision

Project leader: Alex Mauss

Flow-field selectivity of wide-field neurons

Figure 1. Motion-opponent inhibition enhances flow field selectivity. Dendrites of wide-field tangential cells reside predominantly in single layer, for instance in layer 4 for VS cells. Excitatory input to tangential cells originates from cholinergic T4/T5 neurons (only shown in schematic), with axons segregated into four layers according to directional preference. Oppositely tuned inhibitory input is mediated indirectly from neighboring T4/T5 neurons via bi-stratified LPi cells. By spatial integration, excitatory and inhibitory responses to non-matching flow fields such as expansion cancel each other. Hence, selectivity to downward flow is increased. Figure adapted from Mauss et al. (2015).

Figure 1. Motion-opponent inhibition enhances flow field selectivity. Dendrites of wide-field tangential cells reside predominantly in single layer, for instance in layer 4 for VS cells. Excitatory input to tangential cells originates from cholinergic T4/T5 neurons (only shown in schematic), with axons segregated into four layers according to directional preference. Oppositely tuned inhibitory input is mediated indirectly from neighboring T4/T5 neurons via bi-stratified LPi cells. By spatial integration, excitatory and inhibitory responses to non-matching flow fields such as expansion cancel each other. Hence, selectivity to downward flow is increased. Figure adapted from Mauss et al. (2015).

Lobula plate output neurons (tangential cells) signal the presence of certain flow fields (Krapp & Hengstenberg, 1996). They receive two major kinds of inputs: excitatory local motion signals from cholinergic T4/T5 neurons (Schnell et al., 2012; Mauss et al., 2014) as well as feed-forward inhibition tuned to opposite directions via LPi neurons (Mauss et al., 2015). In combination with spatial integration, this simple connectivity motive ensures that tangential cells do not respond to any pattern containing preferred direction motion somewhere in the receptive field but rather selectively only to matching flow fields such as panoramic downward motion (Figure 1) (Mauss et al., 2015). Using electrophysiology and genetic circuit manipulation, we are investigating the connectivity and mechanisms that generate these and other response types.

Locomotor control by wide-field neurons in tethered flies

Figure 2. Bidirectional control of turning behavior by HS cells. HS cells send horizontal optic flow and are thought to mediate corrective turns to stabilize heading during locomotion. Their membrane potential on each side of the head can be controlled optogenetically using de- or hyperpolarizing light-sensitive channels. Both manipulations in tethered walking flies evoke turning responses syn-directional with the mimicked visual motion direction. Therefore, HS cells contribute bi-directionally to turning behavior that may underlie optic flow-based course stabilization under natural conditions. Figure adapted from Busch et al. (2018).

Figure 2. Bidirectional control of turning behavior by HS cells. HS cells send horizontal optic flow and are thought to mediate corrective turns to stabilize heading during locomotion. Their membrane potential on each side of the head can be controlled optogenetically using de- or hyperpolarizing light-sensitive channels. Both manipulations in tethered walking flies evoke turning responses syn-directional with the mimicked visual motion direction. Therefore, HS cells contribute bi-directionally to turning behavior that may underlie optic flow-based course stabilization under natural conditions. Figure adapted from Busch et al. (2018).

Optic flow-sensing neurons such as Horizontal System (HS) cells signal opposite directions of motion with graded de- and hyperpolarization (Hausen, 1984; Schnell et al., 2010). They are long thought to stabilize movement trajectories by sensing optic flow patterns arising from ego-motion and eliciting counteractive turning behavior. We are conducting experiments to study the effects of HS cell stimulation on tethered walking and flight. To gain control over the HS cells’ membrane potential, we express light-activatable optogenetic channels in those (Haikala et al., 2013; Mauss et al., 2017; Busch et al., 2018). For example, if depolarization is superimposed unilaterally on the HS cell potential, the animal will react with turning such that the simulated optic flow would be reduced. Interestingly, hyperpolarization also evokes turning: opposite to depolarization but again syndirectional with the simulated visual movement direction (Busch et al., 2018). Therefore, HS cells act as bidirectional optic flow sensors whose responses are likely useful to stabilize gaze and heading under natural conditions (Figure 2).

Roles of direction-selective neurons in freely moving flies

Studying visual behavior in tethered flies has many experimental advantages such as precise control over visual or optogenetic stimuli. However, tethered behavior is also unnatural. The animal is forced to behave in certain ways and sensory feedback from self-motion is either lacking or untypical. We therefore explore the natural role of motion vision and specific neuronal elements for behavior by combining genetic manipulations with automated tracking of freely walking and flying flies (Movie).

Tracking of walking flies

Walking velocity and direction relative to orientation is encoded in length and angle of black lines in the lower left corner of each inset.

References

Busch C, Borst A, Mauss A (2018) Bi-directional control of walking behavior by horizontal optic flow sensors. Curr Biol 28: 4037–4045.

Hausen K (1984) The lobula-complex of the fly: structure, function and significance in visual behaviour. Photoreception and Vision in Invertebrates (Chapter 15):523–559.

Krapp HG, Hengstenberg R (1996) Estimation of self-motion by optic flow processing in single visual interneurons. Nature 384(6608):463–466.

Mauss AS, Busch C, Borst A (2017) Optogenetic neuronal silencing in Drosophila during visual processing. Sci Reports 7: 13823.

Mauss AS, Meier M, Serbe E, Borst A (2014) Optogenetic and pharmacologic dissection of feedforward inhibition in Drosophila motion vision. J Neurosci 34: 2254-2263.

Mauss AS, Pankova K, Arenz A, Nern A, Rubin GM, Borst A (2015) Neural circuit to integrate opposing motions in the visual field. Cell 162: 351-362.

Haikala V, Joesch M, Borst A, Mauss AS (2013) Optogenetic control of fly optomotor responses. J Neurosci 33: 13927-13934.

Schnell B, Joesch M, Forstner F, Raghu SV, Otsuna H, Ito K, Borst A, Reiff DF (2010) Processing of horizontal optic flow in three visual interneurons of the Drosophila brain. J Neurophysiol 103: 1646-1657.

Schnell B, Raghu SV, Nern A, Borst A (2012) Columnar cells necessary for motion responses of wide-field visual interneurons in Drosophila. J Comp Physiol A 198: 389-395.