Abstract
During locomotion animals rely heavily on visual cues gained from the environment to guide their behavior. Examples are basic behaviors like collision avoidance or the approach to a goal. The saccadic gaze strategy of flying flies, which separates translational from rotational phases of locomotion, has been suggested to facilitate the extraction of environmental information, because only image flow evoked by translational self-motion contains relevant distance information about the surrounding world. In contrast to the translational phases of flight during which gaze direction is kept largely constant, walking flies experience continuous rotational image flow that is coupled to their stride-cycle. The consequences of these self-produced image shifts for the extraction of environmental information are still unclear. To assess the impact of stride-coupled image shifts on visual information processing, we performed electrophysiological recordings from the HSE cell, a motion sensitive wide-field neuron in the blowfly visual system. This cell has been concluded to play a key role in mediating optomotor behavior, self-motion estimation and spatial information processing. We used visual stimuli that were based on the visual input experienced by walking blowflies while approaching a black vertical bar. The response of HSE to these stimuli was dominated by periodic membrane potential fluctuations evoked by stride-coupled image shifts. Nevertheless, during the approach the cell’s response contained information about the bar and its background. The response components evoked by the bar were larger than the responses to its background, especially during the last phase of the approach. However, as revealed by targeted modifications of the visual input during walking, the extraction of distance information on the basis of HSE responses is much impaired by stride-coupled retinal image shifts. Possible mechanisms that may cope with these stride-coupled responses are discussed.
Highlights
Gathering information about the external world during selfmotion is a fundamental challenge for visually guided animals
As revealed by targeted modifications of the visual input during walking, the extraction of distance information on the basis of HSE responses is much impaired by stride-coupled retinal image shifts
By recording the activity of HSE cells, a specific Lobula plate tangential cells (LPTCs), during stimulation with image motion as perceived by freely walking flies in a goal-directed paradigm, we addressed three open questions: (i) How strong is the stride-induced response component in relation to the overall responses of HSE cells?; (ii) How do stride-induced gaze shifts interfere with the representation of external information in HSE cells?; and (iii) To what extent do HSE cell responses reliably reflect the retinal edge velocities? A pronounced edge velocity response component would be required if the consequences of rotational stride-coupled image flow are to be eliminated by subtracting the edge velocities of the object
Summary
Gathering information about the external world during selfmotion is a fundamental challenge for visually guided animals. For example, of a task where an object needs to be detected and fixated during locomotion, before it can be successfully approached In such a situation the retinal image displacements are affected by potential motion of the object, and by the way the animal moves itself and by its ability to stabilize its gaze. While approaching an object, walking flies experience relatively fast rotational image motion with velocities of up to ±170◦/s around the yaw axis and amplitudes of up to 4◦ (Kress and Egelhaaf, 2014). These rotations are modulated at the stride frequency of about 12 Hz even during otherwise straight walking phases. Similar kinematic results for walking flies have been obtained in a pionieering
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