Impact of stride-coupled gaze shifts of walking blowflies on the neuronal representation of visual targets

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.

Saccadic movement strategy in a semiaquatic species – the harbour seal (Phoca vitulina)

“…In our study, head and body movements of the seals were analysed as a first approximation for gaze movements (see Eckmeier et al, 2008;Kress and Egelhaaf, 2012;Kress and Egelhaaf, 2014b) because eye movements could not be resolved in our video recordings. Seals have mobile eyes Hanke et al, 2008), so saccadic eye movements might add to the saccadic head and body shifts, as was reported for goldfish (Easter et al, 1974) and cichlid fish (Fernald, 1975(Fernald, , 1985.…”

Resource-efficient bio-inspired visual processing on the hexapod walking robot HECTOR

“…In comparison to other recently proposed hardware solutions for bio-inspired processing of visual information on autonomous robots [47], the direct implementation of the processing unit on the robot avoids computational bottlenecks such as the transmission-related reduction of the frame rate. By employing behavioral strategies such as active head stabilization-which is also found in insects-it might be possible to further reduce the influence of rotational optic flow components which potentially obfuscate the estimation of relative nearness from optic flow [15]. Hence, a prototype for mechanical gaze-stabilization will be implemented on the robot in order to increase the collision avoidance performance of the vision-based direction controller.…”

“…This allows the robot to perform visually-guided tasks such as collision avoidance or navigation. rather than a flying system is challenging as stride-coupled motion of the camera might obfuscate nearness estimation from optic flow [15]. The controller architecture implemented on the embedded hardware module [16] comprises a simple model for insect-inspired visual collision avoidance which has been proposed recently [17].…”

A Bio-Inspired Model for Visual Collision Avoidance on a Hexapod Walking Robot

“…For example, walking blowflies hardly ever show purely translational locomotion phases. Rather, they perform relatively large periodic rotations of their body around all axes due to walking [9]. While stride-induced body rotations around the roll and pitch axes are compensated by counter-rotations of the head, body rotations around the yaw axis are not [8].…”

“…In contrast to flight, walking imposes specific constraints on the processing of optic flow information. Due to the mechanical coupling of the agent to the ground the perceived image flow is superimposed by continuous rotational components about all axes correlated to the stride-cycle [9]. Therefore, nearness estimation from optic flow during translational walking might be obfuscated, potentially reducing the reliability of the collision avoidance algorithm.…”