Abstract
Sensing is often implicitly assumed to be the passive acquisition of information. However, part of the sensory information is generated actively when animals move. For instance, humans shift their gaze actively in a sequence of saccades towards interesting locations in a scene. Likewise, many insects shift their gaze by saccadic turns of body and head, keeping their gaze fixed between saccades. Here we employ a novel panoramic virtual reality stimulator and show that motion computation in a blowfly visual interneuron is tuned to make efficient use of the characteristic dynamics of retinal image flow. The neuron is able to extract information about the spatial layout of the environment by utilizing intervals of stable vision resulting from the saccadic viewing strategy. The extraction is possible because the retinal image flow evoked by translation, containing information about object distances, is confined to low frequencies. This flow component can be derived from the total optic flow between saccades because the residual intersaccadic head rotations are small and encoded at higher frequencies. Information about the spatial layout of the environment can thus be extracted by the neuron in a computationally parsimonious way. These results on neuronal function based on naturalistic, behaviourally generated optic flow are in stark contrast to conclusions based on conventional visual stimuli that the neuron primarily represents a detector for yaw rotations of the animal.
Highlights
In moving animals, retinal image flow differs from conventional visual stimuli used in the laboratory, by its characteristic dynamics that are largely determined by the animals’ own actions and reactions
For most of the time during this stimulus, the horizontal system equatorial cell (HSE) cell was depolarised relative to its resting potential
We may conclude that the overall depolarisation of HSE is not evoked by preferred-direction saccades, but by optic flow between saccades
Summary
Retinal image flow differs from conventional visual stimuli used in the laboratory, by its characteristic dynamics that are largely determined by the animals’ own actions and reactions. The eyes are rotated actively in a sequence of saccades towards interesting locations in the scene (review [1]) Many insects, such as blowflies, employ a similar saccadic viewing strategy (review [2]). They shift their gaze during free flight by saccadic turns of body and head, keeping gaze basically fixed between saccades [3,4,5]. This active viewing strategy generates retinal image flow with characteristic dynamical features and separates to a large extent the image flow resulting from rotational and translational movements of the animal. This hypothesis is tested here by analysing the performance of an identified motion-sensitive neuron in the blowfly under stimulus conditions that approximate natural situations
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