New insight into functional eye evolution: seeing the world through moving photoreceptors.

We wish to understand how insects perceive the 3-dimensional world they live in and use this knowledge to simulate what they see, mathematically. We have made the first critical step of this unique approach by generating a new theory that predicts how well a fruit fly sees 3-dimensional objects and demonstrated its accuracy in predicting neural responses and visual behaviours. This proposal aims for the next step: to test and expand this approach to other insects, in which eyes and brains have adapted to different lifestyles and environments, to decipher stereo vision from a completely new dynamic perspective.

To move efficiently, animals must continuously work out their x,y,z-positions in respect to real-world objects, and many animals have a pair of eyes to achieve this. How photoreceptors actively sample the eyes' optical image disparity is not understood because this fundamental information-limiting step has not been investigated in vivo over the eyes' whole sampling matrix.

This integrative multiscale study aims to advance our current understanding of stereopsis in insect compound eyes, from static image disparity comparison to a new morphodynamic active sampling theory. It is designed, using experiments and theory, to reveal and analyse how photomechanical photoreceptor microsaccades in the butterfly, honeybees, ant and housefly eyes have adapted through evolution to provide super-resolution 3D vision. This research aims to reveal how well each of these insect species see the three-dimensional world, and use this information to predict their visual capabilities and behaviours. Moreover, the results obtained with this research have real potential to provide new algorithms for robotic sensing and three-dimensional machine vision.

The objectives are to (O1-O2) measure, analyse and (O3) model dynamic light information sampling in different insect compound eyes by light-activated motion of photoreceptors (microsaccades) and (O4) test our predictions by behavioural experiments. We will ask how insect eyes of unique designs use photoreceptor microsaccades to dynamically sample the 3-dimensional world, and how acute are the resulting neural images and visual perception.

We will use the original multiscale experimental and theoretical methodologies developed in my laboratory to address the following hypotheses: (H1) Microsaccades are a general feature of compound eyes. (H2) Microsaccade dynamics and directions in different species are organised uniquely, matching vision to lifestyle to maximise information and stereopsis. (H3) Microsaccades show sex-specificity, reflecting the eye and behaviour differences.

We will study how microsaccades inside the eyes are organized to the world order to actively sample its stereoscopic structure. We do this both globally, across the eyes of living insects, using ultrafast X-ray imaging (synchrotrons) with extracellular electrophysiology, and locally with high-speed optical recordings and intracellular electrophysiology. By implementing the obtained results into theoretical multiscale models, we will simulate the adaptive eye optics with photoreceptor microsaccades sampling light information across the different insect eyes and how well these dynamics support each species' stereopsis. Finally, by performing behavioural experiments, we will test how well this new binocular active sampling theory - for each tested insect species - can estimate object depth and compare the predictions to a suite of visual behaviours.

The outcome will be new understanding of functional eye evolution - how the low-resolution compound eyes evolved to see the world in high-resolution 3D through moving photoreceptors - with new algorithms for machine vision and robotics.