Many insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly's sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the 'sky compass' pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

Graphical Abstract Highlights d LC11 neurons are suppressed by motion and flicker in the local surround d LC11 expresses a GABA receptor required for normal object detection d T2/T3 respond to ON and OFF components of object motion and flicker d T3 neurons excite LC11 and are required for normal LC11 function SUMMARYThe direction-selective T4/T5 cells innervate opticflow processing projection neurons in the lobula plate of the fly that mediate the visual control of locomotion. In the lobula, visual projection neurons coordinate complex behavioral responses to visual features, however, the input circuitry and computations that bestow their feature-detecting properties are less clear. Here, we study a highly specialized small object motion detector, LC11, and demonstrate that its responses are suppressed by local background motion. We show that LC11 expresses GABA-A receptors that serve to sculpt responses to small objects but are not responsible for the rejection of background motion. Instead, LC11 is innervated by columnar T2 and T3 neurons that are themselves highly sensitive to small static or moving objects, insensitive to wide-field motion and, unlike T4/T5, respond to both ON and OFF luminance steps.

The use of vision to coordinate behavior requires an efficient control design that stabilizes the world on the retina or directs the gaze towards salient features in the surroundings. With a level gaze, visual processing tasks are simplified and behaviorally relevant features from the visual environment can be extracted. No matter how simple or sophisticated the eye design, mechanisms have evolved across phyla to stabilize gaze. In this review, we describe functional similarities in eyes and gaze stabilization reflexes, emphasizing their fundamental role in transforming sensory information into motor commands that support postural and locomotor control. We then focus on gaze stabilization design in flying insects and detail some of the underlying principles. Systems analysis reveals that gaze stabilization often involves several sensory modalities, including vision itself, and makes use of feedback as well as feedforward signals. Independent of phylogenetic distance, the physical interaction between an animal and its natural environment - its available senses and how it moves - appears to shape the adaptation of all aspects of gaze stabilization.

SUMMARYMany insects use patterns of polarized light in the sky to orient and navigate. Here we functionally characterize neural circuitry in the fruit fly, Drosophila melanogaster, that conveys polarized light signals from the eye to the central complex, a brain region essential for the fly’s sense of direction. Neurons tuned to the angle of polarization of ultraviolet light are found throughout the anterior visual pathway, connecting the optic lobes with the central complex via the anterior optic tubercle and bulb, in a homologous organization to the ‘sky compass’ pathways described in other insects. We detail how a consistent, map-like organization of neural tunings in the peripheral visual system is transformed into a reduced representation suited to flexible processing in the central brain. This study identifies computational motifs of the transformation, enabling mechanistic comparisons of multisensory integration and central processing for navigation in the brains of insects.

Many animals use the visual motion generated by traveling straight-the translatory optic flow-to successfully navigate obstacles: near objects appear larger and to move more quickly than distant objects. Flies are expert at navigating cluttered environments, and while their visual processing of rotatory optic flow is understood in exquisite detail, how they process translatory optic flow remains a mystery. We present novel cell types that have local motion receptive fields matched to translation self-motion, the vertical translation (VT) cells. One of these, the VT1 cell, encodes self-motion in the forward-sideslip direction and fires action potentials in spike bursts as well as single spikes. We show that the spike burst coding is size and speed-tuned and is selectively modulated by motion parallax-the relative motion experienced during translation. These properties are spatially organized, so that the cell is most excited by clutter rather than isolated objects. When the fly is presented with a simulation of flying past an elevated object, the spike burst activity is modulated by the height of the object, and the rate of single spikes is unaffected. When the moving object alone is experienced, the cell is weakly driven. Meanwhile, the VT2-3 cells have motion receptive fields matched to the lift axis. In conjunction with previously described horizontal cells, the VT cells have properties well suited to the visual navigation of clutter and to encode the fly's movements along near cardinal axes of thrust, lift, and forward sideslip.