Neural circuitry for stimulus selection in the zebrafish visual system.

When navigating the environment, animals need to prioritize responses to the most relevant stimuli. Although a theoretical framework for selective visual attention exists, its circuit implementation has remained obscure. Here we investigated how larval zebrafish select between simultaneously presented visual stimuli. We found that a mix of winner-take-all (WTA) and averaging strategies best simulates behavioral responses. We identified two circuits whose activity patterns predict the relative saliencies of competing visual objects. Stimuli presented to only one eye are selected by WTA computation in the inner retina. Binocularly presented stimuli, on the other hand, are processed by reciprocal, bilateral connections between the nucleus isthmi (NI) and the tectum. This interhemispheric computation leads to WTA or averaging responses. Optogenetic stimulation and laser ablation of NI neurons disrupt stimulus selection and behavioral action selection. Thus, depending on the relative locations of competing stimuli, a combination of retinotectal and isthmotectal circuits enables selective visual attention.

Retinotectal circuitry of larval zebrafish is adapted to detection and pursuit of prey.

Retinal axon projections form a map of the visual environment in the tectum. A zebrafish larva typically detects a prey object in its peripheral visual field. As it turns and swims towards the prey, the stimulus enters the central, binocular area, and seemingly expands in size. By volumetric calcium imaging, we show that posterior tectal neurons, which serve to detect prey at a distance, tend to respond to small objects and intrinsically compute their direction of movement. Neurons in anterior tectum, where the prey image is represented shortly before the capture strike, are tuned to larger object sizes and are frequently not direction-selective, indicating that mainly interocular comparisons serve to compute an object's movement at close range. The tectal feature map originates from a linear combination of diverse, functionally specialized, lamina-specific, and topographically ordered retinal ganglion cell synaptic inputs. We conclude that local cell-type composition and connectivity across the tectum are adapted to the processing of location-dependent, behaviorally relevant object features.

The retina is the thin layer of tissue in the eye that can receive light stimuli and convert them into electric signals to be transmitted to the brain. The cells that sense fine detail cluster at the center of the retina while the motion-sensing cells that keep track of movement lie at the periphery. When zebrafish larvae hunt, their motion-sensing cells are triggered as a prey crosses their peripheral field of view. They then turn and swim towards it. As they approach, the prey image moves to the detail-sensing part of the retina and appears larger, filling more of the field of view at close range. The signals are then processed in defined parts of the brain, in particular in a region called the optic tectum. How this area is organized in response to the organization of the eye and the requirements of the hunt is still unclear. Förster et al. set out to explore how the hunting routine of zebrafish larvae shapes the arrangement of neurons in the optic tectum. The larvae were exposed to different images representing the various aspects of the prey capture process: small moving dots represented passing prey at a distance, while large moving dots stood for prey just before capture. Measuring activity in the neurons of the optic tectum revealed that, like the eye, different areas specialize in different tasks. The back of the tectum was frequently activated by small dots and worked out which direction they were moving in during the first hunting steps. The front of the tectum responded best to large dots, often ignoring their direction, and helped the larvae to track their prey straight ahead. To test these findings, Förster et al. destroyed the large object-responsive cells with a laser and watched the larvae hunting real prey. Without the cells, the fish found it much harder to track and catch their targets. These results shed light on the link between behavior and how neurons are arranged in the brain. Future work could explore how the different neurons in the optic tectum are connected, and the behaviors they trigger in the fish. This could help to reveal general principles about how sensory information guides behavior and how evolution has shaped the layout of the brain.

Deconstructing Hunting Behavior Reveals a Tightly Coupled Stimulus-Response Loop.

Animal behavior often forms sequences, built from simple stereotyped actions and shaped by environmental cues. A comprehensive characterization of the interplay between an animal's movements and its environment is necessary to understand the sensorimotor transformations performed by the brain. Here, we use unsupervised methods to study behavioral sequences in zebrafish larvae. We generate a map of swim bouts, revealing that fish modulate their tail movements along a continuum. During prey capture, larvae produce stereotyped sequences using a subset of bouts from a broader behavioral repertoire. These sequences exhibit low-order transition dynamics and immediately respond to changes in visual cues. Chaining of prey capture bouts is disrupted in visually impaired (lakritz and blumenkohl) mutants, and removing the prey stimulus during ongoing behavior in closed-loop virtual reality causes larvae to immediately abort the hunting sequence. These results suggest that the continuous integration of sensory information is necessary to structure the behavior. This stimulus-response loop serves to bring prey into the anterior dorsal visual field of the larvae. Fish then release a capture strike maneuver comprising a stereotyped jaw movement and tail movements fine-tuned to the distance of the prey. Fish with only one intact eye fail to correctly position the prey in the strike zone, but are able to produce the strike itself. Our analysis shows that short-term integration of binocular visual cues shapes the behavioral dynamics of hunting, thus uncovering the temporal organization of a goal-directed behavior in a vertebrate.