Visuomotor Transformations Underlying Hunting Behavior in Zebrafish

Isaac H Bianco,Florian Engert

doi:10.1016/j.cub.2015.01.042

Abstract

SummaryVisuomotor circuits filter visual information and determine whether or not to engage downstream motor modules to produce behavioral outputs. However, the circuit mechanisms that mediate and link perception of salient stimuli to execution of an adaptive response are poorly understood. We combined a virtual hunting assay for tethered larval zebrafish with two-photon functional calcium imaging to simultaneously monitor neuronal activity in the optic tectum during naturalistic behavior. Hunting responses showed mixed selectivity for combinations of visual features, specifically stimulus size, speed, and contrast polarity. We identified a subset of tectal neurons with similar highly selective tuning, which show non-linear mixed selectivity for visual features and are likely to mediate the perceptual recognition of prey. By comparing neural dynamics in the optic tectum during response versus non-response trials, we discovered premotor population activity that specifically preceded initiation of hunting behavior and exhibited anatomical localization that correlated with motor variables. In summary, the optic tectum contains non-linear mixed selectivity neurons that are likely to mediate reliable detection of ethologically relevant sensory stimuli. Recruitment of small tectal assemblies appears to link perception to action by providing the premotor commands that release hunting responses. These findings allow us to propose a model circuit for the visuomotor transformations underlying a natural behavior.

Highlights

To generate visually guided behavior, the nervous system extracts task-relevant information from the retinal image to select and control an appropriate response
Functional Calcium Imaging during Tethered Hunting Behavior in Larval Zebrafish To monitor neural activity during the recognition of prey-like visual cues and the initiation of hunting routines, we combined a virtual hunting assay for tethered larval zebrafish [13] with in vivo 2P functional imaging in transgenic larvae expressing a genetically encoded fluorescent calcium indicator under the control of a pan-neuronal promoter, Tg(elavl3:GCaMP5G) a4598 [23] (Figure 1)
Larval zebrafish were tethered in agarose gel but able to freely move their eyes and tail, and visual cues were projected onto a diffusive screen in front of the animal (Figures 1A and 1D)

Summary

Introduction

To generate visually guided behavior, the nervous system extracts task-relevant information from the retinal image to select and control an appropriate response. Over 50 years ago, neuroethologists introduced the idea that specific behaviors can be triggered by ‘‘key stimuli,’’ delivered under appropriate conditions [1, 2]. In this context, individual neurons have been discovered in visual pathways that are proposed to function as ‘‘feature detectors.’’ Such neurons are selective for specific spatiotemporal patterns within the visual scene and include neurons tuned to visual features that define key stimuli. The small size and optical transparency of the nervous system allows functional imaging of neural activity at cellular resolution and throughout the brain, during behavior [5,6,7].

Results

Discussion

Conclusion