Neural Circuits Underlying Visually Evoked Escapes in Larval Zebrafish

Abstract

SUMMARY Escape behaviors deliver organisms away from imminent catastrophe. Here, we characterize behavioral responses of freely swimming larval zebrafish to looming visual stimuli simulating predators. We report that the visual system alone can recruit lateralized, rapid escape motor programs, similar to those elicited by mechanosensory modalities. Two-photon calcium imaging of retino-recipient midbrain regions isolated the optic tectum as an important center processing looming stimuli, with ensemble activity encoding the critical image size determining escape latency. Furthermore, we describe activity in retinal ganglion cell terminals and superficial inhibitory interneurons in the tectum during looming and propose a model for how temporal dynamics in tectal periventricular neurons might arise from computations between these two fundamental constituents. Finally, laser ablations of hindbrain circuitry confirmed that visual and mechanosensory modalities share the same premotor output network. Together, we establish a circuit for the processing of aversive stimuli in the context of an innate visual behavior.

Object approach computation by a giant neuron and its relation with the speed of escape in the crab Neohelice

“…The optical parameters that have been most commonly associated with the response time are: (1) angular size, e.g. in locusts (Fotowat and Gabbiani, 2007), flies (Card and Dickinson, 2008) or fish (Dunn et al, 2016); (2) angular increment, e.g. in crayfish (Glantz, 1974); and (3) a combination of angular size and velocity, which allows an estimation of the time to collision, e.g.…”

“…Studies focused on the response of a single morphologically wellidentified type of neuron, such as the LGMD of the locust (e.g. , or on population responses of neurons, such as those recently described in the optic tectum of the zebrafish (Dunn et al, 2016). In both examples, the neural response encodes the dynamic of the stimulus expansion, and the activity reached at a fixed angular size was associated with the stimulus threshold of the corresponding avoidance behavior.…”

Three-dimensional motion tracking reveals a diving component to visual and auditory escape swims in zebrafish larvae

“…While detailed kinematic information can be obtained from 2D imaging, such as speed, latency, direction and frequency of swimming movements, a restriction in vertical range can be a confound in locomotor assays (Zhu and Weng, 2007) and leaves open the question of whether vertical swimming would occur as part of the 'natural' behavior. Recordings of neural activity have been used in conjunction with analyses of swimming movements to study escape circuits in zebrafish, including recent advances made by measuring the lateral direction of escape tail movements during optical calcium imaging of neurons in the brain (Dunn et al, 2016;Temizer et al, 2015). These and other neural recording methods have elucidated mechanisms of lateral movement control in zebrafish (Kohashi and Oda, 2008;Gabriel et al, 2009;Knogler and Drapeau, 2014), but the need to partially or fully immobilize the animal limits the potential to detect vertical movements.…”

Anatomical and functional analysis of non-retinal tectal afferents in larval zebrafish

“…The tectal neuropil contains these afferent axons, the dendrites of periventricular layer (PVL) neurons, and the axons of PVL interneurons. PVL neurons are morphologically diverse, including both tectal interneurons and projection neurons (Figure 1.7) Robles et al, 2011), and the tectal circuits arising from these cells are necessary for high-acuity vision, and for distinguishing between small prey items and larger visual features that may represent predators (Del Bene et al, 2010;Preuss et al, 2014;Semmelhack et al, 2014;Bianco and Engert, 2015;Temizer et al, 2015;Dunn et al, 2016). Anatomical and functional studies have suggested that visual information principally enters superficial laminae of the neuropil, and is progressively filtered before being relayed to other brain regions by the PVL projection neurons Del Bene et al, 2010;Robles et al, 2011;Gabriel et al, 2012).…”

“…At 6dpf, zebrafish are able to track and capture prey (Borla et al, 2002), can respond to predatory visual cues (Temizer et al, 2015;Dunn et al, 2016), perform phototaxis (Burgess et al, 2010) and can display optomotor and optokinetic responses (Roeser and Baier, 2003). Beyond visual behaviours, zebrafish have been shown to be capable of exhibiting complex social behaviours such as shoaling and aggression (Engeszer et al, 2004;Engeszer et al, 2007;Saverino and Gerlai, 2008;Dreosti et al, 2015), and are capable of responding appropriately to chemical stimuli (Speedie and Gerlai, 2008;Ogawa et al, 2014).…”