A Visual Pathway for Looming-Evoked Escape in Larval Zebrafish

Abstract

Avoiding the strike of an approaching predator requires rapid visual detection of a looming object, followed by a directed escape maneuver. While looming-sensitive neurons have been discovered in various animal species, the relative importance of stimulus features that are extracted by the visual system is still unclear. Furthermore, the neural mechanisms that compute object approach are largely unknown. We found that a virtual looming stimulus, i.e., a dark expanding disk on a bright background, reliably evoked rapid escape movements. Related stimuli, such as dimming, receding, or bright looming objects, were substantially less effective, and angular size was a critical determinant of escape initiation. Two-photon calcium imaging in retinal ganglion cell (RGC) axons revealed three retinorecipient areas that responded robustly to looming stimuli. One of these areas, the optic tectum, is innervated by a subset of RGC axons that respond selectively to looming stimuli. Laser-induced lesions of the tectal neuropil impaired the behavior. Our findings demonstrate a visually mediated escape behavior in zebrafish larvae exposed to objects approaching on a collision course. This response is sensitive to spatiotemporal parameters of the looming stimulus. Our data indicate that a subset of RGC axons within the tectum responds selectively to features of looming stimuli and that this input is necessary for visually evoked escape.

The effects of environmental enrichment objects on behaviors ofJapanese quails at different cage stocking densities

“…Avoiding the strike of an approaching predator requires rapid visual detection of a looming object, followed by a directed escape maneuver (Temizer et al, 2015). Approach-avoidance conflict results in behaviors that have been correlated with increases in physiological stress indicators (Holmes et al, 2003).…”

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

“…Although the larvae were the same approximate age when tested, we observed much faster dives, with −72±4.2 mm of vertical displacement over 60 s of dimming (∼72% of the tank's vertical range) versus about 10 mm (∼33% of the vertical range of the tank used in that study). This may reflect the loss of visual input from retinotectal pathways to premotor neurons, including the Mauthner neuron, which activate large-angle, high velocity turns at the onset of visual escapes (Temizer et al, 2015). In separate experiments where only lateral swimming was measured, these blind larvae did lack the large-angle turns, termed O-bends, normally seen upon dimming (Fernandes et al, 2012).…”

“…However, a localized looming shadow stimulus (a dark circle that rapidly expands in size) elicits strongly directional escape swims; looming shadows presented to one side activate contraversive turns, and shadows presented from the front or back activate escapes with higher or lower initial turn angles, respectively (Temizer et al, 2015). The looming shadow stimulus, which is a better approximation than whole-field brightness changes of natural visual input preceding an aerial predator strike, was also shown to activate specific retinotectal pathways, suggesting a hardwired circuit for directional responses to sudden localized dimming.…”

“…Our stimuli were not localized in the lateral plane but nevertheless elicited a downward directional response. We predict that a lateralized looming shadow presented in a cubical tank would combine these navigational reflexes and elicit an initial, Mauthner neuron-mediated lateral turn away from the stimulus (Temizer et al, 2015) followed by a spiral dive and then a period of decreased swimming. The persistent hyperactivity previously reported during dimming (Burgess and Granato, 2007) may reflect larvae attempting to perform such a 3D maneuver in a shallow tank.…”

“…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.…”