Canal neuromasts enhance foraging in zebrafish (Danio rerio)

Abstract

Aquatic animals commonly sense flow using superficial neuromasts (SNs), which are receptors that extend from the body's surface. The lateral line of fishes is unique among these systems because it additionally possesses receptors, the canal neuromasts (CNs), that are recessed within a channel. The lateral line has inspired the development of engineered sensors and concepts in the analysis of flow fields for submersible navigation. The biophysics of CNs are known to be different from the SNs and thereby offer a distinct submodality. However, it is generally unclear whether CNs play a distinct role in behavior. We therefore tested whether CNs enhance foraging in the dark by zebrafish (Danio rerio), a behavior that we elicited with a vibrating rod. We found that juvenile fish, which have only SNs, bite at this rod at about one-third the rate and from as little as one-third the distance of adults for a high-frequency stimulus (50 < f < 100 Hz). We used novel techniques for manipulating the lateral line in adults to find that CNs offered only a modest benefit at a lower frequency (20 Hz) and that foraging was mediated entirely by cranial neuromasts. Consistent with our behavioral results, biophysical models predicted CNs to be more than an order of magnitude more sensitive than SNs at high frequencies. This enhancement helps to overcome the rapid spatial decay in high-frequency components in the flow around the stimulus. These findings contrast what has been previously established for fishes that are at least ten-times the length of zebrafish, which use trunk CNs to localize prey. Therefore, CNs generally enhance foraging, but in a manner that varies with the size of the fish and its prey. These results have the potential to improve our understanding of flow sensing in aquatic animals and engineered systems.

Brain-Wide Mapping of Water Flow Perception in Zebrafish

“…The encoding and processing of the water flow stimuli may change with age, as the ratio of body size to stimulus features changes, and with the development of canal neuromasts (Van Trump and McHenry, 2008;Wada et al, 2014). As such, studying the ontogeny of the processing would be interesting, especially for the afferent neurons receiving information from the newly developed canal neuromasts, which have been linked to foraging in zebrafish (Carrillo et al, 2019). However, collecting such an ontological dataset would require imaging in ossified zebrafish, whose skulls and pigmentation preclude the use of one-photon light sheet microscopy.…”

Physiological responses of mechanosensory systems in the head of larval zebrafish (Danio rerio)

“…Through the lateral line system, fish can detect these hydrodynamic cues and use them to make behavioral decisions ( Bleckmann and Zelick, 2009 ). For example, the detection of hydrodynamic pressure gradients that are generated by nearby prey movements allows predators to localize and approach the prey, thus improving their hunting success ( Coombs and Conley, 1997 ; Montgomery et al, 2002 ; Carrillo and McHenry, 2016 ; Carrillo et al, 2019 ). Similarly, a prey itself may rely on detecting the wakes produced by approaching or striking predators ( Stewart and McHenry, 2010 ; Stewart et al, 2013 ).…”

Learning swimming escape patterns for larval fish under energy constraints

“…Since early studies where prey fish were reported to rapidly accelerate from rest by bending into a C-shape and unfurling their tail [9][10][11][12], impulsive locomotion patterns have been the subject of intense investigation. Studying escape strategies of prey fish has led to the discovery of sensing mechanisms [13][14][15], dedicated neural circuits [16][17][18][19], and bio-mechanic principles [20,21]. From the perspective of hydrodynamics, several studies have sought to understand the C-start escape response and how it imparts momentum to the surrounding fluid [22][23][24][25][26][27].…”