A sensation for inflation: initial swim bladder inflation in larval zebrafish is mediated by the mechanosensory lateral line

Abstract

Larval zebrafish achieve neutral buoyancy between 4-5 days post-fertilization by swimming up to the surface and taking in air through their mouths to inflate their swim bladders. We define this behavior as 'surfacing'. Little is known about the sensory basis for this underappreciated behavior of larval fish. A strong candidate is the mechanosensory lateral line, a hair cell-based sensory system that detects hydrodynamic information from sources like water currents, predators, prey, and surface waves. However, a role for the lateral line in mediating initial inflation of the swim bladder has not been reported. To explore the connection between the lateral line and surfacing, we utilized a genetic mutant (lhfpl5b-/-) that renders the zebrafish lateral line insensitive to mechanical stimuli. We observe that approximately half of these lateral line mutants over-inflate their swim bladders during initial inflation and become positively buoyant. Thus, we hypothesize that larval zebrafish use their lateral line to moderate interactions with the air-water interface during surfacing to regulate swim bladder inflation. To test the hypothesis that lateral line defects are responsible for swim bladder over-inflation, we show exogenous air is required for the hyperinflation phenotype and transgenic rescue of hair cell function restores normal inflation. We also find that chemical ablation of anterior lateral line hair cells in wild type larvae causes hyperinflation. Furthermore, we show that manipulation of lateral line sensory information results in abnormal inflation. Finally, we report spatial and temporal differences in the surfacing behavior between wild type and lateral line mutant larvae. In summary, we propose a novel sensory basis for achieving neutral buoyancy where larval zebrafish use their lateral line to sense the air-water interface and regulate initial swim bladder inflation.

Larval zebrafish maintain elevation with multisensory control of posture and locomotion

“…Larval zebrafish must instead gulp air at the water's surface to inflate the swim bladder 15 , maintaining volume by control of a sphincter at the junction of the pneumatic duct of the swim bladder and the esophagus 16 . Constitutive and early loss of the head neuromasts of the anterior lateral line 46,47 leads ~50% of larval zebrafish to over-inflate their swim bladders by gulping more air at the surface 38,48 . We propose that our copper treatment similarly affects the esophageal sphincter, leading to a transient secretion of gas that decreases the volume of the swim bladder.…”