Sensing flow when it matters: a behavioral and circuit analysis of mechanosensation in the larval zebrafish

Abstract

When flying or swimming, animals must adjust their own movement to compensate for displacements induced by the flow of the surrounding air or water. These flow-induced displacements can most easily be detected as visual whole field motion with respect to the animal’s frame of reference. In spite of this, many aquatic animals consistently orient and swim against oncoming flows (a behavior known as rheotaxis) even in the absence of visual cues. How animals achieve this task, and its underlying sensory basis, is still unknown. Here we show that in the absence of visual information, larval zebrafish (\textit{Danio rerio}) perform rheotaxis by using flow velocity gradients as navigational cues. We present behavioral data that support a novel algorithm based on such local velocity gradients, that fish use to efficiently avoid getting dragged by flowing water. Specifically, we show that fish use their mechanosensory lateral line to first sense the curl (or vorticity) of the local velocity vector field to detect the presence of flow and, second, measure its temporal change following swim bouts to deduce flow direction. These results reveal an elegant navigational strategy based on the sensing of flow velocity gradients. Such a refined sensitivity to velocity gradients underscores the need that animals have to correctly identify the source of sensory stimuli to guide appropriate responses. Because fluid drag during locomotion can strongly activate the lateral line, the accurate interpretation of mechanosensory inputs requires that animals distinguish between external and self-generated stimuli. To overcome this kind of challenge, most organisms have evolved to perform neural computations that can nullify or otherwise compensate for the expected self-generated stimulation. These involve efference copies, which are signals from motor-command centers that inform the sensory pathway about impending movements. The existence of diverse centrifugal projections that contact the lateral line suggests that efference copy mechanisms are involved in this process, yet the circuitry and its consequences on behavior are not well understood. Using retrograde labeling of the lateral line nerve, we identify two parallel descending inputs that can influence lateral line sensitivity. We perform functional imaging to show that cholinergic signals originating from the the hindbrain transmit efference copies that cancel out self-generated stimulation during locomotion, while dopaminergic signals from the hypothalamus may have a role in threshold modulation in response to locomotion and salient mechanosensory stimuli. We propose that this simple circuit is involved in state-dependent gain modulation and are currently investigating its importance for sensory processing during spontaneous locomotion and mechanosensory-guided behaviors.