Whole-body central processing of lateral line inputs encodes flow direction relative to the center-of-mass

Abstract

From shifting visual scenes to tactile deformations and fluid motion, animals must interpret patterns of sensory flow around their body to construct stable internal models and produce adaptive behavior. Understanding of how such transformations are encoded within the brain remains incomplete. To tackle this question, we leverage the lateral line of larval zebrafish as a tractable sensory system sensitive to fluid motion that is used to steer navigation, feed, and avoid predators. By presenting stimuli of either direction to neuromasts along the body, we used high-resolution calcium imaging to map hindbrain responses. Unexpectedly, our findings challenge the notion that central lateral line processing lacks topographic structure by revealing a simple yet powerful principle centered on a egocentric spatial framework: the direction and location of local flow motions are encoded in reference to the animals center-of-mass. This simple representation enables the brain to register complex flow patterns and provides a robust basis for subsequent behavioral action selection. MON neurons that encode flow toward the center-of-mass broadly project to form bilateral connections onto reticulospinal neurons that coordinate forward locomotion while MON neurons that encode flow away from the center-of-mass displayed a more selective and unilateral projection profile to command neurons for turns. Our discovery represents a shift from purely somatotopic encoding toward an integrative representation of axial position and directionality combined, revealing a novel principle of encoding spatio-directional cues in the hindbrain. This study advances our understanding of how complex mechanosensory inputs select appropriate motor outputs via simple egocentric neural maps in the hindbrain. Significance StatementSpatial and directional cues are essential to select appropriate actions in response to changes in the environment. How information from broadly distributed mechanosensors across the entire body occurs in the brain enables motor selection remains elusive. By directionally stimulating each and virtually all neuromasts distributed along the lateral line of larval zebrafish, our study uncovers that spatial and directional inputs from each flow sensors is encoded in the medial octavolateralis nuclei relative to the animals center-of-mass in order to subsequently recruit reticulospinal neurons driving forward and turn bouts. These results establish a new framework for understanding how broadly distributed inputs get integrated to recruit motor command neurons responsible for producing diverse behaviors.