Divergent Visuomotor Strategies in Teleosts: Neural Circuit Mechanisms in Zebrafish and Danionella cerebrum

Abstract

Many animals respond to sensory cues with species-specific coordinated movements to successfully navigate their environment. However, the neural mechanisms that support diverse sensorimotor transformations across species with distinct navigational strategies remain largely unexplored. By comparing related teleost species, zebrafish (Danio rerio, ZF) and Danionella cerebrum (DC), we investigated behavioral patterns and neural architectures during the visually guided optomotor response (OMR). Closed-loop behavioral tracking during visual stimulation revealed that larval ZF employ burst-and-glide locomotion, while larval DC display continuous, smooth swimming punctuated with sharp directional turns. Although DC achieve higher average speeds, they lack the direction-dependent velocity modulation observed in ZF. Whole-brain two-photon calcium imaging and tail tracking in head-fixed fish reveals that both species exhibit direction-selective motion encoding in homologous regions, including the retinorecipient pretectum, with DC exhibiting fewer binocular, direction-selective neurons overall. Kinematic analysis of head-fixed behavior reveals that DC sustain significantly longer directed swim events across all stimuli than ZF, highlighting the divergent visuomotor strategies, with ZF reducing tail movement duration in response to oblique, turn-inducing stimuli. Lateralized motor-associated neural activity in the medial and anterior hindbrain of both species suggests a shared circuit motif, with distinct neural circuits that independently control movement vigor and direction. These findings highlight the diversity in visuomotor strategies among teleost species, underscored by shared sensorimotor neural circuit motifs, and establish a robust framework for unraveling the neural mechanisms driving continuous and discrete visually guided locomotion, paving the way for deeper insights into vertebrate sensorimotor functions. Research HighlightsO_LILarval DC exhibit faster swimming than ZF, matching the direction of visual motion. C_LIO_LIDC execute OMR in smooth, curved swimming patterns, interspersed with sharp directional turns. C_LIO_LIZF and DC share similar visuomotor neural architecture, recruiting pretectal and hindbrain regions. C_LIO_LIZF and DC demonstrate lateralized encoding of turns, particularly in medial hindbrain neurons. C_LI In BriefLarval Danionella cerebrum respond to global visual motion cues in smooth, low-angle swimming patterns, interspersed with sharp directional turns, swimming consistently faster than zebrafish. Fouke et al. use behavioral tracking of freely moving and head fixed fish to reveal an evolutionarily conserved visuomotor neural architecture transforming visual motion cues into species-specific locomotor behaviors. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=200 SRC="FIGDIR/small/624938v1_ufig1.gif" ALT="Figure 1"> View larger version (64K): org.highwire.dtl.DTLVardef@13076f4org.highwire.dtl.DTLVardef@d18dc8org.highwire.dtl.DTLVardef@1b35025org.highwire.dtl.DTLVardef@152d2f0_HPS_FORMAT_FIGEXP M_FIG O_FLOATNOGraphical AbstractC_FLOATNO C_FIG