Behavioral algorithms of ontogenetic switching in larval and juvenile zebrafish phototaxis

Abstract

Animals undergo major behavioral adjustments during ontogeny, but how the underlying cognitive algorithms change during this process remains elusive. Here, we describe that zebrafish shift from light-seeking to dark-seeking, as they grow from larval to juvenile stage, within the first few weeks of their life. We apply a combination of complementary phototaxis assays in virtual reality and modeling to dissect the computational basis of this transition. We identify three parallel pathways, one analyzing ambient whole-field luminance levels, one spatially comparing light levels across the eyes, and one computing eye-specific temporal derivatives. Larvae mostly use the latter two spatio-temporal computations for navigation, while juveniles largely employ the first one. We build a library of agent-based models to predict animal behavior across stimulation conditions and in more complex environments. Model-based extraction of latent cognitive variables points towards potential neural correlates of the observed behavioral inversion and illustrates a novel way to explore the processes of vertebrate ontogeny. We suggest that zebrafish phototaxis is regulated via parallel processing streams, which could be a universal implementation to change strategies depending on developmental stage, context, or internal state, making behavior flexible and goal-oriented. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=188 SRC="FIGDIR/small/659371v3_ufig1.gif" ALT="Figure 1"> View larger version (49K): org.highwire.dtl.DTLVardef@40848forg.highwire.dtl.DTLVardef@1bed6c6org.highwire.dtl.DTLVardef@68a10org.highwire.dtl.DTLVardef@1525f06_HPS_FORMAT_FIGEXP M_FIG C_FIG HIGHLIGHTSO_LIWe provide a framework to describe how behavioral strategies evolve during ontogeny. C_LIO_LIZebrafish switch their phototactic behavior within the first weeks of their life. C_LIO_LIBrightness navigation strategies can be described with a three-pathway model. C_LIO_LILarvae use spatial cues, while juveniles use ambient whole-field luminance for phototaxis. C_LI