Evolution of a central dopamine circuit underlies adaptation of a light-evoked sensorimotor response in the blind cavefish.

Abstract

Adaptive behaviors emerge in novel environments through functional changes in neural circuits. While relationships between circuit function and behavior are well studied, how evolution shapes circuits to drive behavioral adaptation is poorly understood. The Mexican cavefish, <i>Astyanax mexicanus</i>, provides a unique genetically tractable model, with above ground eyed surface fish and multiple blind cavefish populations that have evolved in darkness. These differences in environment and vision offer a way to examine how neural circuits evolve. We examine differences in detection and behavioral responses to the nonvisual effects of light in cave and surface <i>A. mexicanus</i>. Both populations exhibit photokinesis: Surface fish become hyperactive after darkness, and cavefish after illumination. Using whole-brain functional imaging aligned to an established <i>Astyanax</i> brain atlas, we identify the caudal posterior tuberculum as key to light- and dark-induced photokinesis. Pan-neuronal GCaMP imaging shows that dark-sensitive neurons in surface fish are light-sensitive in cavefish. Light sensing depends on dopamine signaling, suggesting that a conserved dopamine circuit mediates photokinesis and highlighting <i>Astyanax</i> as a model for sensory adaptation.