Place learning overrides innate behaviors in Drosophila

Abstract

Animals in a natural environment confront many sensory cues. Some of these cues bias behavioral decisions independent of experience, and action selection can reveal a stimulus–response (S–R) connection. However, in a changing environment it would be a benefit for an animal to update behavioral action selection based on experience, and learning might modify even strong S–R relationships. How animals use learning to modify S–R relationships is a largely open question. Three sensory stimuli, air, light, and gravity sources were presented to individual Drosophila melanogaster in both naïve and place conditioning situations. Flies were tested for a potential modification of the S–R relationships of anemotaxis, phototaxis, and negative gravitaxis by a contingency that associated place with high temperature. With two stimuli, significant S–R relationships were abandoned when the cue was in conflict with the place learning contingency. The role of the dunce (dnc) cAMP-phosphodiesterase and the rutabaga (rut) adenylyl cyclase were examined in all conditions. Both dnc¹ and rut²⁰⁸⁰ mutant flies failed to display significant S–R relationships with two attractive cues, and have characteristically lower conditioning scores under most conditions. Thus, learning can have profound effects on separate native S–R relationships in multiple contexts, and mutation of the dnc and rut genes reveal complex effects on behavior.