Stability of olfactory behavior syndromes in the Drosophila larva.

Individuals of many animal populations exhibit idiosyncratic behaviors. One measure of idiosyncratic behavior is a behavior syndrome, defined as the stability of one or more behavior traits in an individual across different situations. While behavior syndromes have been described in various animal systems, their properties and the circuit mechanisms that generate them are poorly understood. We thus have an incomplete understanding of how circuit properties influence animal behavior. Here, we characterize olfactory behavior syndromes in the Drosophila larva. We show that larvae exhibit idiosyncrasies in their olfactory behavior over short time scales. They are influenced by the larva's satiety state and odor environment. Additionally, we identified a group of antennal lobe local neurons that influence the larva's idiosyncratic behavior. These findings reveal previously unsuspected influences on idiosyncratic behavior. They further affirm the idea that idiosyncrasies are not simply statistical phenomena but manifestations of neural mechanisms. In light of these findings, we discuss more broadly the importance of idiosyncrasies to animal survival and how they might be studied.

Internal state affects local neuron function in an early sensory processing center to shape olfactory behavior in Drosophila larvae.

Crawling insects, when starved, tend to have fewer head wavings and travel in straighter tracks in search of food. We used the Drosophila melanogaster larva to investigate whether this flexibility in the insect's navigation strategy arises during early olfactory processing and, if so, how. We demonstrate a critical role for Keystone-LN, an inhibitory local neuron in the antennal lobe, in implementing head-sweep behavior. Keystone-LN responds to odor stimuli, and its inhibitory output is required for a larva to successfully navigate attractive and aversive odor gradients. We show that insulin signaling in Keystone-LN likely mediates the starvation-dependent changes in head-sweep magnitude, shaping the larva's odor-guided movement. Our findings demonstrate how flexibility in an insect's navigation strategy can arise from context-dependent modulation of inhibitory neurons in an early sensory processing center. They raise new questions about modulating a circuit's inhibitory output to implement changes in a goal-directed movement.

Frameshift mutations of YPEL3 alter the sensory circuit function in Drosophila.

A frameshift mutation in Yippee-like (YPEL) 3 was recently found from a rare human disorder with peripheral neurological conditions including hypotonia and areflexia. The YPEL gene family is highly conserved from yeast to human, but its members' functions are poorly defined. Moreover, the pathogenicity of the human YPEL3 variant is completely unknown. We generated a Drosophila model of human YPEL3 variant and a genetic null allele of Drosophila homolog of YPEL3 (referred to as dYPEL3). Gene-trap analysis suggests that dYPEL3 is predominantly expressed in subsets of neurons, including larval nociceptors. Analysis of chemical nociception induced by allyl-isothiocyanate (AITC), a natural chemical stimulant, revealed reduced nociceptive responses in both dYPEL3 frameshift and null mutants. Subsequent circuit analysis showed reduced activation of second-order neurons (SONs) in the pathway without affecting nociceptor activation upon AITC treatment. Although the gross axonal and dendritic development of nociceptors was unaffected, the synaptic contact between nociceptors and SONs was decreased by the dYPEL3 mutations. Furthermore, expressing dYPEL3 in larval nociceptors rescued the behavioral deficit in dYPEL3 frameshift mutants, suggesting a presynaptic origin of the deficit. Together, these findings suggest that the frameshift mutation results in YPEL3 loss of function and may cause neurological conditions by weakening synaptic connections through presynaptic mechanisms.