Neuropeptidergic control of innate and adaptive behaviors

Abstract

Innate behaviors regulate a large degree of our daily actions including feeding and escaping from noxious stimuli. Except for reflex actions, innate behaviors are not always static and can be flexibly and adaptively tuned to the animal`s current sensory context and internal state. Neuromodulators including neuropeptides are known to be key components involved in behavioral plasticity in animals. However, exactly where and how they act on innate circuits to regulate adaptive behaviors depending on context and internal state is not well understood. Drosophilamelanogaster larvae have a relatively simple nervous system but exhibit an array of innate behaviors and express conserved neuromodulators. I show here that two innate behaviors, namely noxious light avoidance, and fructose foraging, are driven by the action of a pair of central nervous system neurons (Dp7) and Insulin-like peptide 7 (Ilp7). Interestingly, Dp7 neurons and its peptide Ilp7 promote noxious light avoidance, but limit foraging behavior. I reconstructed the Dp7 neuron network at the synaptic level and showed that they receive extensive somatosensory as well as gustatory input and connect to downstream neurons related to feeding functions. In addition, I identified a local region in Dp7 neurons where noxious light is processed, likely via acute release of Ilp7 acting via the Lgr4 receptor expressed in connected downstream neurons. The identified peptidergic feedforward circuit may aid fast processing of light avoidance behavior. Moreover, I found that in the multisensory context of noxious light and fructose, hunger drives the prioritization for fructose foraging and adaptively tunes down light avoidance behavior. Conversely, sated animals preferred light avoidance to foraging behavior. I could show that this behavioral switch depends on Dp7 neuron function and its neuropeptide Ilp7. In fed animals, Ilp7 action activates the light avoidance circuit, but puts a break on the fructose foraging circuit. In starved animals, reduced Dp7 neuron and Ilp7 function likely drives fructose foraging behavior. Dp7 neurons thus act as hub neurons that integrate the sensory context in a bottom-up manner to tune avoidance and foraging. Overall, the identified Dp7 network allows the larva to adaptively respond to its internal state and external environment, which is a key function of circuits regulating adaptive behavior in all animals.