CAREER: Linking sensory neuron plasticity to adaptive injury-induced behavior

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Most animals, including humans, will experience sub-lethal injury at least once in their lives. Injured animals can incur long-lasting costs that impact survival, reproduction, and almost every other aspect of behavior, and which often extend beyond the acute post-injury period. Long-lasting behavioral changes that minimize injury costs are therefore likely to be advantageous and widespread among diverse species. However, despite their obvious importance to survival, the brain mechanisms that govern changes in behavior after injury are poorly understood. The objective of this CAREER proposal is to reveal links between memory-like changes in sensory neurons that detect injury (nociceptors), and long-lasting enhancement of adaptive behaviors that compensate for injury. One group of animals that have evolved particularly complex injury-induced behaviors are cephalopod molluscs (octopus, squid, and cuttlefish), who rely on changeable skin camouflage that is heavily impaired if the skin is injured. Previous work in the investigator’s lab has shown long-lasting behavioral changes in cephalopods that promote survival after injury. This project focuses specifically on asking how these changes are produced by the nervous system, and how these changes may be similar or different from those of other animals, including mammals and humans. Broader impacts of the proposal include science education outreach to pre-K children, research training of diverse student populations, and improved knowledge of invertebrate animal welfare.Injury-induced plasticity underlies a range of long-term behavioral changes, ranging from peripheral reflex hypersensitivity to complex, emotionally-valenced cognitive processing. The PI has shown previously that in cephalopods, activity-dependent nociceptive sensitization promotes hypervigilance toward potential threats, and that this hypervigilance promotes survival. The neural mechanisms driving long-term injury-induced plasticity in defensive behaviors remain poorly understood, and whether nociceptive sensitization also promotes fitness-protecting behavior in other contexts is completely unknown. In this CAREER project, the principal investigator conducts experiments to evaluate whether permanent changes to the intrinsic excitability of nociceptors drives plasticity in higher-order neural circuits governing attention and arousal. Next, the investigator examines whether these circuits modulate not only defensive behavioral plasticity, but also fitness-protecting plasticity in foraging, social, and reproductive contexts. Finally the investigator determines if molecular mechanisms of plasticity driving diverse injury-induced behaviors are shared among invertebrates and vertebrates. The studies involve use of a combination of molecular, genetic, physiological and behavioral techniques. This project provides training and educational experiences for Pre-K children, as well as undergraduate and graduate students from groups under-represented in science.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.