Behavioral, Endocrine, and Neuronal Responses to Odors in Lampreys

Lampreys are primitive fish that rely significantly on olfactory cues throughout their complex life cycle. The olfactory system of the sea lamprey (Petromyzon marinus) is among the best characterized in vertebrates. In recent decades, tremendous advances have been made by isolating individual compounds from sea lampreys that can replicate natural behavior when artificially applied in the wild. In no other aquatic vertebrate has the olfactory ecology been described in such extensive detail. In the first section, we provide a comprehensive review of olfactory behaviors induced by specific, individual odorants during every major developmental stage of the sea lamprey in behavioral contexts such as feeding, predator avoidance, and reproduction. Moreover, pheromonal inputs have been shown to induce neuroendocrine responses through the hypothalamic-pituitary-gonadal axis, triggering remarkable developmental and physiological effects, such as gametogenesis and increased pheromone release. In the second section of this review, we describe a hypothetical endocrine signaling pathway through which reproductive fitness is increased following pheromone detection. In the final section of this review, we focus on the neuronal circuits that transform olfactory inputs into motor output. We describe specific brain signaling pathways that underlie odor-evoked locomotion. Furthermore, we consider possible modulatory inputs to these pathways that may induce plasticity in olfactory behavior following changes in the external or internal environment. As a whole, this review synthesizes previous and recent progress in understanding the behavioral, endocrine, and neuronal responses of lampreys to chemosensory signals.