Dual antennular chemosensory pathways mediate odor-associative learning and odor discrimination in the Caribbean spiny lobsterPanulirus argus

SUMMARYChemosensory neurons in the antennular flagella of lobsters mediate long-range responses to chemicals. These neurons are part of two parallel chemosensory pathways with different peripheral and central components. Aesthetasc sensilla on the lateral flagella are innervated by chemosensory neurons that project to the olfactory lobes. A diversity of other ‘non-aesthetasc’ sensilla on both lateral and medial flagella are innervated by mechano- and chemosensory neurons, and most of these non-aesthetasc neurons project to the lateral antennular neuropils. We investigated the roles of these two pathways in odor-associative learning and odor discrimination by selectively removing either aesthetasc or non-aesthetasc sensilla from the spiny lobster Panulirus argus. Lobsters lacking both aesthetasc and non-aesthetasc antennular sensilla show very reduced or no odor-mediated searching behavior. We associatively conditioned lobsters using two paradigms: aversive conditioning with generalization testing (which reveals the similarity in the lobsters’ perception of odorants) and discrimination conditioning (which reveals the lobsters’ ability to discriminate odorants). Sham-control intact lobsters performed these tasks well, as did lobsters lacking either aesthetascs or non-aesthetasc setae. There was a strong but statistically non-significant trend that lobsters lacking either aesthetascs or non-aesthetasc setae generalized more between complex odor mixtures than did intact lobsters. After aversive conditioning with generalization testing, aesthetasc-ablated lobsters had more difficulty discriminating among the most closely related complex mixtures than did intact or non-aesthetasc-ablated lobsters. However, after discrimination conditioning, aesthetasc-ablated lobsters were as proficient as intact animals in discriminating highly similar mixtures. These results indicate overlap and redundancy in the function of these two chemosensory pathways in odor-associative learning and odor discrimination, but these pathways also complement each other to enable better discrimination. This study presents the first evidence for a role of non-aesthetasc chemosensory neurons in complex odor-mediated behaviors such as learning and discrimination.