Anatomical Investigation Reveals a Second Olfactory System in Locusts

Olfaction in locusts offers a useful model for understanding how the brain encodes environmental information. While previous studies of olfaction in locusts have focused mainly on the antennal pathway, most insects, including locusts, possess olfactory receptors on their palps. Although they are traditionally considered to be gustatory or mechanosensory structures, accumulating molecular, electrophysiological, and behavioral evidence shows locust palps also mediate olfactory processing. The palps therefore initiate a second olfactory pathway, whose neural architecture and sensory functions remain largely unexplored. Here, we used anatomical approaches to characterize the chemosensory system of the palps in Schistocerca americana, mapping pathways from the peripheral sensilla through the brain to third-order neurons. We found that sensory input from the palps projects to two distinct regions: the gnathal ganglion, which integrates gustatory input from multiple head appendages, and the glomerular lobe of the cerebral ganglion, which, traditionally thought of as a gustatory center, appears instead to receive only olfactory input. The glomerular lobe, in turn, provides olfactory input to the accessory calyx of the mushroom body, a region traditionally considered gustatory. Notably, the palp and antennal olfactory pathways remain anatomically segregated through at least the third-order neurons. Our systematic characterization of the palp olfactory system anatomy challenges existing views of olfactory and gustatory integration in hemimetabolous insects and establishes a framework for comparative studies of antennal and palp-based olfactory coding.