In animal societies, chemical communication plays an important role in conflict and cooperation. For ants, cuticular hydrocarbon (CHC) blends produced by non-nestmates elicit overt aggression. We describe a sensory sensillum on the antennae of the carpenter ant Camponotus japonicus that functions in nestmate discrimination. This sensillum is multiporous and responds only to non-nestmate CHC blends. This suggests a role for a peripheral recognition mechanism in detecting colony-specific chemical signals.

The antennae are a critically important component of the ant's highly elaborated chemical communication systems. However, our understanding of the organization of the sensory systems on the antennae of ants, from peripheral receptors to central and output systems, is poorly understood. Consequently, we have used scanning electron and confocal laser microscopy to create virtually complete maps of the structure, numbers of sensory neurons, and distribution patterns of all types of external sensilla on the antennal flagellum of all types of colony members of the carpenter ant Camponotus japonicus. Based on the outer cuticular structures, the sensilla have been classified into seven types: coelocapitular, coeloconic, ampullaceal, basiconic, trichoid-I, trichoid-II, and chaetic sensilla. Retrograde staining of antennal nerves has enabled us to count the number of sensory neurons housed in the different types of sensilla: three in a coelocapitular sensillum, three in a coeloconic sensillum, one in an ampullaceal sensillum, over 130 in a basiconic sensillum, 50-60 in a trichoid-I sensillum, and 8-9 in a trichoid-II sensillum. The basiconic sensilla, which are cuticular hydrocarbon-receptive in the ant, are present in workers and unmated queens but absent in males. Coelocapitular sensilla (putatively hygro- and thermoreceptive) have been newly identified in this study. Coelocapitular, coeloconic, and ampullaceal sensilla form clusters and show biased distributions on flagellar segments of antennae in all colony members. The total numbers of sensilla per flagellum are about 9000 in unmated queens, 7500 in workers, and 6000 in males. This is the first report presenting comprehensive sensillar maps of antennae in ants.

In the primary olfactory center of animals, glomeruli are the relay stations where sensory neurons expressing cognate odorant receptors converge onto interneurons. In cockroaches, moths, and honeybees, sensory afferents from sensilla on the anterodorsal surface and the posteroventral surface of the flagellum form two nerves of almost equal thicknesses. In this study, double labeling of the two nerves, or proximal/distal regions of the nerves, with fluorescent dyes was used to investigate topographic organization of sensory afferents in the honeybee. The sensory neurons of ampullaceal sensilla responsive to CO2, coelocapitular sensilla responsive to hygrosensory, and thermosensory stimuli and coeloconic sensilla of unknown function were characterized with large somata and supplied thick axons exclusively to the ventral nerve. Correspondingly, all glomeruli innervated by sensory tract (T) 4 received thick axonal processes exclusively from the ventral nerve. Almost all T1-3 glomeruli received a similar number of sensory afferents from the two nerves. In the macroglomerular complexes of the drone, termination fields of afferents from the two nerves almost completely overlapped; this differs from moths and cockroaches, which show heterogeneous terminations in the glomerular complex. In T1-3 glomeruli, sensory neurons originating from more distal flagellar segments tended to terminate within the inner regions of the cortical layer. These results suggest that some degree of somatotopic organization of sensory afferents exist in T1-3 glomeruli, and part of T4 glomeruli serve for processing of hygro- and thermosensory signals.

Most insects are equipped with specialized thermo- and hygroreceptors to locate a permissible range of ambient temperature and distant water sources, respectively. In the cockroach, Periplaneta americana, cold, moist, and dry receptor cells in the antennae send axons to particular sets of two or three glomeruli in the dorsocentral part of the antennal lobe (primary olfactory center), designated DC1-3 glomeruli. However, it is not known how thermo- and hygrosensory signals from these glomeruli are represented in higher-order centers, the protocerebrum, in any insect species. With the use of intracellular recording and staining techniques, we identified a new class of interneurons with dendrites almost exclusively in the DC1, DC2, or DC3 glomeruli and axons projecting to the protocerebrum in the cockroach. Remarkably, terminals of all these projection neurons (PNs) covered almost identical areas in the lateral protocerebrum (LP), although their termination areas outside the LP differed from neuron to neuron. The termination areas within the LP were distinct from, but close to, those of uniglomerular and macroglomerular PNs that transmitted signals concerning general odors and female sex pheromones, respectively. PNs originating from DC1, DC2, and DC3 glomeruli exhibited excitatory responses to cold, moist, and dry stimuli, respectively, probably due to excitatory synaptic input from cold, moist, and dry receptor cells, respectively, whereas their responses were often modulated by olfactory stimuli. These findings suggested that dorsocentral PNs participate in neural pathways that lead to behavioral responses to temperature or humidity changes.