Central Projections of Gustatory Receptor Neurons in the Medial and the Lateral Sensilla Styloconica of Helicoverpa armigera Larvae

Abstract

Food selection behavior of lepidopteran larvae is predominantly governed by the activation of taste neurons present in two sensilla styloconica located on the galea of the maxilla. In this study, we present the ultrastructure of the sensilla styloconica and the central projection pattern of their associated receptor neurons in larvae of the heliothine moth, Helicoverpa armigera. By means of light microscopy and scanning electron microscopy, the previous findings of two morphologically fairly similar sensilla comprising a socketed conic tip inserted into a large peg were confirmed. However, the peg size of the medial sensillum was found to be significantly bigger than that of the lateral sensillum. The sensory neurons derived from each sensillum styloconicum were mapped separately using anterograde staining experiments combined with confocal laser-scanning microscopy. For determining the afferents’ target regions relative to each other, we reconstructed the labeled axons and placed them into a common reference framework. The sensory axons from both sensilla projected via the ipsilateral maxillary nerve to the suboesophageal ganglion and further through the ipsilateral circumoesophageal connective to the brain. In the suboesophageal ganglion, the sensory projections targeted two areas of the ipsilateral maxillary neuropil, one located in the ventrolateral neuromere and the other adjacent to the neuromere midline. In the brain, the axon terminals targeted the dorso-anterior area of the ipsilateral tritocerebrum. As confirmed by the three-dimensional reconstructions, the target regions of the neural projections originating from each of the two sensilla styloconica were identical.

Characteristics of morphology, electrophysiology, and central projections of two sensilla styloconica in Helicoverpa assulta larvae

“…Also, the characteristic arrangement of the socketed conic tip inserted into the large peg is in correspondence to previous findings in other lepidopterous caterpillars [5,[22][23][24][25][26][27][28][29], indicating a conservative morphology of sensilla styloconica over lepidopterous species. Interestingly, the different size of the two sensilla in H. assulta, the medial being significantly longer than the lateral, is in accordance with our previous findings on H. armigera [14]. Such a difference in size between the two sensilla styloconica has not been reported in other species of caterpillars.…”

“…The morphology of the sensilla styloconica of H. assulta, as presented here, is similar to that described previously in the sibling species H. armigera [14]. Also, the characteristic arrangement of the socketed conic tip inserted into the large peg is in correspondence to previous findings in other lepidopterous caterpillars [5,[22][23][24][25][26][27][28][29], indicating a conservative morphology of sensilla styloconica over lepidopterous species.…”

“…Anterograde staining of the receptor neurons was performed as described in Tang et al [14]. In brief, crystals of fluorescent dye (tetramethylrhodamine dextran with biotin, Micro-Ruby, Molecular Probes; Invitrogen, Eugene, Oregon, USA) were applied to the cut end of the sensillum styloconica.…”

“…Also, the sensory axons derived from the two sensilla styloconica have been traced previously in two species of lepidopterous caterpillars, the tobacco hornworm Manduca sexta (Sphingidae) and the Japanese oak silkmoth Antheraea yamamai (Saturniidae), showing that the GRNs project to the ipsilateral subesophageal ganglion (SOG) through the maxillary nerve and then to the ipsilateral brain through the circumesophageal connectives [12,13]. In a recent investigation, on the polyphagous caterpillars Helicoverpa armigera, we found that the GRNs target two areas in the ipsilateral SOG: one located in the ventrolateral maxillary neuromere and the other adjacent to the neuromere midline [14]. In addition, our data showed that the subsequent axons target the dorsoanterior area of the ipsilateral tritocerebrum in the brain.…”

Taste discriminating capability to different bitter compounds by the larval styloconic sensilla in the insect herbivore Papilio hospiton (Géné)

“…Lepidopterous larvae are a simple and attractive model for studying the neural coding mechanisms of taste information because they have few GRNs, the dendrites of which interact with taste stimuli in the environment, and the axons of these neurons project directly, without synapsing, to a region of the brain called the subesophageal ganglion (SOG) (Asaoka, 2002;Tang et al, 2014). Host specificity of lepidopteran insects is determined not only by female oviposition preferences, but also by larval food acceptance.…”