Mechanosensory pathways of scorpion pecten hair sensillae-Adjustment of body height and pecten position.

Scorpions' sensory abilities are intriguing, especially the rather enigmatic ventral comb-like chemo- and mechanosensory organs, the so-called pectines. Attached ventrally to the second mesosomal segment just posterior to the coxae of the fourth walking leg pair, the pectines consist of the lamellae, the fulcra, and a variable number of pecten teeth. The latter contain the bimodal peg sensillae, used for probing the substrate with regard to chemo- and mechanosensory cues simultaneously. In addition, the lamellae, the fulcra and the pecten teeth are equipped with pecten hair sensillae (PHS) to gather mechanosensory information. Previously, we have analyzed the neuronal pathway associated with the peg sensillae unraveling their somatotopic projection pattern in dedicated pecten neuropils. Little is known, however, regarding the projections of PHS within the scorpion nervous system. Behavioral and electrophysiological assays showed involvement of PHS in reflexive responses but how the information is integrated remains unresolved. Here, we unravel the innervation pattern of the mechanosensory pecten hair afferents in Mesobuthus eupeus and Euscorpius italicus. By using immunofluorescent labeling and injection of Neurobiotin tracer, we identify extensive arborizations of afferents, including (i) ventral neuropils, (ii) somatotopically organized multisegmental sensory tracts, (iii) contralateral branches via commissures, and (iv) direct ipsilateral innervation of walking leg neuromeres 3 and 4. Our results suggest that PHS function as sensors to elicit reflexive adjustment of body height and obstacle avoidance, mediating accurate pecten teeth alignment to guarantee functionality of pectines, which are involved in fundamental capacities like mating or navigation.

Structure of the pecten neuropil pathway and its innervation by bimodal peg afferents in two scorpion species.

The pectines of scorpions are comb-like structures, located ventrally behind the fourth walking legs and consisting of variable numbers of teeth, or pegs, which contain thousands of bimodal peg sensillae. The associated neuropils are situated ventrally in the synganglion, extending between the second and fourth walking leg neuromeres. While the general morphology is consistent among scorpions, taxon-specific differences in pecten and neuropil structure remain elusive but are crucial for a better understanding of chemosensory processing. We analysed two scorpion species (Mesobuthus eupeus and Heterometrus petersii) regarding their pecten neuropil anatomy and the respective peg afferent innervation with anterograde and lipophilic tracing experiments, combined with immunohistochemistry and confocal laser-scanning microscopy. The pecten neuropils consisted of three subcompartments: a posterior pecten neuropil, an anterior pecten neuropil and a hitherto unknown accessory pecten neuropil. These subregions exhibited taxon-specific variations with regard to compartmentalisation and structure. Most notable were structural differences in the anterior pecten neuropils that ranged from ovoid shape and strong fragmentation in Heterometrus petersii to elongated shape with little compartmentalisation in Mesobuthus eupeus. Labelling the afferents of distinct pegs revealed a topographic organisation of the bimodal projections along a medio-lateral axis. At the same time, all subregions along the posterior-anterior axis were innervated by a single peg's afferents. The somatotopic projection pattern of bimodal sensillae appears to be common among arachnids, including scorpions. This includes the structure and organisation of the respective neuropils and the somatotopic projection patterns of chemosensory afferents. Nonetheless, the scorpion pecten pathway exhibits unique features, e.g. glomerular compartmentalisation superimposed on somatotopy, that are assumed to allow high resolution of substrate-borne chemical gradients.