Neural responses from the wind-sensitive interneuron population in four cockroach species

https://doi.org/10.1016/j.jinsphys.2014.05.017Get rights and content

Highlights

  • We compared cercal wind-sensitive interneuron responses in four cockroach species.

  • Species differed in exhibiting wind-evoked escape responses or flight ability.

  • All four species possessed ascending wind-sensitive interneurons.

  • The species lacking both wind-evoked behaviors exhibited weakest neural responses.

  • The species with a weak escape response but flies exhibited strongest responses.

Abstract

The wind-sensitive insect cercal sensory system is involved in important behaviors including predator detection and initiating terrestrial escape responses as well as flight maintenance. However, not all insects possessing a cercal system exhibit these behaviors. In cockroaches, wind evokes strong terrestrial escape responses in Periplaneta americana and Blattella germanica, but only weak escape responses in Blaberus craniifer and no escape responses in Gromphadorhina portentosa. Both P. americana and B. craniifer possesses pink flight muscles correlated with flight ability while B. germanica possesses white flight muscles that cannot support flight and G. portentosa lacks wings. These different behavioral combinations could correlate with differences in sensory processing of wind information by the cercal system. In this study, we focused on the wind-sensitive interneurons (WSIs) since they provide input to the premotor/motor neurons that influence terrestrial escape and flight behavior. Using extracellular recordings, we characterized the responses from the WSI population by generating stimulus–response (S–R) curves and examining spike firing rates. Using cluster analysis, we also examined the activity of individual units (four per species, though not necessarily homologous) comprising the population response in each species. Our main results were: (1) all four species possessed ascending WSIs in the abdominal connectives; (2) wind elicited the weakest WSI responses (lowest spike counts and spike rates) in G. portentosa; (3) wind elicited WSI responses in B. craniifer that were greater than P. americana or B. germanica; (4) the activity of four individual units comprising the WSI population response in each species was similar across species.

Introduction

Information gathering and behavioral control are two essential functions of the nervous system. Sensory systems allow organisms to extract information about their environment that the nervous system then uses, or ignores, to guide behavior. Additionally, how a sensory modality is incorporated into behavior can affect sensory processing of that modality in an organism. Therefore, how sensory information is encoded and used can vary across organisms. Comparative studies using a model system that involves a measurable behavior with neural correlates that are tractable and accessible for neurophysiological studies are valuable for understanding the neural mechanisms underlying how nervous systems extract, encode and use sensory information to guide behavior. The insect wind-sensitive cercal system, which has been the subject of many neurobiological and neuroethological studies to better understand general principles of nervous system function, can serve as this model system.

The cerci, two posterior appendages, contain filiform hairs that detect air currents and are one of the most sensitive sensory receptors in biology (Barth, 2000, Barth, 2004). A single sensory receptor cell attaches to the base of each filiform hair and its axon projects to the terminal abdominal ganglion (TAG). Within the TAG, the afferents monosynaptically connect to the population of wind-sensitive interneurons (WSIs) that often have large axon diameters and have been termed “giant interneurons” (or GIs). In some insects, the largest nine axons, many of which are WSIs, can comprise as much as 31% (Periplaneta americana) of the abdominal connective cross-sectional area (Boyan and Ball, 1986). The WSIs often occupy the dorsal and ventral intermediate tracts (DIT and VIT, respectively), but have also been found in other anatomical tracts, including the lateral and medial dorsal tracts (LDT and MDT, respectively), dorsal lateral tract (DLT), ventral medial tract (VMT), and ventral lateral tract (VLT). The WSI axons project to the thoracic ganglia containing premotor and motor neurons (motor regions) as well as to the subesophageal and supraesophageal ganglia (Boyan and Ball, 1990, Farley and Milburn, 1969, Spira et al., 1969). Current evidence indicates WSIs activate the thoracic motor regions to generate behavior through indirect (via premotor neurons) synapses to motor neurons (Boyan and Ball, 1989, Casagrand and Ritzmann, 1991, Ritzmann, 1981, Ritzmann and Camhi, 1978, Ritzmann and Pollack, 1981, Ritzmann and Pollack, 1986, Ritzmann and Pollack, 1988, Ritzmann and Pollack, 1990, Westin et al., 1988), though direct synapses could also be present in some systems.

The cercal system has been mostly studied in Orthoptera (i.e. locusts and crickets) and Dictyoptera (i.e. cockroaches and mantids) (reviewed in Boyan and Ball, 1990, Camhi, 1984, Comer and Robertson, 2001, Ritzmann, 1984) as well as Thysanura (firebrats and silverfish; Edwards and Reddy, 1986). Although the basic elements of the cercal system are present across these insect groups, cercal systems vary greatly across species. These variations include differences in cercal morphology (i.e. cercal length, segmented vs. unsegmented cerci, orientation relative to the body axis), filiform hairs (i.e. number, length, and location of hairs), and WSIs (i.e. total number, anatomical tract location, axon diameters, and response properties). The thoracic connections between the WSIs and premotor/motor neurons likely also differ across species, but this has not been widely studied.

The two most common functions of the cercal system are predator detection to initiate terrestrial escape responses (Camhi and Tom, 1978) and providing sensory feedback during flight (Fraser, 1977, Libersat and Camhi, 1988, Ritzmann et al., 1982). These behaviors have been mostly studied in the cockroach P. americana and several cricket species. In predator detection, wind directed at the cerci initiates a two-component terrestrial escape response consisting of a rapid initial turn away from the wind source followed by more variable running and/or, in the case of crickets, jumping (Baba and Shimozawa, 1997, Camhi and Tom, 1978, Dupuy et al., 2011, Tauber and Camhi, 1995). WSIs located in the VIT initiate the turn response (Westin et al., 1977) while WSIs located in the DIT are thought to be involved in the more variable running/jumping phase (Camhi and Nolen, 1981, Ritzmann and Pollack, 1981). WSIs located in the DIT also form the ascending pathway in a sensory feedback loop providing wind information to the flight central pattern generator (CPG) located in the thoracic ganglia (Libersat et al., 1989). This sensory feedback loop functions in maintaining flight through self-generated wind (i.e. “flight maintenance;” Fraser, 1977, Libersat and Camhi, 1988, Ritzmann et al., 1982) and altering flight behavior based on cercal-directed wind generated by external sources (i.e. bat predators; Ganihar et al., 1994). Flight maintenance appears to be a secondary function of WSIs within the DIT, and the cercal system in general, incorporated during the evolution of insect flight (Edwards, 1997).

In some species, such as P. americana, the cercal system mediates both functions and possesses WSIs with large diameter axons in both the DIT and VIT. However, this is not the case for all insects possessing cercal systems. For example, the praying mantis Parasphendale agrionina does not exhibit wind-evoked terrestrial responses, but males incorporate wind directed at the cerci into its flight responses (females do not fly) (Triblehorn, 2003). Furthermore, axons within the VIT occupy less connective space in male P. agrionina compared to species that exhibit wind-mediated terrestrial escape responses while axons in the DIT occupy similar connective space as other species that fly and possess a cercal system. In female P. agrionina, however, DIT axons occupy less connective space (Triblehorn et al., 2012). P. agrionina and P. americana illustrate that variations in the cercal system may correlate with cercal system function in a species.

Differences in wind-mediated behaviors (terrestrial escape responses and flight maintenance) can also occur in closely related species. In cockroaches (Blatteria), wind puffs presented at room temperature evoke terrestrial escape responses in the German cockroach Blattella germanica, but not in the Madagascan hissing cockroach Gromphadorhina portentosa. Furthermore, Simpson et al. (1986) found that wind evoked weak terrestrial responses in Blaberus craniifer (Death’s head cockroach) compared to P. americana. These weaker responses would not be effective for evading capture despite B. craniifer possessing large diameter axons comparable to P. americana in the VIT of the abdominal connectives (Simpson et al., 1986). G. portentosa does not fly since the species lacks wings. Although both B. craniifer and B. germanica possess fully formed wings, only B. craniifer possesses pink flight muscle, which is correlated with flight ability, while B. germanica possesses white flight muscles that cannot support flight (Bell et al., 2007, Kramer, 1956). Compared to white flight muscles, pink flight muscles contain more muscle fibers, larger muscle fibers, and have higher metabolic respiration rates since they possess more mitochondria (cytochromes contribute to the pink coloration of the muscle) and have higher activity from metabolic enzymes such as isocitrate dyhydrogenase and citrate synthase (Zera et al., 1997).

Here, we compare the cercal system sensory processing of wind information in these four species (P. americana, B. germanica, B. craniifer, and G. portentosa) that vary in their wind-mediated behaviors. Our study focused on the WSI population since the WSIs provide input to the premotor/motor neurons that initiate and modify behavior. We used a wind stimulus similar to that used to study the behavioral terrestrial escape responses of P. americana (Camhi and Tom, 1978) and B. craniifer (Simpson et al., 1986), referred to as a “bulk flow” stimulus. Using this stimulus allowed us to make meaningful comparisons between our physiological responses of WSI activity to results from those behavioral studies. We characterized the neural responses by examining how the WSI population encodes wind velocity as well as the spike rates of WSI responses to different wind velocities. We also identified and analyzed individual units comprising the WSI population response.

Section snippets

Animals

This study examined wind-sensitive interneurons (WSIs) in four different cockroach (Blattaria) species: P. americana (Linnaeus, 1758) (Blattidae:Blattinae), B. germanica (Linnaeus, 1767) (Blattellidae:Blattellinae), G. portentosa (Schaum, 1853) (Blaberidae:Oxyhaloinae), and B. craniifer (Burmeister, 1838) (Blaberidae:Blaberinae). These species provide examples of the four different combinations of the presence or absence of terrestrial escape response and flight maintenance wind-mediated

Wind-evoked neural responses across species

Wind puffs evoked neural responses in all four cockroach species, indicating that each species possessed WSIs (Fig. 4). Multiple WSIs contributed to the neural responses based on the different spike amplitudes comprising each species’ responses. Neural responses generated by the WSI population increased with wind velocity, from low range (<10 cm/s) to medium range (108–125 cm/s range) to high range (>185 cm/s) wind velocities across all species. There also was a qualitative difference in the WSI

Discussion

In this study, we investigated four cockroach (Blattaria) species that possess a wind-sensitive cercal system, but differ in whether they exhibit two cercal-mediated wind behaviors: terrestrial escape responses and flight maintenance. Wind only evokes terrestrial escape responses in P. americana and B. germanica. In B. craniifer, wind only elicits weak terrestrial escape responses and elicits no terrestrial escape responses in G. portentosa. Flight has been well-characterized in P. americana

Acknowledgements

This work was supported by Grants from the National Center for Research Resources [Grant number 5 P20 RR016461] and the National Institute of General Medical Sciences [Grant number 8 P20 GM103499] from the National Institutes of Health; and a Howard Hughes Medical Institute (HHMI) Undergraduate Education Grant. The authors would like to thank Tyler Dobbins and Catherine Harpe for their help in constructing the wind stimulus setup and Nedda Joudeh for her comments on the manuscript. Finally, the

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