Reproduction-Related Sound Production of Grasshoppers Regulated by Internal State and Actual Sensory Environment

The interplay of neural and hormonal mechanisms activated by entero- and extero-receptors biases the selection of actions by decision making neuronal circuits. The reproductive behavior of acoustically communicating grasshoppers, which is regulated by short-term neural and longer-term hormonal mechanisms, has frequently been used to study the cellular and physiological processes that select particular actions from the species-specific repertoire of behaviors. Various grasshoppers communicate with species- and situation-specific songs in order to attract and court mating partners, to signal reproductive readiness, or to fend off competitors. Selection and coordination of type, intensity, and timing of sound signals is mediated by the central complex, a highly structured brain neuropil known to integrate multimodal pre-processed sensory information by a large number of chemical messengers. In addition, reproductive activity including sound production critically depends on maturation, previous mating experience, and oviposition cycles. In this regard, juvenile hormone released from the corpora allata has been identified as a decisive hormonal signal necessary to establish reproductive motivation in grasshopper females. Both regulatory systems, the central complex mediating short-term regulation and the corpora allata mediating longer-term regulation of reproduction-related sound production mutually influence each other’s activity in order to generate a coherent state of excitation that promotes or suppresses reproductive behavior in respective appropriate or inappropriate situations. This review summarizes our current knowledge about extrinsic and intrinsic factors that influence grasshopper reproductive motivation, their representation in the nervous system and their integrative processing that mediates the initiation or suppression of reproductive behaviors

Neural representation of calling songs and their behavioral relevance in the grasshopper auditory system

Acoustic communication plays a key role for mate attraction in grasshoppers. Males use songs to advertise themselves to females. Females evaluate the song pattern, a repetitive structure of sound syllables separated by short pauses, to recognize a conspecific male and as proxy to its fitness. In their natural habitat females often receive songs with degraded temporal structure. Perturbations may, for example, result from the overlap with other songs. We studied the response behavior of females to songs that show different signal degradations. A perturbation of an otherwise attractive song at later positions in the syllable diminished the behavioral response, whereas the same perturbation at the onset of a syllable did not affect song attractiveness. We applied naïve Bayes classifiers to the spike trains of identified neurons in the auditory pathway to explore how sensory evidence about the acoustic stimulus and its attractiveness is represented in the neuronal responses. We find that populations of three or more neurons were sufficient to reliably decode the acoustic stimulus and to predict its behavioral relevance from the single-trial integrated firing rate. A simple model of decision making simulates the female response behavior. It computes for each syllable the likelihood for the presence of an attractive song pattern as evidenced by the population firing rate. Integration across syllables allows the likelihood to reach a decision threshold and to elicit the behavioral response. The close match between model performance and animal behavior shows that a spike rate code is sufficient to enable song pattern recognition.Peer Reviewe

Critical Song Features for Auditory Pattern Recognition in Crickets

Many different invertebrate and vertebrate species use acoustic communication for pair formation. In the cricket Gryllus bimaculatus, females recognize their species-specific calling song and localize singing males by positive phonotaxis. The song pattern of males has a clear structure consisting of brief and regular pulses that are grouped into repetitive chirps. Information is thus present on a short and a long time scale. Here, we ask which structural features of the song critically determine the phonotactic performance. To this end we employed artificial neural networks to analyze a large body of behavioral data that measured females’ phonotactic behavior under systematic variation of artificially generated song patterns. In a first step we used four non-redundant descriptive temporal features to predict the female response. The model prediction showed a high correlation with the experimental results. We used this behavioral model to explore the integration of the two different time scales. Our result suggested that only an attractive pulse structure in combination with an attractive chirp structure reliably induced phonotactic behavior to signals. In a further step we investigated all feature sets, each one consisting of a different combination of eight proposed temporal features. We identified feature sets of size two, three, and four that achieve highest prediction power by using the pulse period from the short time scale plus additional information from the long time scale

Sound Signalling in Orthoptera

The sounds produced by orthopteran insects are very diverse. They are widely studied for the insight they give into acoustic behaviour and the biophysical aspects of sound production and hearing, as well as the transduction of sound to neural signals in the ear and the subsequent processing of information in the central nervous system. The study of sound signalling is a multidisciplinary area of research, with a strong physiological contribution. This review considers recent research in physiology and the links with related areas of acoustic work on the Orthoptera

Neuronal precision and the limits for acoustic signal recognition in a small neuronal network

Recognition of acoustic signals may be impeded by two factors: extrinsic noise, which degrades sounds before they arrive at the receiver’s ears, and intrinsic neuronal noise, which reveals itself in the trial-to-trial variability of the responses to identical sounds. Here we analyzed how these two noise sources affect the recognition of acoustic signals from potential mates in grasshoppers. By progressively corrupting the envelope of a female song, we determined the critical degradation level at which males failed to recognize a courtship call in behavioral experiments. Using the same stimuli, we recorded intracellularly from auditory neurons at three different processing levels, and quantified the corresponding changes in spike train patterns by a spike train metric, which assigns a distance between spike trains. Unexpectedly, for most neurons, intrinsic variability accounted for the main part of the metric distance between spike trains, even at the strongest degradation levels. At consecutive levels of processing, intrinsic variability increased, while the sensitivity to external noise decreased. We followed two approaches to determine critical degradation levels from spike train dissimilarities, and compared the results with the limits of signal recognition measured in behaving animals

Modulatory effects of nitric oxide and juvenile hormone on the control of reproductive behavior in female Chorthippus biguttulus

Sowohl Juvenilhormon (JH) als auch Stickstoffmonoxid (NO) beeinflussen das reproduktive Verhalten weiblicher Heuschrecken. Die vorliegende Arbeit untersucht eine mögliche Verbindung zwischen JH und NO Signalen bei der Kontrolle des weiblichen Paarungsverhaltens in der Heuschrecke Chorthippus biguttulus. Die Effekte von JH auf die Lauterzeugung und das Paarungsverhalten von Heuschreckenweibchen wurden nach der Manipulation des JH Levels analysiert. Durch neuroanatomische Studien konnte eine funktionelle Beziehung zwischen JH und NO auf zellulärer Ebene gefunden werden. Die Beobachtung des natürlichen Reproduktionsverhaltens von Ch. biguttulus Weibchen in kleinen Laborpopulationen lieferte ein verlässliches Zeitschema für den Ablauf reproduktiver Stadien. Auf die Imaginalhäutung folgt eine Periode der primären Abwehr , die nach ca. einer Woche direkt in die Periode der aktiven Paarungsbereitschaft übergeht, welche mit weiblicher Lautproduktion einhergeht, die für Männchen ein sehr attraktives Kommunikationssignal darstellt. Weibchen paaren sich mehrere Male bevor sie zur ersten Eiablage kommen. Die experimentelle Manipulation des JH Titers der Hemolymphe zeigte, dass JH benötigt wird, um Reproduktionsverhalten zu initiieren und zu erhalten, jedoch unterdrücken hohe JH Titer die weibliche Lautproduktion. Die Inhibition der NO Produktion durch systemische Applikation eines Stickstoffmonoxidsynthase (NOS) Inhibitors steigerte die weibliche Lautproduktion während sie den JH Titer der Hemolymphe absenkte. In den JH produzierenden Corpora allata wurden NOS exprimierende Zellkörper durch NADPHdiaphorase Färbung, anti NOS Immunfärbung und Immunzytochemie gegen Citrullin, ein Nebenprodukt der NO Synthese, gefunden. RFamid immunreaktive Hirn-zu-Corpora allata Projektionen aus der Pars intercerebralis und lateralis wurden als zelluläre Zielorte der NO-Abgabe in den Corpora allata identifiziert. Die Beteiligung von NO/cGMP Signalen an der Regulation der Corpora allata Funktion, NO Produktion und die Kontrolle der Hormonausschüttung durch RFamid stellt eine Parallele zur Funktion der Adenohypophyse der Vertebraten dar, wo NO unter anderem in gonadotropen Zellen produziert wird und RFamid die Ausschüttung von Gonadotropinen kontrolliert

Sequential Filtering Processes Shape Feature Detection in Crickets: A Framework for Song Pattern Recognition.

Intraspecific acoustic communication requires filtering processes and feature detectors in the auditory pathway of the receiver for the recognition of species-specific signals. Insects like acoustically communicating crickets allow describing and analysing the mechanisms underlying auditory processing at the behavioral and neural level. Female crickets approach male calling song, their phonotactic behavior is tuned to the characteristic features of the song, such as the carrier frequency and the temporal pattern of sound pulses. Data from behavioral experiments and from neural recordings at different stages of processing in the auditory pathway lead to a concept of serially arranged filtering mechanisms. These encompass a filter for the carrier frequency at the level of the hearing organ, and the pulse duration through phasic onset responses of afferents and reciprocal inhibition of thoracic interneurons. Further, processing by a delay line and coincidence detector circuit in the brain leads to feature detecting neurons that specifically respond to the species-specific pulse rate, and match the characteristics of the phonotactic response. This same circuit may also control the response to the species-specific chirp pattern. Based on these serial filters and the feature detecting mechanism, female phonotactic behavior is shaped and tuned to the characteristic properties of male calling song.Supported by the Biotechnology and Biological Sciences Research Council (BB/J01835X/1) and the Isaac Newton Trust (Trinity College, Cambridge).This is the final version of the article. It first appeared from Frontiers via http://dx.doi.org/10.3389/fphys.2016.0004

Investigating an adaptive radiation in temperate Neoconocephalus

Evolution of communication system is seemingly complex requiring coevolution between sender and receiver mechanisms. Studying acoustic communication in the katydid genus Neoconocephalus (coneheaded katydids), I compare traits between individuals and across species looking at patterns of evolution and origins of novel traits. There are three lines of male call trait divergence in Neoconocephalus. Combinations of these traits make species specific call phenotypes, typically matching with female preference for calls. Each novel male call trait has many independent evolutionary origins. Even more excitedly, preliminary studies of female preference for male call traits suggests that the evolutionary history is even more diverse with many different recognition systems forming similar preferences. Based upon comparative methods it appears that communication traits in Neoconocephalus are pliable, easily turned on and off, subject to drift, female preferences are very diverse and male calls seem limited to a few traits. Seven of the ten species of Neoconocephalus found in North America are closely related sharing a single common ancestor. Species in this clade represent all the diversity in acoustic communication found in the entire genus. I propose that this diversification is the result of an adaptive radiation triggered by the extreme ecological opportunity following the last glacial maxima. Molecular-clock analysis reveled that the diversification in this clade occurred in a single glacial cycle. In fact, this adaptive radiation occurred 11 thousand years ago. Previously the most rapid arthropod diversification event known occurred in Hawaiian Laupala crickets five million years ago. I found that temperate Neoconocephalus species were radiating into North America out of tropical grasslands at the same time that humans were entering North American by crossing the Bering Straight.Includes bibliographical references