Phonotaxis In Crickets Research Articles

Connecting brain to behaviour: a role for general purpose steering circuits in insect orientation?

The lateral accessory lobes (LALs), paired structures that are homologous among all insect species, have been well studied for their role in pheromone tracking in silkmoths and phonotaxis in crickets, where their outputs have been shown to correlate with observed motor activity. Further studies have shown more generally that the LALs are crucial both for an insect's ability to steer correctly and for organising the outputs of the descending pathways towards the motor centres. In this context, we propose a framework by which the LALs may be generally involved in generating steering commands across a variety of insects and behaviours. Across different behaviours, we see that the LAL is involved in generating two kinds of steering: (1) search behaviours and (2) targeted steering driven by direct sensory information. Search behaviours are generated when the current behaviourally relevant cues are not available, and a well-described LAL subnetwork produces activity which increases sampling of the environment. We propose that, when behaviourally relevant cues are available, the LALs may integrate orientation information from several sensory modalities, thus leading to a collective output for steering driven by those cues. These steering commands are then sent to the motor centres, and an additional efference copy is sent back to the orientation-computing areas. In summary, we have taken known aspects of the neurophysiology and function of the insect LALs and generated a speculative framework that suggests how LALs might be involved in steering control for a variety of complex real-world behaviours in insects.

Internal state transition to switch behavioral strategies in cricket phonotaxis.

Animals employ multiple behavioral strategies for exploring food and mating partners based on both their internal state and external environment. Here, we examined how cricket phonotaxis, which was considered an innate reactive behavior of females to approach the calling song of conspecific males, depended on these internal and external conditions. Our observation revealed that the phonotaxis process consisted of two distinctive phases: wandering and approaching. In the latter phase, crickets moved directly towards the sound source. The transition into this phase, referred to as the 'approach phase', was based on changes in the animal's internal state. Moreover, retention of the approach phase required recognition of the calling song, while song loss downregulated cricket mobility and induced frequent stopping. This is a typical movement in local search behaviors. Our results indicate that phonotaxis is not only a reactive response but a complicated process including multiple behavioral strategies.

Background noise disrupts host-parasitoid interactions.

The soundscape serves as a backdrop for acoustic signals dispatched within and among species, spanning mate attraction to parasite host detection. Elevated background sound levels from human-made and natural sources may interfere with the reception of acoustic signals and alter species interactions and whole ecological communities. We investigated whether background noise influences the ability of the obligate parasitoid Ormia ochracea to locate its host, the variable field cricket (Gryllus lineaticeps). As O. ochracea use auditory cues to locate their hosts, we hypothesized that higher background noise levels would mask or distract flies from cricket calls and result in a decreased ability to detect and navigate to hosts. We used a field manipulation where fly traps baited with playback of male cricket advertisement calls were exposed to a gradient of experimental traffic and ocean surf noise. We found that increases in noise amplitude caused a significant decline in O. ochracea caught, suggesting that background noise can influence parasitoid–host interactions and potentially benefit hosts. As human-caused sensory pollution increases globally, soundscapes may influence the evolution of tightly co-evolved host–parasitoid relationships. Future work should investigate whether female cricket phonotaxis towards males is similarly affected by noise levels.

Calls of Recently Introduced Coquí Frogs Do Not Interfere with Cricket Phonotaxis in Hawaii

Acoustically-signaling animals such as crickets may experience interference from environmental noise, a particular concern given the rise in anthropogenic or other novel sources of sound. We examined the potential for acoustic interference of female phonotaxis to calling song in the Pacific field cricket (Teleogryllus oceanicus) by invasive coqui frogs (Eleutherodactylus coqui) in Hawaii. The frogs were introduced to Hawaii from Puerto Rico in the 1980s. When female crickets were exposed to male calling songs with and without simultaneous broadcast of a coqui chorus, they were equally likely to move toward the cricket song, regardless of the location of the frog sound (ground level or above ground). Unlike some species of frogs and birds, T. oceanicus do not appear to experience acoustic interference from an introduced signaler, even though the introduced species’ calls subjectively seem to be masking the crickets’ songs.

Selective phonotaxis of female crickets under natural outdoor conditions

Acoustic mate choice in insects has been extensively studied under laboratory conditions, using different behavioural paradigms. Ideally, however, mate choice designs should reflect natural conditions, including the physical properties of the transmission channel for the signal. Since little is known about the discrimination ability of females between male song variants under natural conditions, we performed phonotaxis experiments with female field crickets (Gryllus bimaculatus) outdoors, using two-choice decisions based on differences in carrier frequency, sound pressure level, and chirp rate. For all three song parameters, minimum differences necessary for a significant preference between two song models were considerably larger outdoors compared to laboratory conditions. A minimum amplitude difference of 5 dB was required for a significant choice in the field, compared to only 1–2 dB reported for lab-based experiments. Due to the tuned receiver system, differences in carrier frequency equal differences in perceived loudness, and the results on choice for differences in carrier frequency corroborate those in amplitude. Similarly, chirp rate differences of 50 chirps/min were required outdoors compared to only 20 chirps/min in the lab. For predictions about patterns of sexual selection, future studies need to consider the different outcomes of mate choice decisions in lab and field trials.

Changes in the selectivity of phonotaxis and its neuronal correlates in response to prothoracic nanoinjection of modulators in female cricket Acheta domesticus

Event Abstract Back to Event Changes in the selectivity of phonotaxis and its neuronal correlates in response to prothoracic nanoinjection of modulators in female cricket Acheta domesticus Benjamin Navia1*, Ashley Groeneweg2, John Stout2 and Gordon Atkins2 1 Kettering College, Department of Science and Math, United States 2 Andrews University, Department of Biology, United States Phonotaxis in female crickets has been shown to exhibit variability. While some females respond to syllable periods typical of the males’ calling song (50–70 ms), others only respond to calling songs with shorter or longer syllable periods, outside the range of males’ calling songs. Other females are not selective to any syllable period and respond to the full range of calling songs. Nanoinjection of histamine into the prothoracic ganglion decreases phonotactic selectivity. Nanoinjection of antihistamine has the reverse effect. Nanoinjection of Juvenile Hormone III increases phonotactic selectivity, while a protein kinase C inhibitor blocks the effect of Juvenile Hormone III. This suggests that Juvenile Hormone II exerts its effects through a protein kinase C pathway. The L3 neuron is a prothoracic interneuron in female crickets that responds selectively to the syllable period of the male’s calling song. The L3 neuron has been proposed to be responsible for syllable period-selective responses during phonotaxis. If this is true, then L3s should show variable responses, which would parallel the phonotactic behavior. Preliminary results indicate that the application of histamine to the prothoracic ganglion decreases the selective responses, whereas injections of antihistamine increases L3s’ selectivity. This mirrors the effect of these two modulators on phonotactic selectivity. Juvenile Hormone applications also increase the selective responses of L3 similar to its effect on phonotaxis. The effect of protein kinase C blockers on the response of L3s is currently being tested. To date the data support the hypothesis that processing by L3 contributes to the syllable period selective phonotaxis observed in this species. References Atkins G., Kilmer J. et al. (2008) Modulation of syllable period-selective phonotaxis by neural processing in the prothoracic ganglion of female crickets (Acheta domesticus): juvenile hormone III, picrotoxin and phonoinactivation of the ON1 neurons. Physiological Entomology 33, 322-333 Navia B. (2005) Plasticity in the selectivity of phonotaxis and neuronal response in crickets. PhD dissertation, Loma Linda University, Loma Linda, California Stout J., Navia B. et al. (2010) Plasticity of the phonotactic selectiveness of four species of chirping crickets (gryllidae): implications for call recognition. Physiological Entomology 35, 99-116 Keywords: Neuronal Plasticity, phonotaxis Conference: Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012. Presentation Type: Poster Presentation (see alternatives below as well) Topic: Sensory: Audition Citation: Navia B, Groeneweg A, Stout J and Atkins G (2012). Changes in the selectivity of phonotaxis and its neuronal correlates in response to prothoracic nanoinjection of modulators in female cricket Acheta domesticus. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00332 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 30 Apr 2012; Published Online: 07 Jul 2012. * Correspondence: Dr. Benjamin Navia, Kettering College, Department of Science and Math, Kettering, Ohio, 45429, United States, benjamin.navia@kc.edu Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Benjamin Navia Ashley Groeneweg John Stout Gordon Atkins Google Benjamin Navia Ashley Groeneweg John Stout Gordon Atkins Google Scholar Benjamin Navia Ashley Groeneweg John Stout Gordon Atkins PubMed Benjamin Navia Ashley Groeneweg John Stout Gordon Atkins Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Acoustic mate choice in field crickets: influence of environment and behavioral paradigms

Acoustic mate choice in field crickets: influence of environment and behavioral paradigms

Processing of species-specific auditory patterns in the cricket brain by ascending, local, and descending neurons during standing and walking

The recognition of the male calling song is essential for phonotaxis in female crickets. We investigated the responses toward different models of song patterns by ascending, local, and descending neurons in the brain of standing and walking crickets. We describe results for two ascending, three local, and two descending interneurons. Characteristic dendritic and axonal arborizations of the local and descending neurons indicate a flow of auditory information from the ascending interneurons toward the lateral accessory lobes and point toward the relevance of this brain region for cricket phonotaxis. Two aspects of auditory processing were studied: the tuning of interneuron activity to pulse repetition rate and the precision of pattern copying. Whereas ascending neurons exhibited weak, low-pass properties, local neurons showed both low- and band-pass properties, and descending neurons represented clear band-pass filters. Accurate copying of single pulses was found at all three levels of the auditory pathway. Animals were walking on a trackball, which allowed an assessment of the effect that walking has on auditory processing. During walking, all neurons were additionally activated, and in most neurons, the spike rate was correlated to walking velocity. The number of spikes elicited by a chirp increased with walking only in ascending neurons, whereas the peak instantaneous spike rate of the auditory responses increased on all levels of the processing pathway. Extra spiking activity resulted in a somewhat degraded copying of the pulse pattern in most neurons.

Evaluating the importance of different temporal features of calling songs in cricket phonotaxis

Event Abstract Back to Event Evaluating the importance of different temporal features of calling songs in cricket phonotaxis Gundula Meckenhäuser1, 2*, Matthias R. Hennig3 and Martin P. Nawrot1, 2 1 Freie Universität Berlin, Institute of Biology, Germany 2 Bernstein Center for Computational Neuroscience Berlin, Germany 3 Humboldt-Universität zu Berlin, Department of Biology, Germany Acoustic signals are used by Gryllus bimaculatus to communicate and they play a key role in mate choice. Males produce calling songs to attract females, females in turn use these songs to discriminate conspecific songs from the signals of other species. If they are willing to pair females approach the singing male - a behavior referred to as phonotaxis. So far, extensive behavioral experiments in which phonotactic responses of female crickets were tested by varying song features, revealed that song patterns are processed in the time rather than in the spectral domain [1]. Here, we explored the relevant cues for song pattern discrimination on several time scales. We present feed-forward artificial neural networks (ANNs) that quantitatively predict the phonotactic value for untested calling songs that are described by temporal features such as duration, pause, period and duty cycle for both pulses and chirps. We employ ANNs with the following architecture: Input neurons representing temporal song features project to nonlinear neurons in the hidden layer which project to the output neuron that relates the phonotactic value. For training and testing the networks we used 218 artificial songs for which the phonotactic values had already been determined in experiments. Our complete ANNs that use eight temporal song features show a mean squared error (MSE) of MSE = 0.034. By a greedy backward elimination of features, we came up with minimal ANNs using just pulse period, chirp duration and chirp duty cycle as features. The dimensionality reduction of the feature space also improved the performance: The mean squared error for minimal networks is MSE = 0.019. Thus, our findings suggest that among all tested temporal features, pulse period on the short time scale and chirp duration and chirp duty cycle on the long time scale are the most relevant ones for the evaluation of conspecific signals. Further, the minimal ANNs show high predictive power and can be used to complement experimental testing of female phonotaxis in the laboratory. Acknowledgements This work is funded by the German Research Council (DFG) within the Collaborative Research Center "Theoretical Biology" (SFB 618).

Closed-loop Locomotion Analyzer for Investigating Context-dependent Collision Avoidance Systems in Insects

Insects are capable of extremely rapid collision avoidance behaviors with a minimum of processing overhead. These features make them interacting for robotics. To implement the strategies of insect in mobile robots or cars, a through evaluation of these systems is necessary. We developed a closed-loop experimental system for analyzing insect collision avoidance behavior in virtual environments. In the current implementation, a tethered female cricket walks on a floating sphere and the rotations of the sphere are translated into movements of a “virtual cricket” in a computer-generated virtual space. Visual information including obstacle and background patterns in the virtual space are then fed back to the tethered cricket as visual stimuli projected onto a screen in front of the cricket. To induce reliably reproducible straight-line walking, we applied the male calling song that induces positive phonotaxis in female crickets. We demonstrated that the tethered female cricket displayed collision avoidance behavior in response to visual stimuli during positive phonotaxis. By employing this system, we investigated a key stimulus that triggered collision avoidance behavior in crickets in different behavioral contexts: a cricket approaching a static object and an object moving towards a quiescent cricket. The results indicate that crickets used a certain threshold of image size (visual angle) of the projected object as a key stimulus. Furthermore, we found that the threshold depended on the behavioral context: quiescent crickets started avoidance farther from the approaching object compared to crickets walking towards a static object. We conclude that behavioral context is an important factor in decision making. With our closed-loop system for behavioral analysis, we can systematically extract the conditions under which optimal behavioral performance is obtained. This will be an important step in the design of sensory processors for robots.

Hyperacute Directional Hearing and Phonotactic Steering in the Cricket (Gryllus bimaculatus deGeer)

BackgroundAuditory mate or prey localisation is central to the lifestyle of many animals and requires precise directional hearing. However, when the incident angle of sound approaches 0° azimuth, interaural time and intensity differences gradually vanish. This poses a demanding challenge to animals especially when interaural distances are small. To cope with these limitations imposed by the laws of acoustics, crickets employ a frequency tuned peripheral hearing system. Although this enhances auditory directionality the actual precision of directional hearing and phonotactic steering has never been studied in the behaviourally important frontal range.Principal FindingsHere we analysed the directionality of phonotaxis in female crickets (Gryllus bimaculatus) walking on an open-loop trackball system by measuring their steering accuracy towards male calling song presented at frontal angles of incidence. Within the range of ±30°, females reliably discriminated the side of acoustic stimulation, even when the sound source deviated by only 1° from the animal's length axis. Moreover, for angles of sound incidence between 1° and 6° the females precisely walked towards the sound source. Measuring the tympanic membrane oscillations of the front leg ears with a laser vibrometer revealed between 0° and 30° a linear increasing function of interaural amplitude differences with a slope of 0.4 dB/°. Auditory nerve recordings closely reflected these bilateral differences in afferent response latency and intensity that provide the physiological basis for precise auditory steering.ConclusionsOur experiments demonstrate that an insect hearing system based on a frequency-tuned pressure difference receiver achieves directional hyperacuity which easily rivals best directional hearing in mammals and birds. Moreover, this directional accuracy of the cricket's hearing system is reflected in the animal's phonotactic motor response.

Phonotactic walking paths of field crickets in closed-loop conditions and their simulation using a stochastic model

Field cricket females localize one of many singing males in the field in closed-loop multi-source conditions. To understand this behaviour, field cricket phonotaxis was investigated in a closed-loop walking phonotaxis paradigm, in response to two simultaneously active speakers playing aphasic calling songs. Female phonotactic paths were oriented towards the louder sound sources, but showed great inter-individual variability. Decisions made in the initial phases were correlated with the overall directions of the paths. Interestingly, the sound pressure levels of stimuli did not greatly influence several features of phonotactic paths such as sinuosity, walking bout lengths and durations. In order to ascertain the extent of our understanding of walking phonotaxis, a stochastic model was used to simulate the behaviour observed in the experiment. The model incorporated data from the experiment and our current understanding of field cricket auditory physiology. This model, based on stochastic turning towards the louder side, successfully recaptured several qualitative and quantitative features of the observed phonotactic paths. The simulation also reproduced the paths observed in a separate outdoor field experiment. Virtual crickets that were unilaterally deafened or had poor ear directionality exhibited walking paths similar to those observed in previous experiments.

Validating biorobotic models**Part of the 3rd Neuro-IT and Neuroengineering Summer School Tutorial Series.

Some issues in neuroscience can be addressed by building robot models of biological sensorimotor systems. What we can conclude from building models or simulations, however, is determined by a number of factors in addition to the central hypothesis we intend to test. These include the way in which the hypothesis is represented and implemented in simulation, how the simulation output is interpreted, how it is compared to the behaviour of the biological system, and the conditions under which it is tested. These issues will be illustrated by discussing a series of robot models of cricket phonotaxis behaviour.

New technologies for testing a model of cricket phonotaxis on an outdoor robot

If biological inspiration can be used to build robots that deal robustly with complex environments, it should be possible to demonstrate that ‘biorobots’ can function in natural environments. We report on initial outdoor experiments with a robot designed to emulate cricket behaviour. The work integrates a detailed neural model of auditory localisation in the cricket with a robot morphology that incorporates principles of six-legged locomotion. We demonstrate that it can successfully track a cricket calling song over natural terrain. Limitations in its capability are evaluated, and a number of biologically based improvements are suggested for future work.

Reafferent or Redundant: Integration of Phonotaxis and Optomotor Behavior in Crickets and Robots

A general problem in understanding the mechanisms underlying animal behavior is the integration or interaction of different sensorimotor systems. Webb and Harrison (2000a, b) investigated the addition of an optomotor reflex to a sound-localizing robot modeled on cricket behavior. Böhm, Schildberger, and Huber (1991) proposed a simple additive mechanism to explain how the cricket combines the two behaviors. Problems implementing this on the robot led us to propose an alternative inhibition mechanism, which proved effective. Here we directly compare these two possibilities and several further alternatives. First, in a simulation of the open-loop paradigm used by Böhm et al. we demonstrate that there are at least five algorithms (including “efferent copy”) that may adequately account for the data they present. We then consider possible neural implementations of several of these schemes, and test them in robot experiments. The results suggest that inhibition is both neurally plausible and effective as a means of combining these behaviors in real sensorimotor situations.

Physical and temporal scaling considerations in a robot model of cricket calling song preference.

Behavioral experiments with crickets show that female crickets respond to male calling songs with syllable rates within a certain bandwidth only. We have made a robot model in which we implement a simple neural controller that is less complex than the controllers traditionally hypothesized for cricket phonotaxis and syllable rate preference. The simple controller, which had been successfully used with a slowed and simplified signal, is here demonstrated to function, using songs with identical parameters to those found in real male cricket song, using an analog electronic model of the peripheral auditory morphology of the female cricket as the sensor. We put the robot under the same experimental conditions as the female crickets, and it responds with phonotaxis to calling songs of real male Gryllus bimaculatus. Further, the robot only responds to songs with syllable rates within a bandwidth similar to the bandwidth found for crickets. By making polar plots of the heading direction of the robot, we obtain behavioral data that can be used in statistical analyses. These analyses show that there are statistically significant differences between the behavioral responses to calling songs with syllable rates within the bandwidth and calling songs with syllable rates outside the bandwidth. This gives the verification that the simple neural control mechanism (together with morphological auditory matched filtering) can account for the syllable rate preference found in female crickets. With our robot system, we can now systematically explore the mechanisms controlling recognition and choice behavior in the female cricket by experimental replication.

Investigating acoustic localization using artificial ears

Physical modeling is a technique wherein sensorimotor mechanisms believed to underlie animal behavior are mimicked using functionally analogous transducers and electromechanical circuitry. Because physical models inhabit the same environment as animals, they allow biologists to examine more realistic environmental interactions. In turn, physical modeling can enable engineers to discover the general principles underlying robust, adaptive sensorimotor control of robots. Two acoustic localization mechanisms are being physically modeled: cricket phonotaxis and echolocation by constant frequency emitting bats. (1) The function of the cricket trachea was modeled by connecting the output of two miniature microphones to a circuit measuring the relative intensity and binaural phase shift of a received call. Using only tracheal phase cancellation and latency comparison, a robot bearing this sensor obtains directional information enabling it to approach only those sounds with the right (frequency and envelope) structure. (2) An artificial echolocation system was built using a continuous, pure-tone-emitting transducer and a pair of receivers mounted on the pan/tilt head of a robot. Directional cues contained in echoes reflected from moving targets—interaural intensity disparities and temporal differences in the echo modulating waveforms—are used to orient the robot toward these targets.

Using robots to model animals: a cricket test

Abstract The sensorimotor problems faced by animals and by robots have much in common, yet identifying this similarity has so far led to very few successful attempts to implement specific biological neural control structures on robots. One major limitation is that understanding of the biological mechanisms is insufficient for straightforward installation. However, using robots as a method of physically modeling animal systems can potentially contribute to our understanding of these mechanisms. This approach is employed in an investigation of phonotaxis (sound-seeking) in crickets. The process of building a robot forms the basis of a critical evaluation of the neuroethological evidence about the cricket, and generates an alternative hypothesis to explain this evidence. The explanatory power of this hypothesis is explored by testing and analyzing the behaviour of the robot that embodies it. The robot behaved like the cricket, competently and robustly finding its way to a specific sound source under a variety of conditions. It is argued that the methodology is more appropriate than symbolic simulation for the kinds of problems raised in the investigation of sensorimotor behaviour in animals and robots.

Changes in the mechanics of the cricket ear during the early days of adult life

From behavioural experiments it is known that the thresholds for both positive and the negative phonotaxis in crickets (Gryllus bimaculatus) decrease during the first days of adult life. Neuronal recordings have shown that a part of the changes in threshold has its origin in the ears. In this study we investigate some changes of the mechanics of the ears in the days after the imaginal moult.

Ontogeny of positive phonotaxis in female crickets, Gryllus bimaculatus De Geer: dynamics of sensitivity, frequency-intensity domain, and selectivity to temporal pattern of the male calling song

1. The ontogeny of positive phono taxis (PPT) in female crickets, Gryllus bimaculatus was followed in tethered flight. During the first day of adult life many females already demonstrated PPT to the calling song (CS) of conspecific males. The average threshold of PPT at 5 kHz, the dominant frequency of the CS, decreased by 30 dB by the time of sexual maturity (Fig. 1). 2. No correlates of this decrease were found in the activity of the most sensitive ascending prothoracic neuron tuned to 5 kHz recorded in the neck connective. This is presumably the AN1 neuron which is known to be involved in PPT realization. Its threshold at 5 kHz in young animals was the same as in adults. Therefore, ascending circuits of PPT seem to be mature by the first day of imago life and there should be some other mechanisms preventing performance of PPT by young walking females until maturation. 3. The PPT of females in flight is tuned to 5 kHz, much sharper than in walking (Fig. 2). In flight, the carrier frequency of a signal is probably an important parameter driving PPT, at least in a no-choice situation, whereas on the substrate, at close range, temporal parameters become decisive. 4. The ontogenetic development of the selectivity of a female's PPT to temporal parameters of a signal passes 3 successive steps: 1) response mainly to the trill with pulse repetition rate as in the CS; 2) response mainly to the actual CS with chirp structure; 3) destruction of selectivity (Figs. 3–6). The existence of steps 1 and 2 strengthens our hypothesis, that in phylogeny, the trill (pulse rate) detector of the CS “recognizer” in the CNS appeared earlier, and was later accompanied by the chirp detector. 5. Joint breeding of female larvae with males accelerates maturation of the CS recognizer.