The effects of injecting Juvenile Hormone III into the prothoracic ganglion on phonotaxis by female crickets Gryllus bimaculatus

Nanoinjection of Juvenile Hormone III (JH III) into the prothoracic ganglion causes virgin female crickets Gryllus bimaculatus De Geer to become more phonotactically selective for the syllable periods (SPs) of model calling songs. Females responding to all, or almost all, of the SPs presented before JH III injection significantly narrow their responses to a range of SPs that is usually centered on the SPs included in the conspecific males' calling song. Control injections of acetone (i.e. the solvent for JH III) into the prothoracic ganglion do not significantly change the recipient females' phonotactic responses. Injection of JH III into the metathoracic ganglion also has no effect the females' phonotactic choices.     

Temperature coupling in cricket acoustic communication

Summary Temperature effects on calling song production and recognition were investigated in the North American field cricket, Gryllus firmus. Temporal parameters of field-recorded G. firmus calling song are strongly affected by temperature. Chirp rate and syllable rate increase, by factors of 4 and 2, respectively, as linear functions of temperature over the range in which these animals sing in the field (12°–30 °C). Temperature affects syllable duration to a lesser extent, and does not influence calling song carrier frequency. Female phonotactic preference, measured on a spherical treadmill in the laboratory, also changes with temperature such that warmer females prefer songs with faster chirp and syllable rates. Best phonotaxis, measured as accuracy of orientation to the sound source, and highest walking velocity, occur in response to temperature-matched songs at 15°, 21°, and 30 °C. Experiments under semi-natural conditions in an outdoor arena revealed that females perform phonotaxis at temperatures as low as 13 °C. Taken together, the song and phonotaxis data demonstrate that this communication system is temperature coupled. A strategy is outlined by which temperature coupling may be exploited to test hypotheses about the organization of neural networks subserving song recognition.Abbreviations CP chirp period - SP syllable period - SD syllable duration     

Plasticity of the phonotactic selectiveness of four species of chirping crickets (Gryllidae): Implications for call recognition

Earlier studies of phonotaxis by female crickets describe this selective behavioural response as being important in the females' choices of conspecific males, leading to reproduction. In the present study, moderate (30+) to very large data sets of phonotactic behaviour by female Acheta domesticus L., Gryllus bimaculatus DeGeer, Gryllus pennsylvanicus Burmeister and Gryllus veletis Alexander demonstrate substantially greater plasticity in the behavioural choices, as made by females of each species, for the syllable periods (SP) of model calling songs (CS) than has been previously described. Phonotactic choices by each species range from the very selective (i.e. responding to only one or two SPs) to very unselective (i.e. responding to all SPs presented). Some females that do not respond to all SPs prefer a range that includes either the longest or shortest SP tested, which fall outside the range of SPs produced by conspecific males. Old female A. domesticus and G. pennsylvanicus are more likely to be unselective for SPs than are young females. Each species includes females that do not respond to a particular SP when responding to CSs with longer and shorter SPs. The results suggest that the plasticity of phonotactic behaviour collectively exhibited by the females of each species does not ensure that choices of a male's CS effectively focus the female's phonotactic responses on CSs that represent the conspecific male. The phonotactic behaviour collectively exhibited by females of each species does not readily fit any of the models for selective processing by central auditory neurones that have been proposed to underlie phonotactic choice.     

Filtering of temporal parameters of the calling song by cricket females of two closely related species: a behavioral analysis

The phonotactic response of cricket females was investigated on a locomotion compensator to determine the temporal parameters of the male's calling song which are important for species recognition. Two sympatric species (Teleogryllus commodus, T. oceanicus) that show different syllable periods in the chirp and trill parts of their calling songs were used. By their responses T. commodus females exhibited two temporal filters for syllable periods, which were tuned to the species-specific syllable periods occurring during chirp and trill. For song recognition both filters had to be activated and for both a minimum number of three to five consecutive syllable periods was necessary. In contrast, T. oceanicus females showed only one sharply tuned filter corresponding to the chirp part of the male's calling song. This filter was sufficient for calling song recognition. Syllable periods of the trill part also influenced calling song recognition, but these played only a minor role. Carrier frequency was also important for positive phonotaxis. Calling song recognition by T. commodus females is largely based on central nervous processing, while for T. oceanicus both peripheral frequency filtering and central temporal filtering is important. Accepted: 17 January 1997     

The L3 neuron and an associated prothoracic network are involved in calling song recognition by female crickets

In young virginAcheta domesticus females, the spiking response of the prothoracic L3 auditory interneuron discriminates between calling songs (CSs) with phonotactically attractive and unattractive syllable periods (SPs), which parallels phonotactic discrimination. Presentation of a CS with an originally attractive SP, but with the intensity modulated so as to minimize L3's selective response, results in a CS with little phonotactic attractiveness. Conversely, a CS with an originally unattractive SP becomes much more attractive when the CS is intensity modulated in ways that duplicate L3's selective response. L3's discriminatory response to CS SP deteriorates with age, in parallel with decreased phonotactic selectiveness (females, older than 14 days, typically are unselective for CS SPs). SP-selective processing, which was not apparent in these old L3s, is immediately restored by removing the contralateral ear. SP-specific information is resident in a network of neurons within the prothoracic ganglion that results in the SP selective responses of the L3 neuron in young females. Changes in the SP-selective responses of the L3 neuron are highly correlated with corresponding changes in the female's phonotactically selective behavior.     

Prolonged response to calling songs by the L3 auditory interneuron in female crickets (Acheta domesticus): possible roles in regulating phonotactic threshold and selectiveness for call carrier frequency

L3, an auditory interneuron in the prothoracic ganglion of female crickets (Acheta domesticus) exhibited two kinds of responses to models of the male's calling song (CS): a previously described, phasically encoded immediate response; a more tonically encoded prolonged response. The onset of the prolonged response required 3-8 sec of stimulation to reach its maximum spiking rate and 6-20 sec to decay once the calling song ceased. It did not encode the syllables of the chirp. The prolonged response was sharply selective for the 4-5 kHz carrier frequency of the male's calling songs and its threshold tuning matched the threshold tuning of phonotaxis, while the immediate response of the same neuron was broadly tuned to a wide range of carrier frequencies. The thresholds for the prolonged response covaried with the changing phonotactic thresholds of 2- and 5-day-old females. Treatment of females with juvenile hormone reduced the thresholds for both phonotaxis and the prolonged response by equivalent amounts. Of the 3 types of responses to CSs provided by the ascending L1 and L3 auditory interneurons, the threshold for L3's prolonged response, on average, best matched the same females phonotactic threshold. The prolonged response was stimulated by inputs from both ears while L3's immediate response was driven only from its axon-ipsilateral ear. The prolonged response was not selective for either the CS's syllable period or chirp rate.     

Nanoinjection of neurotransmitters into the prothoracic ganglion of female cricket Acheta domesticus changes phonotactic selectivity

The phonotactic response by female crickets is influenced by Juvenile Hormone III, which affects selectivity to the syllable period of the calling song. This pathway is influenced by an inhibitory input in the prothoracic ganglion, possibly chloride-mediated inhibition. In order to identify potential neurotransmitters involved in such pathway, we performed nanoinjection of five neurotransmitters into the prothoracic ganglion of virgin female Acheta domesticus. Phonotaxis for these females was evaluated before and after injections. All five neurotransmitters that were nanoinjected are known to bind to chloride channels. Nanoinjection of histamine significantly decreased phonotactic selectivity to the syllable period of the calling song while glycine, gamma aminobutyric acid, serotonin and saline controls did not. Octopamine significantly decreased phonotactic responses overall. The effect of histamine was tested further by nanoinjecting the antihistamine pyrilamine into the prothoracic ganglion of older unselected females, which resulted in increased phonotactic selectivity.     

Responses and song pattern copying of Omega-type I-neurons in the cricket,Gryllus bimaculatus,at different prothoracic temperatures

Summary Omega-type I-neurons (ON/1) (Fig. 1A) were recorded intracellularly with the prothoracic ganglion kept at temperatures of either 8–9°, or 20–22° or 30–33 °C and the forelegs with the tympanal organs kept at ambient temperature (20–22 °C). The neurons were stimulated with synthetic calling songs (5 kHz carrier frequency) with syllable periods (SP in ms) varying between 20 and 100, presented at sound intensities between 40 and 80 dB SPL. The amplitude and duration of spikes as well as response latency decreased at higher temperatures (Figs. 1 B, 2, 6). At lower prothoracic temperatures (8–9 °C) the neuron's responses to songs with short SP (20 ms) failed to copy single syllables, or with moderate SP (40 ms) copied the syllable with low signal to noise ratio (Fig. 3). The auditory threshold of the ON/1 type neuron, when tested with the song model, was temperature-dependent. At 9° and 20 °C it was between 40 and 50 dB SPL and at 33 °C it was less than 40 dB SPL (Fig. 4). For each SP, the slope of the intensity-response function was positively correlated with temperature, however, at low prothoracic temperatures the slope was lower for songs with shorter SPs (Fig. 5). The poor copying of the syllabic structure of the songs with short SPs at low prothoracic temperatures finds a behavioral correlate because females when tested for phonotaxis on a walking compensator responded best to songs with longer SPs at a similar temperature.Abbreviations epsps excitatory postsynaptic potentials - ON/1 omega-type I-neuron - SP syllable period - SPL sound pressure level     

Responses to features of the calling song by ascending auditory interneurones in the cricket Gryllus campestris

ABSTRACT. In female Gryllus campestris L., three functional types of ascending auditory intemeurones have been studied by recording from them extracellularly in the split cervical connectives using suction electrodes. Type 1 neurones are characterized by an optimal sensitivity to the carrier frequency of the species calling song (4–5 kHz). They copy the syllable and pause structure of the call at all intensities. The patterned spike discharge is observable at least 8 dB above absolute threshold. With suprathreshold stimulation, the neurones exhibit maximal responses (number of spikes/chirp) around the carrier frequency. The intensity response curves are approximately linear in the range of 40–90 dB SPL. The envelope of each syllable is reflected by a corresponding change in the firing rate, and syllable periods of 24ms and longer are resolved. This type can be considered as a neural correlate for phonotactic behaviour of the female where the syllable period has been found to be the most important temporal parameter. Type 2 neurones are most sensitive in the range of 4–6 and 11–13 kHz. They copy the syllable and pause structure of the species calling song at low and moderate intensities. However, the spikes invade the intersyllable pauses, when stimulated with the calling song at higher intensities (above 85 dB). This is particularly apparent at the onset of a chirp series. The slope of the intensity—response curve mimics that of type 1 units. The neurones cannot follow syllable periods shorter than 32 ms. Type 3 neurones differ from types 1 and 2 by a rather broad-band sensitivity in the range of 3–16 kHz, and in copying the chirp as a whole. Even at low stimulus intensities, the intersyllable pauses are filled with spikes, and information about the syllable—pause structure is lost. Stimulation with suprathreshold intensities gives rise to a rather uniform, broad-band response without distinctive peaks. The intensity—response curve is characterized by a higher absolute threshold, and by the reduction in the response magnitude starting above 70–80 dB. These units are not suitable for copying the calling song temporal structure in detail, but would indicate the chirping rhythm. Their strong response in the range of the species courtship song carrier frequency make them suitable to copy the courtship song.     

Phonotactic Behavior of Male Field Crickets (Gryllus texensis) in Response to Acoustic Calls From Conspecific Males

We studied male phonotactic behaviors elicited by acoustic cues that simulate conspecific male songs in the field cricket, Gryllus texensis. Males exhibited significant positive phonotaxis in response to the simulated song stimuli, but showed no such response to atypical song stimuli. We found no significant relationship between males’ own calling behavior and their phonotactic responses to the stimuli. Analyses indicated that larger males exhibited greater phonotactic responses, which may indicate a greater tendency to engage in aggressive interactions if size is an indicator of fighting ability. Male phonotactic responses were significantly weaker than those exhibited by females, and adult males did not exhibit stronger responses with increasing age as has been documented for females. Observed sex differences in the strengths of phonotactic responses may reflect differences in the fitness-payoffs of responding. That is, females are under strong selection pressure to respond to male songs and subsequently mate. In contrast, males responding to acoustic signals from other males need not precisely locate the signaler but would likely move to areas where females are likely to be found. Alternatively, males might benefit from avoiding areas with calling males and establishing their own calling stations away from competing males.     

The effect of visual input on calling song attractiveness for female Acheta domesticus

ABSTRACT. Of twelve mature phonotactically-responsive female Acheta domesticus L., ten responded phonotactically to a wider range (30 or SO to 100 ms) of model calling song (CS) syllable periods (SP) on the Kramer treadmill in the dark than in a lighted visually structured arena (50–70 ms). When given a choice between the visually attractive target and the invisible loudspeaker, seven of the ten females that tracked a visually attractive target (black square) when presented alone in the light reduced the range of SPs they tracked phonotactically to 50–70 ms. Three of the ten females that were not strongly attracted to the visual target when presented alone, continued to respond to model calling songs with a wide range of SPs (30–100 ms) when given a choice between visual and acoustical targets under the same conditions. Two of the twelve females responded only to model calling songs with a 50–70 ms SP on the Kramer treadmill in the dark. These females did not change their choice for model calling song SPs when presented with the visually attractive target.     

Calling song and selective phonotaxis in the field crickets,Gryllus firmus andG. pennsylvanicus (Orthoptera: Gryllidae)

The field cricket species, Gryllus firmusand G. pennsylvanicus,occur in a mosaic hybrid zone that roughly parallels the eastern slope of the Appalachian mountains in the northeastern United States. It is important to know what role, if any, the calling song plays in mate choice in sympatric and allopatric populations. In this report, we present results on the variability of calling song properties along transects across this hybrid zone. We also present the results of experiments on phonotactic selectivity of females from an allopatric population of G. firmus.The male calling song of allopatric G. firmuswas significantly slower in temporal rhythm (i. e., chirp and pulse repetition rates) and lower in pitch (i.e., dominant frequency) than that of allopatric G. pennsylvanicus.Calling song properties of males recorded in the hybrid zone varied considerably in temporal and spectral properties. In two-stimulus (choice) phonotaxis experiments, allopatric females of G. firmuspreferred synthetic calling songs with conspecific pulse repetition rates over songs that had lower and higher pulse rates. This preference persisted even when the sound pressure levels of alternative stimuli were unequal. Therefore, allopatric females of G. firmuscan discriminate between conspecific and heterospecific calling songs. Whether or not this same selectivity is present in sympatric populations remains unclear. Investigations of phonotactic selectivity in other allopatric and sympatric populations of both species are currently under way.     

Separate localization of sound recognizing and sound producing neural mechanisms in a grasshopper

Summary In the two acridid speciesChorthippus parallelus andCh. montanus, the sound template by which females recognize male song varies with temperature, as does the song itself. At relatively high temperatures the females respond best to simulated songs with high syllable frequencies, and at lower temperatures songs with lower syllable frequencies are preferred.The temperature around the supraesophageal and metathoracic ganglia of female grasshoppers was monitored by implanted thermocouples, and either the head or the thorax was warmed selectively while the animal was free to move (within the imits of the wires). Then simulations of the conspecific song varying in syllable frequency corresponding to different song temperatures were presented, and the stridulatory responses of the animals were observed.The results were as follows. 1. Song recognition (in particular, the position of the peak of the response curve) depended on the temperature of the head. 2. The rate of stridulatory hindleg movement was determined by the temperature of the thoracic ganglia.This result provides strong evidence against the genetic coupling hypothesis.     

Processing of Song Signals in the Cricket and its Hormonal Control

SYNOPSIS. Phonotaxis by female crickets to the calling songof males, is an important model for investigating the neuralbasis of auditory behavior. Recent advances make it possibleto explain some components of this behavior and its hormonalcontrol, at the level of identified neurons and molecular expressionwithin those neurons Tonotopically arranged afferents from the cricket's ear, projectto local and intersegmental prothoracic interneurons. Bilateralprocessing of signals and some temporal-pattern specific processingoccurs in the prothoracic ganglion and influences acoustic informationthat is sent to the brain via ascending interneurons that aredemonstrably involved in phonotaxis. High, low and band- passinterneurons in the brain continue temporal pattern processingwhich matches the selectivity of phonotaxis and may be filtersfor recognition of the calling song. Neurons descending fromthe brain and prothoracic ganglion, direct multimodal signals(including auditory) to more posterior regions, possibly theleg motor neurons that are responsible for phonotaxis Age-related changes or artificially induced changes in JuvenileHormone III levels regulate the threshold for phonotaxis inAcheta domesticus, by varying the threshold of LI, a prothoracicascending interneuron that is necessary for phonotaxis to lowintensity calling songs. Results from in situ hybridizationsuggest that this might be accomplished, in part, by controllingthe levels of nicotinic acetylcholine receptor-like mRNA expressedin LI, presumably by increasing its neurotransmitter receptordensity. L3 is a prothoracic ascending interneuron that exhibitsbandselective response properties to the syllable period ofthe calling song. L3's response is age and JHIII related, andis correlated to phonotactic selectivity. These changes in L3might be accomplished, at least in part by JHIII regulatingthe expression of nicotinic acetylcholine receptor-like mRNAin L3     

Female Acheta domesticus track acoustical and visual targets with different walking modes

ABSTRACT. Female Acheta domesticus L. were tested for tracking model calling songs with different syllable periods on the Kramer treadmill in the dark, under homogenous light, and in the presence of a visually attractive target (black square) positioned either perpendicular to or in front of the invisible acoustical target. The females exhibited tracking of the two targets by different walking modes.     

Matched Counter-singing Signals Escalation of Aggression in Black-capped Chickadees (Parus atricapillus)

Black-capped chickadees (Parus atricapillus) have the ability to shift their songs up and down over a wide range of absolute frequencies. Males can shift their songs over 465 ± 52.9 (SE) Hz. During the dawn chorus, males shift their songs by 80 Hz or more every 41 ± 8.8 (SE) songs, but it appears that males can sing at any frequency within their range. Frequency shifting may allow males to match counter-sing with rival males; that is, to switch song output to match that of a rival. During simultaneously recorded dawn choruses, however, there was no correlation over time in the frequency of neighbouring males' songs, nor was there a correlation over time in the size of shifts between their songs. Moreover, males did not match the frequencies of songs presented on a played-back tape at the edge of their territories during the dawn chorus. Matching was observed during some bouts of counter-singing between males. In these cases, matched counter-singing was highly associated with escalation of the conflict. We suggest that frequency matching in this species may be a graded signal that allows the singer to direct aggression towards a particular rival.     

The influence of auditory and visual experience on the phonotactic behavior of the cricket,Gryllus bimaculatus

Female crickets lacking experience with phonotaxis to conspecific calling song respond to trains of continuously repeated sound pulses (trill), whereas experienced females do not. In the present study such inexperienced crickets were tested for their responsiveness to trills of pulse repetition periods from 30 to 70 ms on a Y- shaped maze. Stimulation with a repetition period of 30 ms led to unexpectedly low phonotactic and exploratory activity. Initial stimulation with trills of 30- ms repetition period drastically reduced the responsiveness of inexperienced animals to conspecific calling song and other attractive stimuli. Effects of visual stimulation on the phonotactic behavior of female crickets are demonstrated. Threatening visual stimuli changed the behavior of experienced animals to a state that resembles that of inexperienced animals. The relevance of these observations is discussed with respect to the development of the auditory pattern recognition mechanism in crickets.     

Auditory pattern recognition and steering in the cricket Teleogryllus oceanicus

Male crickets Teleogryllus oceanicus (Le Guillou) produce a complex species‐specific calling song with phrases combining groups of single pulses (chirps) and groups of double‐pulses (trills) to attract females, which fly or walk towards singing males. In open‐loop trackball experiments, phonotactic steering responses to normal calling song phrases consisting of chirps and trills are strongest, suggesting that both components are necessary for maximal attractiveness. Sequences of just chirps or trills are less effective in eliciting phonotactic walking and steering. Split‐song paradigms are used to analyze the steering behaviour underlying orientation in more detail. The females' phonotactic steering reflects the alternating acoustic pattern of the split‐song paradigm. Analysis with high temporal resolution demonstrate, that even when the calling song is presented only from one side, the steering velocity and lateral deviation towards the song is modulated by steering events to single‐sound pulses. Therefore, pattern recognition, which integrates the structure of the song, appears not to be directly involved in the rapid steering response. This organization of phonotactic behaviour with a parallel processing of pattern recognition and steering is similar to other cricket species and may allow T. oceanicus females to steer transiently towards distorted song patterns as they occur in natural habitats.     

Temperature Effects on the Temporal Properties of Calling Songs in the Crickets <Emphasis Type="Italic">Gryllus fultoni</Emphasis> and <Emphasis Type="Italic">G. vernalis</Emphasis>: Implications for Reproductive Isolation in Sympatric Populations

Two closely related wood-cricket species, Gryllus fultoni (Orthoptera: Gryllidae) and G. vernalis, produce similar calling songs, consisting of 3-pulse chirps. Analysis of field and laboratory recordings of calling songs showed that, after correction to a common temperature, there was a divergence in chirp and pulse rates between far allopatric populations of G. fultoni and populations sympatric with G. vernalis. To determine whether the divergence in calling songs potentially provides reproductive isolation between G. fultoni and G. vernalis throughout the temperature range over which these insects sing, we recorded calling songs of lab-reared G. fultoni and G. vernalis populations between 18 and 28°C. Mean chirp rate significantly differed between sympatric and far allopatric G. fultoni populations as well as between sympatric G. fultoni and G. vernalis populations. Although there was a significant difference in mean pulse rate between sympatric G. fultoni and G. vernalis populations, pulse rate did not differ between sympatric and far allopatric G. fultoni populations in the laboratory study. Considering the magnitudes of differences in calling song characters discriminated by females of G. fultoni and the mean differences and the variability in calling song characters between the two species, the joint difference in chirp and pulse rates may be adequate for species discrimination over most of the range at which these crickets breed.     

The development of stimulus‐specific auditory responses requires song exposure in male but not female zebra finches

Juvenile male zebra finches develop their song by imitation. Females do not sing but are attracted to males' songs. With functional magnetic resonance imaging and event‐related potentials we tested how early auditory experience shapes responses in the auditory forebrain of the adult bird. Adult male birds kept in isolation over the sensitive period for song learning showed no consistency in auditory responses to conspecific songs, calls, and syllables. Thirty seconds of song playback each day over development, which is sufficient to induce song imitation, was also sufficient to shape stimulus‐specific responses. Strikingly, adult females kept in isolation over development showed responses similar to those of males that were exposed to songs. We suggest that early auditory experience with songs may be required to tune perception toward conspecific songs in males, whereas in females song selectivity develops even without prior exposure to song. © 2009 Wiley Periodicals, Inc. Develop Neurobiol 2010