Diversity of intersegmental auditory neurons in a bush cricket

Various auditory interneurons of the duetting bush cricket Ancistrura nigrovittata with axons ascending to the brain are presented. In this species, more intersegmental sound-activated neurons have been identified than in any other bush cricket so far, among them a new type of ascending neuron with posterior soma in the prothoracic ganglion (AN4). These interneurons show not only morphological differences in the prothoracic ganglion and the brain, but also respond differently to carrier frequencies, intensity and direction. As a set of neurons, they show graded differences for all of these parameters. A response type not described among intersegmental neurons of crickets and other bush crickets so far is found in the AN3 neuron with a tonic response, broad frequency tuning and little directional dependence. All neurons, with the exception of AN3, respond in a relatively similar manner to the temporal patterns of the male song: phasically to high syllable repetitions and rhythmically to low syllable repetitions. The strongest coupling to the temporal pattern is found in TN1. In contrast to behavior the neuronal responses depend little on syllable duration. AN4, AN5 and TN1 respond well to the female song. AN4 (at higher intensities) and TN1 respond well to a complete duet.     

Fast and reliable decisions for a dynamic song parameter in field crickets

We investigated the choice of female crickets for a dynamic song parameter (chirp rate) on a walking compensator, and the underlying neuronal basis for the choice in the form of discharge differences in the pair of AN1-neurons driving the phonotactic steering behaviour. Our analysis reveals that decisions about chirp rate in a choice situation are made fast and reliably by female crickets. They steered towards the higher chirp rate after a delay of only 2.2–6 s, depending on the rate difference between the song alternatives. In this time period, the female experienced only one to two additional chirps in the song model with the higher rate. There was a strong correlation between the accumulated AN1 discharge difference and the amount of steering towards the side with the stronger response.     

Hyperacute directional hearing and phonotactic steering in the cricket (Gryllus bimaculatus deGeer)

Background

Auditory 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 Findings

Here 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.

Conclusions

Our 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.     

Modeling and measuring lateral line excitation patterns to changing dipole source locations

In order to determine excitation patterns to the lateral line system from a nearby 50 Hz oscillating sphere, dipole flow field equations were used to model the spatial distribution of pressures along a linear array of lateral line canal pores. Modeled predictions were then compared to pressure distributions measured for the same dipole source with a miniature hydrophone placed in a small test tank used for neurophysiological experiments. Finally, neural responses from posterior lateral line nerve fibers in the goldfish were measured in the test tank to demonstrate that modeled and measured pressure gradient patterns were encoded by the lateral line periphery. Response patterns to a 50 Hz dipole source that slowly changed location along the length of the fish included (1) peaks and valleys in spike-rate responses corresponding to changes in pressure gradient amplitudes, (2) 180° phase-shifts corresponding to reversals in the direction of the pressure gradient and (3) distance-dependent changes in the locations of peaks, valleys and 180° phase-shifts. Modeled pressure gradient patterns also predict that the number of neural amplitude peaks and phase transitions will vary as a function of neuromast orientation and axis of source oscillation. The faithful way in which the lateral line periphery encodes pressure gradient patterns has implications for how source location and distance might be encoded by excitation patterns in the CNS. Phase-shift information may be important for (1) inhibitory/excitatory sculpting of receptive fields and (2) unambiguously encoding source distance so that increases in source distance are not confused with decreases in source amplitude.     

Vibratory interneurons in the non-hearing cave cricket indicate evolutionary origin of sound processing elements in Ensifera

Tympanal hearing organs in the front tibiae of ensiferan insects supposedly evolved from vibration-sensitive tibial organs (TO), like those in the cave cricket Troglophilus neglectus (Rhaphidophoridae). If this is true, one expects to find interneurons in the cave cricket that are homologous to auditory neurons from hearing Ensifera. Therefore, we examined the central projections of the foreleg TO of the cave cricket, as well as morphology and response properties of interneurons responding to foreleg vibration. Sensory axons of the TO adjoined to the "tympanal nerve" terminate in the equivalent portion of the ring tract neuropile in the prothoracic ganglion as corresponding receptors of crickets and weta. We found nine putatively homologous elements to sound- and/or vibration-sensitive interneurons of Ensifera--one local neuron (unpaired median, DUM), three T-fibres (TN), three descending (DN) and two ascending neurons (AN). Presumable first-order interneurons arborising in the ring tract correspond to a local auditory DUM cell of bush crickets and to TN1, DN1 and AN2 of various Ensifera, respectively. Homologues of some prominent auditory cells, the "omega" neuron(s) and the ascending neuron 1 (AN1), however, were not found. We conclude that (a) T. neglectus interneurons are morphologically primitive with respect to those of hearing taxa, (b) significant changes in the dendritic structure/synaptic connectivity have taken place during the evolution of the most specialised first-order auditory interneurons of Ensifera, (c) the data do not contradict independent evolution of hearing in Grylloidea and Tettigonoidea. Other interneurons appear morpho-physiologically conserved across hearing and non-hearing species, possibly as a part of a multimodal "alert" system.     

Selective processing of calling songs by auditory interneurons in the female cricket, Gryllus pennsylvanicus: possible roles in behavior

Female crickets (Gryllus pennsylvanicus), caught in the field as nymphs, responded as adults in the laboratory with selective phonotaxis to model calling songs (CSs) that reproduced the dominant carrier frequencies and syllable periods (SPs) characteristic of the male's natural calling song. Extracellular recordings demonstrated two types of auditory interneurons in the female's cervical connectives that were very similar to the AN1 and AN2 neurons previously described in other gryllid species. The AN2 neuron responded to model CSs with a phasically encoded immediate response, and a more tonically encoded prolonged response. AN2's immediate response exhibited SP-dependent decreases (termed decrement) in its responses to sequential syllables of the CS that were greatest to CSs with the shortest SPs and diminished as SPs were lengthened, resulting in an SP-dependent habituation. Picrotoxin application transformed this SP-dependent habituation by AN2 to SP-selective responses in which the degree of decrement was greatest to SPs that were most phonotactically attractive. AN2's prolonged response was most sensitive to 5 kHz CSs and correlated with the carrier frequency tuning for the thresholds of phonotaxis by females. Thus, in females, AN2's immediate (in the presence of picrotoxin) and prolonged responses were selectively tuned to the SPs and carrier frequencies of the male's calls that were most attractive behaviorally. AN1's responses at threshold were also tuned to the dominant carrier frequencies of the male's CS.     

Acoustic pattern recognition and orientation in orthopteran insects: parallel or serial processing?

In grasshoppers the acoustic information for pattern recognition and directional analysis is processed via parallel channels and not serially. This can be concluded from the following results established by behavioural experiments:

1. For pattern recognition the inputs from both sides are added internally. This implies that directional information is lost on this channel and must be processed in parallel.
2. The location of a female song can be influenced by introducing short clicks from both sides, forcing the grasshopper to turn to the louder resp. leading side. Also, when given a choice between two patterns of different efficiency, the grasshoppers turned towards the side with the stronger directional cues and not to the side with the more efficient pattern.
3. The parallel processing of acoustic information in grasshoppers corresponds to the evolution of acoustic communication in Acridids, as song evolved only when the ability of hearing and localization was already present. This is in contrast to crickets where the close evolutionary coupling of singing and hearing in the context of mate finding possibly favoured a serial processing of song recognition and localization.

     

Neural representations of the axis of acoustic particle motion in nucleus centralis of the torus semicircularis of the goldfish, <Emphasis Type="Italic">Carassius auratus</Emphasis>

Experiments examined differential coding of acoustic particle motion axis in the auditory midbrain of goldfish. Animals were exposed to vibratory stimuli varying in axis orientation as action potentials were recorded from single units in the central neuropil of nucleus centralis in the torus semicircularis. Response magnitudes as a function of stimulation axis were visualized in three dimensional plots called directional response profiles. These are generally comparable to directional responses observed among primary saccular afferents in having substantially vertical orientations. Distortions in shape from the peripheral patterns indicate neural information processing. A three-dimensional model was used to evaluate the hypothesis that responses in the auditory midbrain reflect the convergence of excitatory and inhibitory primary afferent-like responses. Model afferent inputs were generated and combined arithmetically. This analysis gives insight into the mechanisms of information processing that appear to occur in brainstem nuclei. The lack of diversity in best axis directions suggests that this mechanism alone cannot account for directional hearing abilities in this species. The roles that this directional representation and processing may play in directional hearing and sound source localization are not yet clear. Implications of these data on current models of fish directional hearing are discussed.     

Efficient inhibition of bursts by bursts in the auditory system of crickets

In crickets, auditory information about ultrasound is carried bilaterally to the brain by the AN2 neurons. The ON1 neuron provides contralateral inhibitory input to AN2, thereby enhancing bilateral contrast between the left and right AN2s, an important cue for sound localization. We examine how the structures of the spike trains of these neurons affect this inhibitory interaction. As previously shown for AN2, ON1 responds to salient peaks in stimulus amplitude with bursts of spikes. Spike bursts, but not isolated spikes, reliably signal the occurrence of specific features of the stimulus. ON1 and AN2 burst at similar times relative to the amplitude envelope of the stimulus, and bursts are more tightly time-locked to stimulus feature than the isolated spikes. As a consequence, spikes that, in the absence of contralateral inhibition, would occur within AN2 bursts are more likely to be preceded by spikes in ON1 (mainly also in bursts) than are isolated AN2 spikes. This leads to a large decrease in the burst rate of the inhibited AN2. We conclude that the match in coding properties of ON1 and AN2 allows contralateral inhibition to be most efficient for those portions of the response that carry the behaviourally relevant information, i.e. for bursts. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Frequency and temporal pattern-dependent phonotaxis of crickets (Teleogryllus oceanicus) during tethered flight and compensated walking

Summary Phonotactic responses ofTeleogryllus oceanicus were studied with two methods. Tethered crickets were stimulated with sound while they performed stationary flight, and steering responses were indicated by abdominal movements. Walking crickets tracked a sound source while their translational movements were compensated by a spherical treadmill, and their walking direction and velocity were recorded.During both flight and walking, crickets attempted to locomote towards the sound source when a song model with 5 kHz carrier frequency was broadcast (positive phonotactic response) and away from the source when a song model with 33 kHz carrier frequency was used (negative phonotactic response) (Figs. 2, 4).One-eared crickets attempted, while flying, to steer towards the side of the remaining ear when stimulated with the 5 kHz model, and away from that side in response to the 33 kHz model (Fig. 3). While walking, one-eared crickets circled towards and away from the intact side in response to the 5 kHz and 33 kHz models, respectively (Fig. 6).Positive and negative responses differed in their temporal pattern requirements. Phonotactic responses were not elicited when a non-calling song pattern (2 pulses/s) was played with a carrier frequency appropriate for positive phonotactic responses (5 kHz), but this pattern did elicit negative responses with 33 kHz carrier frequency (Figs. 7–10). When an intermediate carrier frequency, 15 kHz, was used, the response type (positive or negative) depended on the stimulus temporal pattern; the calling song pattern elicited primarily positive responses, while the non-calling song pattern elicited negative responses (Figs. 11, 12, 14, 15). A curious phenomenon was often observed in the flight steering responses; while most responses to 15 kHz song pattern were primarily positive, they often had an initial negative component which was supplanted by the positive component of the response after approximately 2–5 s (Figs. 11, 12).In recent experiments onGryllus campestris, Thorson et al. (1982) described frequency-dependent errors in phonotactic direction (anomalous phonotaxis) and showed how such errors might arise from the frequency-dependent directional properties of the cricket's auditory apparatus. Our findings, particularly the dependence of response type on temporal pattern when 15 kHz carrier frequency was used, argue that frequency-dependent directional properties alone cannot account for positive and negative phonotaxis inT. oceanicus. Rather, these represent qualitatively different attempts to locomote towards and away from the sound source, respectively.We discuss the possibility that central integration of these opposing tendencies might contribute to anomalous phonotaxis.     

Neurophysiological Aspects of Song Pattern Recognition and Sound Localization in Grasshoppers

SYNOPSIS. In their intraspecific communication females of thegrasshopper Chorthippus biguttulus are able to detect minutegaps in songs. Males of this species can lateralize sound withless than 1 dB difference between the two ears. Behavioral experimentssuggested that separate pathways exist for song recognitionand sound localization. As for the neurophysiological basis,auditory receptors respond tonically and necessarily carry allinformation explaining behavioral performances in their spikingresponses. However, for pattern recognition as well as for codingof directional information, it seems necessary for the animalto evaluate a whole set of parallel receptor fibres to achievethe precision observed in behavior. The information of receptorsconverges onto thoracic neurons which drive neurons ascendingto the brain. Some of these ascending neurons exhibit dramaticresponse differences either for various temporal patterns orfor sound from different directions and therefore may representpathways specialized for song recognition or for sound localization.     

硕螽(Deracantha onos)听觉中间神经元的方向灵敏度

本文报道了利用神经生理学方法研究硕螽听觉中间神经元方向灵敏度的结果.     

Sound localization in intact and one-eared crickets

Summary Intact and one-eared crickets,Gryllus bimaculatus, were tested for phonotactic behavior in a closed-loop and an open-loop situation and for related physiological characteristics of an identified auditory neuron pair, the left and the right AN2.Intact animals that performed phonotaxis in the closed-loop condition showed intended turning tendencies in the open-loop condition that correlated with the directional characteristics of their AN2s (Figs. 1–3).Animals in which one foreleg had been amputated during postembryonic development (one-eared regenerates) were classified according to their phonotactic performance as tracking or unoriented animals. The ability of one-eared regenerates to track a sound source was closely correlated with the direction of turning tendencies in the open-loop behavior and to specific features of their AN2 pair (Figs. 4–6).Some animals with one foreleg amputated as adults (one-eared amputees) perform stable phonotactic walking. Their open-loop behavior, however, is different from that of the tracking one- eared regenerates (Fig. 7).One-eared amputees showed stable phonotactic walking when calling song was presented from above and the sound intensity was varied according to the actual walking angle of the animal. The only orientational cue under this condition is the difference of sound intensity at different walking directions (Figs. 8–11).Different mechanisms are discussed for sound localization in one-eared regenerates and one- eared amputees based on turning tendencies which depend on the instantaneous stimulus intensity or on the intensity change between successive stimuli.     

A multi-step directional generalized gradient vector flow snake for target tumor segmentation in US-guided high-intensity focused ultrasound ablation

Getting precise locations of target tumors can help to ensure ablation of cancerous tissues and avoid unwanted destruction of healthy tissues in high-intensity focused ultrasound (HIFU) treatment system. Because of speckle noise and spurious boundaries in ultrasound images, traditional image segmentation methods are not suitable for achieving the precise locations of target tumors in HIFU ablation. In this paper, a multi-step directional generalized gradient vector flow snake model is introduced for target tumor segmentation. In the first step, the traditional generalized gradient vector flow (GGVF) snake is used to obtain an approximate contour of the tumor. According to the approximate contour, a new distance map is generated. Subsequently, a new directional edge map is created by calculating a scalar product of the gradients of the distance map and the initial image. In this process, the gradient directional information and the magnitude information of the distance map are used to attenuate unwanted edges and highlight the real edges in the new directional edge map. Finally, a refined GGVF field is derived from a diffusion operation of the gradient vectors of the directional edge map. The GGVF field is used to refine the tumor's contour, by directing the approximate contour to edges with the desired gradient directionality. Based on the newly developed snake model, the influences of the spurious boundaries and the speckle noise are significantly reduced in the ultrasound image segmentation. Experimental results indicate that this technique is greatly useful for target tumor segmentation in HIFU treatment system     

RECENT BIO ACOUSTIC PUBLICATIONS (mainly 1993)

ABSTRACT

Although much research has been done to describe the degradation of sound signals propagating in natural habitats, the directional cues of sound have so far been neglected. This paper describes a first approach to quantifying the degradation of directional cues in sound propagating parallel to the ground in a grassland habitat of orthopteran insects. A matched pair of probe microphones measured the sound amplitude and phase close to the ears of grasshopper carcasses for 12 evenly spaced directions of sound incidence. The degradation was found to increase with frequency and distance from the sound source and to decrease with distance from the ground. The acoustical data were used to predict how well animals with different auditory systems can determine the direction of the sender. At one position in the habitat, the predictions were compared with the pattern of phonotactic responses of live grasshoppers. Amplitude cues appear to degrade much faster with distance than phase cues. Animals exploiting phase cues may therefore maintain a reasonable directional hearing when the amplitude cues no longer make sense. The pressure-difference-receiver type of ears responds to phase differences, and these ears may be particularly suited to overcoming the degradation of directional cues. This suggests that the possession of such ears may be an adaptation not only to small body size (relative to wavelength), but also to the acoustic properties of the habitat.     

Representation of moving stimuli by somatosensory neurons.

The findings obtained in neurophysiological and psychophysical investigations using tactile stimuli that move at constant velocity across the skin are reviewed. For certain neurons in the postcentral gyrus of the cerebral cortex (S-I) of macaque monkeys, direction of stimulus motion is a "trigger feature" i.e., moving tactile stimuli evoke vigorous discharge activity in these neurons only if the stimuli are moved in a particular direction across the receptive field. This directional selectivity is maximal when stimulus velocity is between 5 and 50 cm/sec, and falls off rapidly at lower or higher velocities. The capacity for human subjects to correctly identify the direction of stimulus motion on the skin exhibits a similar dependence on stimulus velocity. The similar effects of velocity on neural and psychophysical measures of directional sensitivity support the idea that direction of stimulus motion on the skin can only be recognized if the moving stimulus optimally activates the group of S-I neurons for which that directions of simulus motion is the trigger feature.     

Out of phase: relevance of the medial septum for directional hearing and phonotaxis in the natural habitat of field crickets

A modified tracheal system is the anatomical basis for a pressure difference receiver in field crickets, where sound has access to the inner and outer side of the tympanum of the ear in the forelegs. A thin septum in the midline of a connecting trachea coupling both ears is regarded to be important in producing frequency-dependent interaural intensity differences (IIDs) for sound localization. However, the fundamental role of the septum in directional hearing has recently been challenged by the finding that the localization ability is ensured even with a perforated septum, at least under controlled laboratory conditions. Here, we investigated the influence of the medial septum on phonotaxis of female Gryllus bimaculatus under natural conditions. Surprisingly, even with a perforated septum, females reliably tracked a male calling song in the field. Although reduced by 5.2 dB, IIDs still averaged at 7.9 dB and provided a reliable proximate basis for the observed behavioural performance of operated females in the field. In contrast, in the closely related species Gryllus campestris the same septum perforation caused a dramatic decline in IIDs over all frequencies tested. We discuss this discrepancy with respect to a difference in the phenotype of their tracheal systems.     

Dissecting the Contribution of Sensory Cues to Directional Responses by Female Crickets in a two-Loudspeaker Paradigm

Sound localization in insects is typically investigated using single loudspeaker paradigms to examine the impact of sensory cues. Here, the contribution of specific cues to turning responses in a two-loudspeaker paradigm equivalent to a choice situation was examined. For that, several sensory cues were systematically varied to determine their respective contribution to the strength of the turning response in female crickets. In three experimental sets (1) the temporal arrangement of chirp patterns broadcast from two speakers, (2) the relative timing of chirps and (3) the impact of phase differences of the carrier frequency were varied at different intensity levels between both speakers. While the arrangement of chirp patterns had little influence on the strength of turning responses, time delays up to 20 ms and phase differences of 90° and 270° clearly affected directional turning at otherwise equal intensities. In all three sets of experiments turning responses were sensitive to intensity differences and saturated at +/? 6 dB. Turning responses due to timing of pulses or phase differences were compensated by intensity differences of 2–3 dB. Building on a large body of literature on peripheral and central processing it was possible to assign the observed effects to specific processing stages in the auditory pathway of crickets.     

Mathematical models of cochlear nucleus onset neurons: I. Point neuron with many weak synaptic inputs

The cochlear nucleus (CN) presents a unique opportunity for quantitatively studying input-output transformations by neurons because it gives rise to a variety of different response types from a relatively homogeneous input source, the auditory nerve (AN). Particularly interesting among CN neurons are Onset (On) neurons, which have a prominent response to the onset of sustained sounds followed by little or no response in the steady-state. On neurons contrast sharply with their AN inputs, which respond vigorously throughout stimuli. On neurons can entrain to stimuli (firing once per cycle of a periodic stimulus) at up to 1000 Hz, unlike their AN inputs. To understand the mechanisms underlying these response patterns, we tested whether an integrate-to-threshold point-neuron model with a fixed refractory period can account for On discharge patterns for tones, systematically examining the effect of membrane time constant and the number and strength of the exclusively excitatory AN synaptic inputs. To produce both onset responses to high-frequency tone bursts and entrainment to a broad range of low-frequency tones, the model must have a short time constant (0.125 ms) and a large number (>100) of weak synaptic inputs, properties that are consistent with the electrical properties and anatomy of On-responding cells. With these parameters, the model acts like a coincidence detector with a threshold-like relationship between the instantaneous discharge rates of the output and the inputs. Onset responses to high-frequency tone bursts result because the threshold effect enhances the initial response of the AN inputs and suppresses their relatively lower sustained response. However, when the model entrains across a broad range of frequencies, it also produces short interspike intervals at the onset of high-frequency tone bursts, a response pattern not found in all types of On neurons. These results show a tradeoff, that may be a general property of many neurons, between following rapid stimulus fluctuations and responding without short interspike intervals at the onset of sustained stimuli.     

Rearing under different conditions results in different functional recoveries of giant interneurons in unilaterally cercus-ablated crickets, Gryllus bimaculatus

The effects of rearing conditions on the functional recovery of wind-sensitive giant interneurons (GIs) after unilateral cercal ablation were investigated in the cricket, Gryllus bimaculatus. Crickets were reared in a glass vials to prohibit free walking for 14 days after unilateral cercal ablation ("14-day vial" crickets). Other crickets were reared in an apparatus called a "walking inducer" (WI) to increase the walking distance during the same 14-day period ("14-day WI" crickets). In these crickets, the response properties of GIs 8-1, 9-1, 9-2, and 9-3 to air currents from various directions were investigated. From the intensity-response curves obtained, directionality curves expressed in terms of threshold velocity and response magnitude were made independently. To understand changes in the functional recovery of GIs more thoroughly, the directional characteristics of GIs in crickets 1 day after unilateral cercal ablation ("1-day free" crickets) were also compared. Between the 1-day free and 14-day vial crickets, all the GIs showed differences in both threshold velocity and response magnitude for some stimulus directions. Between the 14-day vial and 14-day WI crickets, differences in the threshold velocities of GIs 9-1, 9-2, and 9-3, and in the response magnitudes of GIs 8-1, 9-1, and 9-3 were detected. Because the rearing condition after unilateral cercal ablation largely affects the compensatory recovery in some parameters of wind-evoked escape behavior, such as relative occurrence and escape direction, we discuss the functional differences in GIs revealed here in relation to the roles of GIs in the neural system that controls escape behavior.