Hair canopy of cricket sensory system tuned to predator signals

Filiform hairs located on the cerci of crickets are among the most sensitive sensors in the animal world and enable crickets to sense the faintest air movements generated by approaching predators. While the neurophysiological and biomechanical aspects of this sensory system have been studied independently for several decades, their integration into a coherent framework was wanting. In order to evaluate the hair canopy tuning to predator signals, we built a model of cercal population coding of oscillating air flows by the hundreds of hairs on the cerci of the sand cricket Gryllus bimaculatus (Insecta: Orthoptera). A complete survey of all hairs covering the cerci was done on intact cerci using scanning electronic microscopy. An additive population coding of sinusoid signals of varying frequencies and velocities taking into account hair directionality delivered the cercal canopy tuning curve. We show that the range of frequencies and velocities at which the cricket sensory system is best tuned corresponds to the values of signals produced by approaching predators. The relative frequencies of short (< 0.5 x 10(-3) m) and long hairs and their differing responses to oscillating air flows therefore enable crickets to detect predators in a time-frequency-intensity space both as far as possible and at close range.     

The shape of wind-receptor hairs of cricket and cockroach

We examined the exact shapes of the thread-like wind-receptor hairs in the cricket and cockroach. The diameters of hairs at various distances from the hair tip as measured by scanning electron microscopy revealed unexpected hair shapes. We had expected, a priori, that the shape of the hair would be a slender linearly tapered cone, but the measurements revealed hairs in the form of extremely elongated paraboloids. The diameter of the wind-receptor hairs varies with the square root of the distance from the hair tip, i.e., the diameter rapidly increases with the distance from the tip and is asymptotic to the base diameter. Both the cricket, Gryllus bimaculatus, and the cockroach, Periplaneta americana, showed the same hair shape. In both insects, the formation of the wind-receptor hair during metamorphosis seems to be controlled by a common cytological program. The shape of the hair constrains the mobility of the wind-receptor hair, because both the drag force caused by moving air and the moment of inertia of motion dynamics are functions of shaft diameter. The shape of the hair is a biological trait which affects the sensory information transmitted to the central nervous system. Accepted: 24 February 1998     

Anatomy and physiology of identified wind-sensitive local interneurons in the cricket cercal sensory system

1. A group of wind sensitive local interneurons (9DL Interneurons) in the terminal abdominal ganglion of the cricket Acheta domesticus were identified and studied using intracellular staining and recording techniques. 2. The 9DL interneurons had apparent resting potentials ranging from -38 mV to -45 mV. At this membrane potential, these cells produced graded responses to wind stimuli; action potentials were never observed at these resting potentials. However, when the 9DL interneurons were hyperpolarized to a membrane potential of approximately -60 mV, a single action potential at the leading edge of the wind stimulus response was sometimes observed. 3. The wind stimulus threshold of the 9DL interneurons to the types of stimuli used in these studies was approximately 0.01 cm/s. Above this threshold, the excitatory responses increased logarithmically with increasing peak wind velocity up to approximately 0.5 cm/s. 4. The 9DL interneurons were directionally sensitive; their response amplitudes varied with wind stimulus orientation. 9DL1 cells responded maximally when stimulated with wind directed at the front of the animal. The apparent peak in directional sensitivity of the 9DL2 interneurons varied between the side and the rear of the animal, depending upon the site of electrode penetration within the cell's dendritic arbor. 5. The locations of dendritic branches of the 9DL interneurons within the afferent map of wind direction were used to predict the excitatory receptive field of these interneurons.     

Postembryonic changes in the response properties of wind-sensitive giant interneurons in cricket

The intensity-response (I-R) relations for four wind-sensitive giant interneurons (GIs 8-1, 9-1, 9-2 and 9-3) in the fourth-, sixth- and last-instar nymphs of the cricket, Gryllus bimaculatus, were investigated using a unidirectional air current stimulus in order to explore the functional changes of GIs during postembryonic development. Contrary to our expectations, the response properties of GIs in nymphs were largely different from those in adults. The response magnitude of GI 8-1 in an intact cricket decreased during development, i.e. the GI in younger insects showed a larger response magnitude. Although the response magnitudes of GIs 9-1 and 9-2 were almost identical during the nymphal period, a significant decrease was observed after the imaginal ecdysis. During the nymphal period, the response magnitude of GI 9-3 increased according to the developmental stage. However, it decreased significantly after the imaginal ecdysis. We also investigated the response magnitudes of the GIs in nymphs after unilateral cercal ablation. From the results of ablation experiments, the changes in excitatory and/or inhibitory connections between filiform hairs and each GI during postembryonic development were revealed.     

Excitatory influence of wind-sensitive local interneurons on an ascending interneuron in the cricket cercal sensory system

This study examined the effects of a set of identified wind-sensitive local interneurons (9DL interneurons) on the wind-evoked spike output and directional sensitivity of an ascending interneuron (10-3) in the cricket (Acheta domesticus) cercal sensory system. Comparison of the directional sensitivities of the 9DL interneurons and 10-3 revealed that 3 of the 9DL interneurons have a large degree of overlap in their excitatory receptive fields with that of 10-3. Photoinactivation of any one of these 3 9DL interneurons resulted in a significant decrease in the spike output of 10-3 at its optimal excitatory wind stimulus positions. However, the overall directional sensitivity of 10-3 remained essentially unchanged. Photoinactivation of the one 9DL interneuron which had no overlap in its excitatory receptive field with 10-3 did not affect 10-3's responsiveness to wind stimuli. Results from simultaneous intracellular recordings of 10-3 and one of the 9DL interneurons which had an excitatory influence on 10-3 showed that depolarization of the local interneuron produced an epsp in 10-3, and could elicit several action potentials. Comparison of the morphologies of the 9DL interneurons and 10-3 revealed that the 3 9DL interneurons which had an excitatory influence on 10-3 all had regions of dendritic overlap with this ascending interneuron.Abbreviations ANOVA analysis of variance - Contra contralateral - epsp excitatory post-synaptic potential - Ipsi ipsilateral - LGI lateral giant interneuron - MGI medial giant interneuron     

Stimulus-response properties of cricket cereal filiform receptors

The dynamic ranges and stimulus-response properties of a large sample of cereal filiform receptors in Acheta domesticus were investigated electrophysiologically. The relation between receptor response and stimulus velocity was a sigmoid function, the log-linear portion of which spanned 1–1.5 log units of peak air-current velocity. Different receptors responded over different but overlapping velocity ranges, such that the system velocity sensitivity range spanned at least 2.5 log units. Plots of receptor response amplitude vs. stimulus direction were sinusoidal, with a period of 360°. Long-hair receptors responded in phase with air-current velocity, and intermediate-hair receptors responded in phase with air-current acceleration. These results extend those of Shimozawa and Kanou (1984a) and Kämper and Kleindienst (1990), in which the dynamics of receptor responses were shown to depend on hair length. When individual hairs were directly mechanically deflected, their receptors responded in phase with the first derivative of hair deflection. The signal transform between the air-current stimulus and the receptor response is comprised of two processes, one biomechanical/aerodynamic and one membrane biophysical. The results of this study suggest that the parametric sensitivities of receptors are primarily determined by hair biomechanical/aerodynamic properties.Abbreviation IR infrared     

Changes in the mechanical properties of the extensible cuticle of Rhodnius through the fifth larval instar

The ultimate tensile strength (σ_UT) and the modulus of elasticity (E) of Rhodnius extensible cuticle are σ_UT = 2.20 × 10⁷ Nm^?2, E = 2.43 × 10⁸ Nm^?2 (unplasticised); σ_UT = 1.43 × 10⁷ Nm^?2, E = 9.45 × 10⁶ Nm^?2 (plasticised with 5HT) and σ_UT = 9.05 × 10⁶ Nm, E = 2.46 × 10⁶ Nm^?2 (plasticised in pH 5 buffer).The mechanical properties of cuticle from insects which have deposited additional layers of cuticle after they have been fed differ from those of cuticle from unfed insects. This is possibly due to the different composition of the additional cuticle: it is suggested that the post-feeding cuticle is providing protection and a template for the next instars cuticle.The maximum strain of extensible cuticle from starved insects is related to the amount of matrix protein present.     

Embryonic development of the sensory innervation of the antenna of the grasshopper Schistocerca gregaria

The establishment of the sensory nervous system of the antenna of the grasshopper Schistocerca gregaria was examined using immunocytochemical methods and in the light of the appendicular and articulated nature of this structure. The former is demonstrated first by the expression pattern of the segment polarity gene engrailed in the head neuromere innervating the antenna, the deutocerebrum. Engrailed expression is present in identified deutocerebral neuroblasts and, as elsewhere in the body, is continuous with cells of the posterior epithelium of the associated appendage, in this case the antenna. Second, early expression of the glial homeobox gene reversed polarity (repo) in the antenna is by a stereotypic pair of cells at the antenna base, a pattern we show is repeated metamerically for each thoracic appendage of the embryo. Subsequently, three regions of Repo expression (A1, A2, A3) are seen within the antenna, and may represent a preliminary form of articulation. Bromodeoxyuridine incorporation reveals that these regions are sites of intense cell differentiation. Neuron-specific horseradish peroxidase and Lazarillo expression confirm that the pioneers of the ventral and dorsal tracts of the antennal sensory nervous system are amongst these differentiating cells. Sets of pioneers appear simultaneously in several bands and project confluent axons towards the antennal base. We conclude that the sensory nervous system of the antenna is not pioneered from the tip of the antenna alone, but in a stepwise manner by cells from several zones. The early sensory nervous systems of antenna, maxilla and leg therefore follow a similar developmental program consistent with their serially homologous nature.     

Development of the filiform hairs on the cerci of Gryllus bimaculatus Deg. (Saltatoria,Gryllidae)

Summary The filiform hairs, mechanoreceptors of Gryllus, pass through six developmental stages during the last larval stage. The cytoplasm of their sense cells suggests intensive synthesis of protein for cellular metabolism and intercytoplasmic exchange of material via glial evaginations. Ultrahistochemical tests demonstrated acid phosphatase in the lysosomes as well as in components of the Golgi apparatus. There was no significant change in the appearance of the sense cell cytoplasm, indicating a maintained functional state also during molting. The new cuticular apparatus is formed after apolysis by the three enveloping cells. Formation of the replacement hairs is initiated by a cytoplasmic outgrowth of the trichogen cell. During morphogenesis of the new hair, the microtubules serve as a cytoskeleton and probably control the flow of vesicles, which contain phenol oxidase, also demonstrated in the Golgi apparatus, and are incorporated into the new cuticle. Bundles of microfibrils are involved in the surface sculpturing of the replacement hair. The trichogen cell also forms a number of structural elements, e.g. the cup and strut marked geometric peculiarities of which indicate that they are important in the spatial orientation of the dendrite and thus also in transduction. Reduction of the apical cell membrane of the tormogen cell after apolysis permits unrestricted growth of the new hair into the exuvial space. The tormogen cell participates in the formation of the joint membrane, parts of the socket and the articulation of the hair.Supported by the Deutsche Forschungsgemeinschaft. The author thanks Mrs. G. Thomas for drawing the diagrams, and Miss I. Grossman and Mrs. M. Ullmann for technical assistance     

Topographical organization of the auditory pathway within the prothoracic ganglion of the cricket Gryllus campestris L.

Summary The topographical organization of the prothoracic ganglion of the cricket, Gryllus campestris L., is described from horizontal, transverse, and sagittal sections of preparations specially treated to elucidate longitudinal tracts, commissures, and areas of neuropil. These structures were compared to those reported from other insect thoracic ganglia, resulting in still further evidence for a common basic morphological pattern among insect central nervous systems.Six types of auditory interneurons, all existing as mirrorimage pairs, were identified through intracellular application of the dye Lucifer yellow, and then related to several morphological patterns. Two intrasegmental neurons (ON1, ON2) are similar in location of cell bodies and course of neurites and axons; three intersegmental neurons (AN1, AN2, TN1) are likewise similar to one another. The axons of the two intrasegmental neurons cross the midline of the ganglion in the newly described omega commissure. Axons of the other four types all course within the median portion of the ventral intermediate tract and project intersegmentally.All six neuron types arborize within the ventral portion of the ring tract, the same neuropilar region in which auditory sensory neurons terminate. The ring tract is therefore considered the most important region for auditory information processing within the cricket prothoracic ganglion.     

Polar growth in pollen tubes is associated with spatially confined dynamic changes in cell mechanical properties

Cellular morphogenesis involves changes to cellular size and shape which in the case of walled cells implies the mechanical deformation of the extracellular matrix. So far, technical challenges have made quantitative mechanical measurements of this process at subcellular scale impossible. We used micro-indentation to investigate the dynamic changes in the cellular mechanical properties during the onset of spatially confined growth activities in plant cells. Pollen tubes are cellular protuberances that have a strictly unidirectional growth pattern. Micro-indentation of these cells revealed that the initial formation of a cylindrical protuberance is preceded by a local reduction in cellular stiffness. Similar cellular softening was observed before the onset of a rapid growth phase in cells with oscillating growth pattern. These findings provide the first quantitative cytomechanical data that confirm the important role of the mechanical properties of the cell wall for local cellular growth processes. They are consistent with a conceptual model that explains pollen tube oscillatory growth based on the relationship between turgor pressure and tensile resistance in the apical cell wall. To further confirm the significance of cell mechanics, we artificially manipulated the mechanical cell wall properties as well as the turgor pressure. We observed that these changes affected the oscillation profile and were able to induce oscillatory behavior in steadily growing tubes.     

Location and dynamic properties of the spike generator in an insect mechanosensory neuron

1.The cereal bristle hairs of the cockroach, Periplaneta americana, are each innervated by one mechanosensory cell and 1–5 chemosensory cells. In transepithelial recordings, chemo- and mechanosensory spikes could be discriminated from each other by their relative amplitude. 2. When current steps were applied via the sensory hair, trains of impulses were triggered whatever the polarity of the current. 3. All responses adapted to the current, but the time course of adaptation was fitted by a power law for outward currents and an exponential law for inward currents. 4. During application of outward currents, the spikes showed a negative initial phase on which a small positive component was superimposed; strong polarizations produced purely negative spikes. More classical spikes with a positive initial phase were induced by inward currents. 5. The present work supports the hypothesis of a direct excitability of the apical dendrite in cereal bristle mechanoreceptors and confirms previous results suggesting that spikes are normally triggered within that region during mechanical stimulations. It is also established, for the first time, that adaptation to currents may be different in the apical dendrite and in more basal regions of the same mechanosensory neuron.Abbreviation RP receptor potential - TEV transepithelial voltage - TTX tetrodotoxin     

Chiton integument: Ultrastructure of the sensory hairs of Mopalia muscosa (Mollusca: Polyplacophora)

Summary The dorsal integument of the girdle of the chiton Mopalia muscosa is covered by a chitinous cuticle about 0.1 mm in thickness. Within the cuticle are fusiform spicules composed of a central mass of pigment granules surrounded by a layer of calcium carbonate crystals. Tapered, curved chitinous hairs with a groove on the mesial surface pass through the cuticle and protrude above the surface. The spicules are produced by specialized groups of epidermal cells called spiniferous papillae and the hairs are produced by trichogenous papillae. Processes of pigment cells containing green granules are scattered among the cells of each type of papilla and among the common epidermal cells.The wall or cortex of each hair is composed of two layers. The cortex surrounds a central medulla that contains matrix material of low density and from 1 to 20 axial bundles of dendrites. The number of bundles within the medulla varies with the size of the hair. Each bundle contains from 1 to 25 dendrites ensheathed by processes of supporting cells. The dendrites and supporting sheath arise from epidermal cells of the central part of the papilla. At the base of each trichogenous papilla are several nerves that pass into the dermis. Two questions remain unresolved. The function of the hairs is unknown, and we have not determined whether the sensory cells are primary sensory neurons or secondary sensory cells.     

Synaptic inputs to the omega neuron of the cricket Teleogryllus oceanicus: differences in EPSP waveforms evoke by low and high sound frequencies

EPSP waveforms were recorded from the omega neuron of Teleogryllus oceanicus for 5 kHz and ultrasonic sound stimuli. EPSPs in response to 5 kHz stimuli were smooth in shape and increased in amplitude with increasing stimulus intensity, while responses to ultrasound consisted of series' of large, discrete, unitary EPSPs, which increased in frequency with stimulus intensity.The hypothesis that a few, synaptically potent receptors might account for ultrasound sensitivity was tested by examining temporal coupling between ultrasound responses of the omega neuron and of another ultrasound-sensitive neuron, INT-1. INT-1 spikes were temporally correlated both to omega neuron spikes and to the large EPSPs recorded in the omega neuron. Coupling was not apparent for 5 kHz stimuli.The omega neuron encodes the intensity of 5 kHz and ultrasonic stimuli with similar resolution. Response latencies are markedly shorter for ultrasonic stimuli.These findings suggest that 5 kHz information is carried by a relatively large number of receptors, each of which has only a small effect on central neurons, while ultrasound information is carried by a few, synaptically potent, receptors.     

Cytoskeletal changes in actin and microtubules underlie the developing surface mechanical properties of sensory and supporting cells in the mouse cochlea

Correct patterning of the inner ear sensory epithelium is essential for the conversion of sound waves into auditory stimuli. Although much is known about the impact of the developing cytoskeleton on cellular growth and cell shape, considerably less is known about the role of cytoskeletal structures on cell surface mechanical properties. In this study, atomic force microscopy (AFM) was combined with fluorescence imaging to show that developing inner ear hair cells and supporting cells have different cell surface mechanical properties with different developmental time courses. We also explored the cytoskeletal organization of developing sensory and non-sensory cells, and used pharmacological modulation of cytoskeletal elements to show that the developmental increase of hair cell stiffness is a direct result of actin filaments, whereas the development of supporting cell surface mechanical properties depends on the extent of microtubule acetylation. Finally, this study found that the fibroblast growth factor signaling pathway is necessary for the developmental time course of cell surface mechanical properties, in part owing to the effects on microtubule structure.     

Location and major postembryonic changes of identified 5-HT-immunoreactive neurones in the terminal ganglion of a cricket (Acheta domesticus)

Summary In the terminal ganglion of the cricket, Acheta domesticus, the somata of certain interneurones and efferent neurones consistently react to 5-HT immunohistochemistry. There are serially homologous pairs of bilateral interneurones seen in the neuromeres of the 7th to the 10th segment and hindgut neurones with their somata located at the posterior median end of the ganglion. In adult crickets, pairs of large efferent neurones with lateral somata supply specific genital muscles in the 8th and the 9th segment of females. In males, only one pair of these efferent neurones supplies genital muscles of the 9th segment only. These identified 5-HT-immunoreactive neurones are not detected in larval crickets before development of the genital apparatus.