The synaptic origins of receptive field properties in the cricket cercal sensory system

Summary The regional distribution of cerebral glucose utilization, revealed by the¹⁴C-2DG technique, was compared between (i) toads after stimulus-specific long-term habituation of the orienting response toward a repeatedly presented prey dummy (habituation group) and (ii) non-habituated toads, readily orienting toward the repetitively presented prey stimulus (naive group). In the habituation group, the ventral medial pallium (vMP), a certain portion of the preoptic area (PO), and the dorsal hypothalamus (dHYP) showed a statistically significantincrease in¹⁴C-2DG-uptake;decrease was observed in the ventral layers of the optic tectum (vOT), a portion of the tegmental reticular formation (RET), the ventral cerebellum (vCB), and the striatum (STR). The results suggest that stimulus-specific long-term habituation of prey-catching affects both, components of thestimulus-response mediating circuit (e.g., involving OT), and structures extrinsic to it, (e.g., vMP, PO, dHYP), which may belong to amodulatory circuitry. Bilateral lesions to vMP strongly delay habituation. Our results are suggesting that damping of the adequate behavioral motor response during habituation involves active inhibitory processes of a modulatory system that develops in strength during stimulus repetition so as to suppress response output, which basically supports Sokolov's hypothesis (1975).Abbreviations A anterior dorsal thalamic nucleus - AL amygdala, lateral portion - dCB dorsal half of the cerebellum - vCB ventral half of the cerebellum - DP dorsal pallium - dHYP dorsal hypothalamus - pLP posterior half of the lateral pallium - Lpd lateral postero-dorsal thalamus - Lpv lateral postero-ventral thalamus - aMP anterior third of the medial pallium - dMP dorsal portion of the posterior medial pallium - vMP ventral two-third of the posterior medial pallium - MS medial septum - dOT dorsal layers of the optic tectum - vOT ventral layers of the optic tectum - P posterior thalamic nucleus - PO preoptic area - RET tegmental portion of the medial reticular formation - STR striatum, dorsal and ventral portion - vTEG ventral tegmentum     

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.     

Visualization of ensemble activity patterns of mechanosensory afferents in the cricket cercal sensory system with calcium imaging

The cercal sensory system of the cricket mediates the detection and analysis of low velocity air currents in the animal's immediate environment, and is implemented around an internal representation of air current direction that demonstrates the essential features of a continuous neural map. Previous neurophysiological and anatomical studies have yielded predictions of the global spatio-temporal patterns of activity that should be evoked in the sensory afferent map by air current stimuli of different directions. We tested those predictions by direct visualization of ensemble afferent activity patterns using Ca2+ -sensitive indicators. The AM ester of the fluorescent Ca2+ indicator (Oregon Green 488 BAPTA-1 AM) was injected under the sheath of a cercal sensory nerve containing all of the mechanosensory afferent axons from one cercus. Optical signals were recorded with a digital intensified CCD camera. Control experiments using direct electrical stimulation of stained and unstained nerves demonstrated that the observed Ca2+ signals within the terminal abdominal ganglion (TAG) were due to activation of the dye-loaded sensory afferent neurons. To visualize the spatial patterns of air-current-evoked ensemble activity, unidirectional air currents were applied repeatedly from eight different directions, and the optically recorded responses from each direction were averaged. The dispersion of the optical signals by the ganglion limited the spatial resolution with which these ensemble afferent activity patterns could be observed. However, resolution was adequate to demonstrate that different directional stimuli induced different spatial patterns of Ca2+ elevation in the terminal arbors of afferents within the TAG. These coarsely- resolved, optically-recorded patterns were consistent with the anatomy-based predictions.     

Constant representation of signal spatial location in the cricket cercal system]

Directional sensitivity of the abdominal giant fibers of the cricket to auditory stimulation has been investigated with special interest to the effect of the cerci position on the directional sensitivity of the giant neurons of the terminal abdominal ganglion. It has been shown that at least for some giant neurons the preferred directions of stimulation are practically independent of cerci position. (Fig. 2, 3). By other words these neurons have constant preferred directions in relation to the insect body, but not to the cerci. This property of giant neurons can be accounted for their changeable connections with many receptors having different directional selectivity. If innervation of the giant neuron is artificially restricted to one group of receptors with identical directional selectivity the described constancy of preferred directions in relation to the body disappears (Fig. 4).     

Frequency-intensity characteristics of cricket cercal interneurons: broadband units

The bilateral pairs of cercal interneurons 10-2a and 10-3a in the cricket terminal ganglion are supposed to constitute a functional system for measuring the direction of air-borne signals, based on their phase-locked responses and selective directional sensitivity. The purpose of this study was to obtain information on the frequency and intensity characteristics and thus the potential working range of this system. By recording intracellularly from the axons of the interneurons we measured responses for stimuli of varying frequency, intensity, and direction. Typically, the stimulus frequency range examined extended from 5 to 600 Hz, at intensities of 0.03–30 mm s⁻¹ (peak-to-peak air-particle velocity). The results show that interneurons 10-2a and 10-3a preserved their level of activity, response type, and direction tuning in the whole frequency range tested. Stimulus-response cross-correlograms revealed that spike trains were synchronized with stimulus waves at even higher frequencies, at least up to 1000 Hz. At a given air-particle velocity in the range of about 2–2.5 logarithmic units, the spike number responses of the interneurons were nearly constant over a wide frequency range. Directional diagrams appeared to be independent of stimulus frequency, both in orientation and in amplitude. Accepted: 14 October 1998     

Frequency-intensity characteristics of cricket cercal interneurons: low-frequency-sensitive units

Three identified interneurons of the cercal system were investigated electrophysiologically; these interneurons are sensitive only to stimulation of cercal filiform-hair sensilla by low-frequency sound. Measurement of the frequency ranges revealed cut-off frequencies between ca. 20 and 70 Hz. Analysis of the responses near threshold and at higher intensities in the frequency range 5–500 Hz shows that one of them (Interneuron 9-1b) exhibits a sensitivity maximum at the frequency-intensity combination necessary for the perception of an intraspecific signal at 30 Hz. This band-pass behavior disappears at higher stimulus intensities. In order to investigate the mechanism of the low-frequency selectivity of the interneurons, two-tone stimulation experiments were performed. When stimuli in the best-frequency range were superimposed by a 100-Hz tone, the spiking activity was suppressed in an intensity-dependent manner. Accepted: 22 July 1998     

Positional information,compartments, and the cercal sensory system of crickets

Sensory neurons on the cricket cercus preserve the spatial order of the receptor array by forming an orderly afferent projection to the CNS. To examine the mechanisms underlying the production of the receptor array and the corresponding afferent projection, we transplanted epidermis to ectopic sites. The grafted tissue was identified by transplanting epidermis from a black cricket, Gryllus, to a tan cricket, Acheta. The results revealed that apposition of normally nonadjacent tissue usually produced intercalary growth from either donor or host, but not both. The experiments showed that tissue of more lateral origin always produced the intercalary growth. Since the cercus is circular in cross section, two separate hierarchies must exist, dividing the cercus into dorsal and ventral compartments. The border between the dorsal and ventral compartments appears to represent a line of lineage restriction. Transplants from one compartment to another caused more complex responses where both donor and host contributed to the intercalary tissue. Within the dorsal or ventral compartment, positional information guides the intercalary growth. Intercalated receptors always have the phenotype of receptors normally found between the positions represented by donor and host at the graft boundary. This result provides strong support for the idea that orderly synaptic connections between afferents and interneurons are controlled by the position of the receptor at the time of its differentiation.     

Frequency-intensity characteristics of cricket cercal interneurons: units with high-pass functions

Interneurons in the cercal sensory system of crickets respond in a cell-specific manner if the cercal hair sensilla are stimulated by air-particle oscillations at frequencies below about 2000 Hz. We investigated the filter properties of several of these interneurons, and tested the effect of stimulus intensity (typically 0.3–50 mm s⁻¹ peak-to-peak air-particle velocity) on the frequency response in the range 5–600 Hz. We focus on three interneurons (the lateral and medial giant interneurons and interneuron 9-3a) of Acheta domesticus which are characterized by a relatively high sensitivity above ca. 50–200 Hz. The responses of the medial giant interneuron usually increase monotonically with frequency and intensity. Interneuron 9-3a and the lateral giant interneuron exhibit saturation or response decrement at high frequencies and intensities. The lateral giant interneuron has an additional peak of sensitivity below about 40 Hz. Small individual variations in the relative locations of the two response areas of this interneuron within the frequency-intensity field are responsible for a large variability obtained if frequency-response curves are determined for particular intensities. Stimulus frequency does not affect the principal directional preferences of the three interneurons. Nevertheless, if tested individually, the lateral giant interneuron and interneuron 9-3a exhibit small changes of directional tuning. Accepted: 12 November 1997     

Structural scaling and functional design of the cercal wind-receptor hairs of cricket

We have estimated the intrinsic mechanical parameters of cricket cercal wind-receptor hairs. The hairs were modeled as an inverted pendulum, and mechanical parameters of the equation of motion were determined from data given by a systematic measurement of mobility by the least-square error method. The theoretical torque which turns the hair shaft is given by the drag force due to the moving air. The drag force is given by the method of Stokes' mechanical impedance of an oscillating cylinder in viscous fluid. The effect of the boundary layer in which air is stagnating on the substrate surface is also taken into account. The moment of inertia of a hair shaft shows a clear length dependency to the power of 4.32 of the hair length. The torsional resistance within the hair base and the stiffness of hair-supporting spring also show clear length dependencies to the power of 2.77 and 1.67, respectively. The torsional resistance within the hair base is so large that the hair is a strongly damped non-oscillatory second-order system. The large resistance within the hair base represents an efficient energy absorption by the sensory cell. The resistance seems to match with the source impedance, i.e., the frictional resistance at the site of air-hair contact. The impedance matching provides the condition of maximum power transmission from the moving air to the sensory cell. Structural scaling is discussed in relation to the functional scaling of the frequency-range fractionation of the mechanical filter array with a common biological design. Accepted: 24 February 1998     

Mobilities of the cercal wind-receptor hairs of the cricket, Gryllus bimaculatus

The deflection sensitivities of cercal filiform hairs of the cricket, Gryllus bimaculatus, were determined by direct measurement. The tangential velocity of deflecting hair shafts in response to stimulus air motion was measured in situ by a laser-Doppler velocimeter with surface scattering of the shaft. The velocity of the stimulus air motion in a small wind tunnel was calibrated by the same velocimeter with smoke from a joss-stick. The mobility of the hair was obtained from former measurements with reference to the latter calibration of the single apparatus. A Gaussian white noise signal was employed as a stimulus waveform, and the stimulus-response transfer function was calculated through a cross-correlation method, which provides greater precision and wider frequency for a longer period of measurement. The mobility of hair was expressed in deflection amplitudes and phase shifts in reference to the velocity sinusoid of a stimulus at various frequencies. The measurements established the following conclusions. The wind receptor hairs comprise an array of mechanical band-pass filters whose best frequencies are inversely proportional to the length. The motion dynamics of the wind-receptor hairs have strong damping. Accepted: 24 February 1998     

A second cricket cereal sensory system: bristle hairs and the interneurons they activate

Summary A new sensory system, in the abdomen of the cricketAcheta domesticus, is described. It consists of hair-like receptors, which we have called bristles, distributed on the cercus and abdomen. The sensory neurons, innervating bristles of a wide variety of shapes and sizes, project to a common area of the terminal abdominal ganglion. This region is distinct from the area called the cereal glomerulus which receives input from other receptor types.Three interneurons, whose dendrites are located exclusively in the projection area of bristle sensory neurons, are then described. These interneurons respond to tactile stimuli of the cercus and abdomen, but not to infrasound or to body orientation as do previously described interneurons. Based on the anatomical segregation of the afferents and interneurons, as well as the functional distinction from previously described cereal sensory systems, it is becoming clear that the cereal system is a multimodal sensory system.     

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.     

Reaction of single cercal mechanoreceptors of the cricket, Gryllus bimaculatus, to mechanical stimulation

Naked tungsten microelectrodes were introduced through the chitinous wall close to the cell body of the receptor cells of trichoid hair sensillae, and responses to airpuffs, and rectangular, and trapezoidal displacements of the hair were recorded. Receptors of dorsal zone are activated during lateral deflection, those of ventral zone--during medial deflection and receptors of medial and lateral zones--during deflection to the cercal base. Sensitivity of receptors to the air-puffs is a function of hair length, the largest hairs being most sensitive. During trapezoidal displacement of the hair with different velocities of the slope, discharge frequency of the dynamic response is a function of velocity and angle in the range of angles up to 3-5 degrees (fig. 1). Discharge frequency of the stationary phase (corresponding to the plateau of the stimulus) is mainly a function of velocity in the range up to 6 degrees (fig. 2). The presence of sensillae with different hair length, and hence sensitivity, and definite directionality of receptors in different hair length, and hence sensitivity, and definite directionality of receptors in different zones may provide a basis for amplitude, velocity and direction discrimination of air-puffs or low-frequency mechanical stimulation by the cercal system of crickets.