Differing afferent connections of spiking and nonspiking wind-sensitive local interneurons in the terminal abdominal ganglion of the cricket Gryllus bimaculatus

Fifteen local spiking interneurons (LSIs) and twentyone local non-spiking interneurons (LNIs) were identified in the terminal abdominal ganglion (TAG) of the cricket Gryllus bimaculatus on the basis of intracellular recording and staining (Figs. 1, 5, 6). Although the majority of LNIs showed sharp directionalities (Fig. 7) the LSIs did not (Fig. 3). The directionality of LNIs varied with the recording sites within a single cell (Fig. 8). Electrical stimulations of the cereal sensory nerve suggested that the LNIs are connected monosynaptically with the sensory afferents of both the cerci, and that LSIs may possess a variety of bilateral combinations of polysynaptic connections with the sensory afferents. We found that the spiking and the non-spiking local interneurons in the cereal sensory system differ not only in their membrane properties, but also in their afferent connections, and concluded that their differing connectivity to the sensory afferents will associate them with different roles in signal processing.Abbreviations TAG terminal abdominal ganglion - LSI local spiking interneuron - LNI local non-spiking interneurons - CNS central nervous system - PSP post synaptic potential - GI giant interneuron     

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.     

Synchronous firing by specific pairs of cercal giant interneurons in crickets encodes wind direction

One prominent stimulus to evoke an escape response in crickets is the detection of air movement, such as would result from an attacking predator. Wind is detected by the cercal sensory system that consists of hundreds of sensory cells at the base of filiform hairs. These sensory cells relay information to about a dozen cercal giant and non-giant interneurons. The response of cercal sensory cells depends both, on the intensity and the direction of the wind. Spike trains of cercal giant interneurons then convey the information about wind direction and intensity to the central nervous system. Extracellular recording of multiple cercal giant interneurons shows that certain interneuron pairs fire synchronously if a wind comes from a particular direction. We demonstrate here that directional tuning curves of synchronously firing pairs of interneurons are sharper than those of single interneurons. Moreover, the sum total of all synchronously firing pairs eventually covers all wind directions. The sharpness of the tuning curves in synchronously firing pairs results from excitatory and inhibitory input from the cercal sensory neurons. Our results suggest, that synchronous firing of specific pairs of cercal giant interneurons encodes the wind direction. This was further supported by behavioral analyses.     

Biogenic amines modulate synaptic transmission between identified giant interneurons and thoracic interneurons in the escape system of the cockroach

In the escape system of the cockroach, Periplaneta americana, a population of uniquely identifiable throacic interneurons (type A or TI_As) receive information about wind via chemical synapses from a population of ventral giant interneurons (vGIs). The TI_As are involved in the integration of sensory information necessary for orienting the animal during escape. It is likely that there are times in an animal's life when it is advantageous to modify the effectiveness of synaptic transmission between the vGIs and the TI_As. Given the central position of the TI_As inthe escape system, this would greatly alter associated motor outputs. We tested the ability of octopamine, serotonin, and dopamine to modulate synaptic transmission between vGIs and TI_As. Both octopamine and dopamine significantly increased the amplitude of vGI-evoked excitatory postsynaptic potentials (EPSPs) in TI_As at 10^?4?10^?2 M, and 10^?3 M, respectively. On the other hand, serotonin significantly decreased the vGI-evoked EPSPs in TI_As at 10^?4?10^?3 M. These results indicate that octopamine, serotonin, and dopamine are capable of modulating the efficacy of transmission of important neural connections within this circuit. © 1992 John Wiley & Sons, Inc.     

White noise analysis of graded response in a wind-sensitive,nonspiking interneuron of the cockroach

1. A novel approach using a Gaussian white noise as stimulus is described which allowed quantitative analysis of neuronal responses in the cercal system of the cockroach, Periplaneta americana. Cerci were stimulated by air displacement which was modulated by a sinusoidal and a white noise signal. During the stimulation, intracellular recordings were made from a uniquely identifiable, nonspiking, local interneuron which locates within the terminal abdominal ganglion. The white noise stimulation was cross-correlated with the evoked response to compute first- and second-order kernels that could define the cell's response dynamics. 2. The interneuron, cell 101, has an exceptionally large transverse neurite that connects two asymmetrical dendritic arborizations located on both sides of the ganglion. 3. The first-order Wiener kernels in cell 101 were biphasic (differentiating). The waveforms of the kernels produced by the ipsilateral and contralateral stimulations were roughly mirror images of each other: the kernels produced by wind stimuli on the side ipsilateral to the cell body of the interneuron are initially depolarized and then hyperpolarized, whereas those on the other side are initially hyperpolarized. The polarity reversal occurred along the midline of the animal's body, and no well-defined kernel was produced by a stimulus directed head on or from the tail. 4. Mean square error (MSE) between the actual response and the model prediction suggests that the linear component in cell 101 comprises half of the cell's total response (MSEs for the linear models were about 50% at preferred directions), whereas the second-order, non-linear component is insignificant. The linear component of the wind-evoked response was bandpass with the preferred frequency of 70-90 Hz. 5. Accounting for a noise, we reasonably assumed that at high frequencies the graded response in cell 101 is linearly related to a modulation of the air displacement and sensitive to the rate of change of the signal (i.e., wind velocity) and the direction of its source. It is suggested that the dynamics of the first-order kernel simply reflect the dynamics of sensory receptors that respond linearly to wind stimulation.     

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     

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     

Development of cricket sensory hairs: changes of dynamic mechanical properties

Summary Mechanical oscillation properties of cricket (Acheta domesticus) filiform hair sensilla were measured at different larval stages, as an indication of larval sensory capacities and for comparison with data in the literature on central nervous changes during development. The hairs were stimulated by airborne vibration over a frequency range of 10 to 220 Hz. Best frequency, angular displacement at best frequency, slope of angular-displacement tuning curve and phase of hair deflection relative to air particle velocity were tested for correlation with hair length, which is proportional to the age of a sensillum. The ranges found for the various oscillation parameters in early larval stages were similar to or larger than those in adults. Oscillation properties changed with both the developmental stage of the hair sensilla and that of the whole animal. Four individually identifiable hair sensilla were analysed separately; the sensory neurons of two of them are known to change synaptic properties during maturation. Angular displacement at a given stimulus intensity was maximal for all hairs after differentiation, and decreased during further development. The hairs did not show clear common changes for any of the other oscillation parameters. Yet particular changes were found for individual hairs.     

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.     

Assembly of the cricket cercal sensory system: genetic and epigenetic control

The cercal sensory system of the cricket is being examined using anatomical, physiological, and computer simulation techniques in order to better understand the assembly of sensory systems. This particular sensory system is of interest because it functions like numerically more complex vertebrate sensory systems but offers, to the neuroscientist, the technical advantages of a small number of large identified neurons. Two aspects of sensory processing are being examined in this system; the spatial aspects of a stimulus that tell an animal where a target is in its environment, and the qualities of a stimulus that help the animal to identify the stimulus. The spatial aspects of a stimulus are analyzed by a topographic mapping of the animal's sensory environment. The feature extraction machinery for other aspects of the stimulus lacks any obvious anatomical order and is embedded within the topographic map. We are attempting to tease apart the genetic and the epigenetic components of the assembly process for this sensory system. Here we review our progress with emphasis on the epigenetic aspects of its assembly. We describe previously published work on plasticity as well as new experiments focussed on the role of neuronal activity in the assembly of this neural circuit. Finally, we briefly describe simulation experiments that are helping us understand the role of various forms of synaptic plasticity in the determination of receptive fields.     

Wind spectra and the response of the cercal system in the cockroach

Experiments on the cercal wind-sensing system of the American cockroach, Periplaneta americana, showed that the firing rate of the interneurons coding wind information depends on the bandwidth of random noise wind stimuli. The firing rate was shown to increase with decreases in the stimulus bandwidth, and be independent of changes in the total power of the stimulus with constant spectral composition. A detailed analysis of ethologically relevant stimulus parameters is presented. A phenomenological model of these relationships and their relevance to wind-mediated cockroach behavior is proposed.Abbreviations 2D two dimensional - FOWD fiber-optic wind detector - GI giant interneurons - STA spike-triggered average     

Differential channeling of sensory stimuli onto a motor neuron in the leech

We studied a specific sensory-motor pathway in the isolated leech ganglia. Pressure-sensitive mechanosensory neurons were stimulated with trains of action potentials at 5–20 Hz while recording the responses of the annulus erector motorneurons that control annuli erection. The response of the annulus erector neurons was a succession of excitatory postsynaptic potentials followed by inhibitory postsynaptic potentials. The excitatory postsynaptic potentials had a brief time-course while the inhibitory postsynaptic potentials had a prolonged time-course that enabled their temporal summation. Thus, the net effect of pressure-sensitive neuron stimulation on the annulus erector neurons was inhibitory. Both phases of the response were mediated by chemical transmission; the excitatory postsynaptic potentials were transmitted via a monosynaptic pathway, and the inhibitory postsynaptic potentials via a polysynaptic one. The pattern of expression of this dual response depended on the field of innervation of the sensory neuron and it was under the influence of cell 151, a non-spiking interneuron, that could regulate the expression of the hyperpolarization. The interaction between pressure-sensitive neurons and annulus erector neuron reveals how sensory specificity, connectivity pattern and regulatory elements interplay in a specific sensory-motor network. Accepted: 6 November 1998     

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     

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     

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     

Directional sensitivity of wind-sensitive giant interneurons in the cave cricket Troglophilus neglectus.

Unlike the situation in most cockroach and cricket species studied so far, the wind-sensitive cerci of the cave cricket Troglophilus neglectus Krauss (Rhaphidophoridae, Orthoptera) are not oriented parallel to the body axis but perpendicular to it. The effects of this difference on the morphology, and directional sensitivity of cercal giant interneurons (GIs), were investigated. In order to test the hypothesis that the 90 degrees change in cercal orientation causes a corresponding shift in directional sensitivity of GIs, their responses in both the horizontal and vertical planes were tested. One ventral and four dorsal GIs (corresponding to GIs 9-1a and 9-2a, 9-3a, 10-2a, 10-3a of gryllid crickets) were identified. The ventral GI 9-1a of Troglophilus differed somewhat from its cricket homologue in its dendritic arborisation and its directional sensitivity in the horizontal plane. The morphology and horizontal directionality of the dorsal GIs closely resembled that of their counterparts in gryllids. In the vertical plane, the directionality of all GIs tested was similar. They were all excited mainly by wind puffs from the axon-ipsilateral quadrant. The results suggest that directional sensitivity to air currents in the horizontal plane is maintained despite the altered orientation of the cerci. This is presumably due to compensatory modifications in the directional pReferences of the filiform hairs.     

The morphology and fine structure of the giant interneurons of the wood cricket Nemobius sylvestris

The structural and ultrastructural characteristics of giant interneurons in the terminal abdominal ganglion of the cricket Nemobius sylvestris were investigated by means of cobalt and fluorescent dye backfilling and transmission electron microscopy.The projections of the 8 eight pairs of the biggest ascending interneurons (giant interneurons) are described in detail. The somata of all interneurons analyzed are located contralateral to their axons, which project to the posterior region of the terminal ganglion and arborise in the cercal glomerulus. Neuron 7-1a is an exception, because its arborisation is restricted to the anterior region of the ganglion. The fine structure of giant interneurons shows typical features of highly active cells. We observed striking indentations in the perineural layer, enabling the somata of the giant interneurons to be very close to the haemolymph. The cercal glomerulus exhibits a high diversity of synaptic contacts (i.e. axo-dendritic, axo-axonic, dendro-axonic, and dendro-dendritic), as well as areas of tight junctions. Electrical synapses seem to be present, as well as mixed synapses. The anatomical organization of the giant interneurons is finally discussed in terms of functional implications and on a comparative basis.     

Neural circuitry underlying linear representation of wind information in a nonspiking local interneuron of the cockroach

In the cercal system of the cockroach Periplaneta americana, primary sensory interneurons exhibiting a sharp directional sensitivity respond to wind in a linear manner whereas those exhibiting an omnidirectional sensitivity respond nonlinearly. For example, the wind-evoked response in an identifiable, nonspiking local interneuron, 101, which responds preferentially to wind from the left versus the right, is characterized exclusively by a differential first-order (linear) kernel. However, the slow potential response in a cercal giant interneuron, GI-1, is omnidirectional, and characterized by a second-order (nonlinear) kernel with an elongated depolarizing peak on the diagonal with two off-diagonal valleys. We here examined the neural circuitry underlying the linear and nonlinear representations of wind information by the deprivation of inputs from particular sets of cercal hair afferents. Electrical stimulation of the ipsilateral (related to the soma) cercal nerve elicited a depolarizing potential in 101, which was followed by delayed hyperpolarization. A continuous flow of 10^–4 M picrotoxin, which selectively blocked this delayed hyperpolarization, resulted in a significant change in the 101 response from linear to nonlinear. Because no frequency-doubling response was observed, the nonlinearity is due to signal compression (or rectification) that reflects the mechanical property of cercal afferents. This is consistent with the hypothesis that the linear representation in 101 is based on a subtraction process between two subsets of particular column hairs, whose best optimal directions are opposite to each other.Abbreviations GABA -aminobutyric acid - GI(s) giant interneuron(s) - GI-1, GI-2, GI-3, GI-4 giant interneuron 1,2,3,4 - ipsi ipsilateral - cont contralateral - MSE(s) mean square error(s)     

Electrophysiological and morphological characterization of the medulla bilateral neurons that connect bilateral optic lobes in the cricket,Gryllus bimaculatus

The medulla bilateral neurons (MBNs) in the cricket brain directly connect two optic lobes and have been suggested to be involved in mutual coupling between the bilateral optic lobe circadian pacemakers. Single unit analysis with intracellular recording and staining with Lucifer Yellow was carried out to reveal morphology and physiology of the MBNs. Neurons having a receptive field in the rostral part of the compound eye showed greater response and a higher sensitivity to light than those having receptive fields in the ventro-caudal or dorsal portions. The MBN showed diurnal change in their responsiveness to light; the light-induced response in the night was about 1.3, 5 and 2 times of that in the day in MBN-1s, -3s and -4s, respectively. These results suggest that the MBNs mainly encode the temporal information by the magnitude of light-induced responses. The differences in magnitude of light-induced responses and of daily change in photo-responsiveness among MBNs may suggest that each group of MBNs plays different functional role in visual and/or circadian systems.