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.     

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     

Cercal sensory system and giant interneurons in Gryllodes sigillatus

The external morphologies of two cricket species, Gryllodes sigillatus and Gryllus bimaculatus, were investigated. Despite its small body length, G. sigillatus possessed longer cerci and longer cercal filiform hairs than G. bimaculatus. The estimated number of filiform hairs on a cercus was also larger in G. sigillatus than in G. bimaculatus. Wind-sensitive interneurons receiving sensory inputs from cercal filiform hairs and running in the ventral nerve cord (VNC) were investigated in G. sigillatus both morphologically and physiologically. By intracellular staining, these interneurons were proved to be morphologically homologous with previously identified giant interneurons (GIs 8-1, 9-1, 9-2, 9-3, 10-2, and 10-3) in G. bimaculatus and Acheta domesticus. In G. sigillatus, the intensity-response relationship (I-R curve) for each GI was investigated using a unidirectional air current stimulus. The stimulus was applied from 12 different directions, and an I-R curve was obtained for each stimulus direction. Each GI showed a characteristic I-R curve depending on stimulus direction. The directionality curve expressed in terms of threshold velocity showed that each GI had a distinctive directional characteristic. The functional properties of GIs in G. sigillatus, such as I-R curve, threshold velocity, and directional characteristics, were compared with those of homologous GIs in G. bimaculatus in Discussion.     

Filter characteristics of cercal afferents in the cockroach

Summary The response dynamics of cercal afferents in the cockroach, Periplaneta americana, were determined by means of a cross-correlation technique using a Gaussian white noise modulation of wind as a stimulus. The white noise stimulus could evoke sustained firing activity in most of the afferents examined (Fig. 1). The spike discharges were unitized and then cross-correlated with the stimulus to compute 1st- and 2nd-order Weiner kernels. The Ist-order kernels from a total of 28 afferents were biphasic and closely matched the time differential of a pulse (Figs. 1, 3 and 4). The amplitude and waveform of the kernels depended on the stimulus angle in such a way that the kernels were the mirror image of those on the polar opposite side (Figs. 2 and 3). The 2nd-order kernels were also differential. They had 2 diagonal peaks and 2 off-diagonal valleys in a 2-dimensional plot with 2 time axes (Figs. 1, 5 and 6). This 4-eye configuration was basically invariant irrespective of the stimulus angle, although the kernels varied in amplitude when the stimulus angle was changed. The time between the peak and a following trough of the 1st-order kernel was constant and had a mean of 4.6±0.1 ms, whereas the time between 2 diagonal peaks of the 2nd-order kernels was 4.7±0.1 ms (Figs. 4 and 6), suggesting that wind receptors (filiform sensilla) on cerci act as a band-pass filter with a peak frequency of about 106 Hz. The peak time, however, varies from 2.3 to 6.9 ms in both kernels, which may reflect the spatial distribution of the corresponding hairs on the cercus. The summation of the 1st- (linear) and 2nd-order (nonlinear) models precisely predicted the timing of the spike firing (Fig. 8). Thus, these 2 lower-order kernels can totally characterize the response dynamics of the wind receptors. The nonlinear response explains the directional sensitivity of the sensory neurons, while the differentiating 1st-order kernel explains the velocity sensitivity of the neurons. The nonlinearity is a signal compression in which one of the diagonal peaks of the 2nd-order kernel always offsets the downward phase of the 1st-order kernel (Fig. 7) and obviously represents a half-wave rectification property of the wind receptors that are excited by hair movement in only one direction and inhibited by hair movement in the polar opposite direction.     

Proboscis extension in the blowfly: directional responses to stimulation of identified chemosensitive hairs

Summary We studied the direction of proboscis extension elicited by stimulating each of an identified array of gustatory sensilla, the largest hairs, on the labellum of the flyPhormia regina. Individual hairs, or pairs of hairs, were stimulated with sucrose or water and the angle of the ensuing extension of the proboscis was recorded. The direction of the response was graded and depended on the identities of the hairs stimulated. Hairs situated on the anterior region of the labellum elicited anterior extensions, mid-level hairs elicited lateral extensions and posterior hairs resulted in posterior extensions. Previous studies of the labellar hairs have been concerned with their encoding of the chemical nature of the stimulus. Our findings show that each hair also relays information about the location of the stimulus. The positional information provided by these sensilla may help the fly to orient itself with respect to a food source.Abbreviation CES central excitatory state     

Wind-activated thoracic interneurons of the cockroach: I. Responses to controlled wind stimulation

The cockroach escape response begins with a turn away from a wind puff such as that generated by an approaching predator. The presence and direction of that wind is detected by hairs on the animal's cerci, and this information is conducted to the thoracic ganglia via two populations of giant interneurons. In the thoracic ganglia, the giant interneurons excite a number of interneurons, at least some of which in turn excite motor neurons that control leg movement. In this paper we examine response properties of various thoracic neurons to wind stimuli originating from different directions. Three sets of thoracic neurons were distinguished on the basis of latency. Type A interneurons had short latencies to wind stimuli (1.3-2.25 ms). Type B interneurons had longer latencies (4-6 ms), and motor neurons had the longest latencies (5.6-17.0 ms). Individual type A interneurons either responded equally to wind from all directions or were biased in their response. Directionality was related to the presence of ventral branches near one or both sides of the midline of the ganglion. Cells with ventral median (VM) branches on either side tended to be omnidirectional or front-rear biased, whereas cells with VM branches on only one side were biased to that side. Although several type B interneurons had strong wind responses and were directionally sensitive, they did not have VM branches. We hypothesize that the presence of VM branches in type A interneurons permits connection with ventral giant interneurons, and this connection accounts for their short latency and directional properties. This hypothesis will be tested in the companion paper.     

Distributing coordinated motor outputs to several body segments: escape movements in the cockroach

In the escape behavior of the cockroach, all six legs begin to make directed movements nearly simultaneously. The sensory stimulus that evokes these leg movements is a wind puff. Posterior wind receptors excite giant interneurons that carry a multi-cellular code for stimulus direction — and thus for turn direction-to the three thoracic ganglia, which innervate the three pairs of legs. We have attemptd to discriminate among various possible ways that the directional information in the giant interneurons could be distributed to each leg's motor circuit. Do the giant interneurons, for instance, inform separately each thoracic ganglion of wind direction? Or is there one readout system that conveys this information to all three ganglia, and if so, might the identified thoracic interneurons, which are postsynaptic to the giant interneurons, subserve this function? We made mid-sagittal lesions in one or two thoracic ganglia, thus severing the initial segments of all the known thoracic interneurons in these ganglia, and thus causing their projection axons to the other thoracic ganglia to degenerate. This lesion did not sever the giant interneurons, however (Fig. 5). Following such lesions, the legs innervated by the intact thoracic ganglia made normally directed leg movements (Figs. 4, 6, 7). Thus, the projection axons of the thoracic interneurons are not necessary for normal leg movements. Rather, the giant interneurons appear to specify to each thoracic ganglion in which direction to move the pair of legs it innervates.     

Temperature compensation in the nervous system of the grasshopper

Abstract The wind-sensitive head hair neurones of the grasshopper Schistocerca americana (Drury) are influenced by temperature, increasing the number of spikes fired in response to a given hair deflection as temperature increases. Because these neurones show similar increases in spike output for greater hair deflections, an interneurone which receives their input would not be able to distinguish changes in stimulus strength from changes in temperature, unless the effects of temperature were compensated or independently measured. This study examines the effects of temperature on the output of the tritocerebral commissure giant (TCG), an interneurone that receives wind hair input. Some wind hairs provide excitatory input to the TCG, while others are inhibitory (Bacon & Möhl, 1983). Temperature variations similar to those measured in freely moving animals were applied to the wind hairs and TCG while the interneurone's spike output was recorded. Two manipulations resulted in temperature compensated outputs from the TCG: (1) When both excitatory and inhibitory hair fields were stimulated simultaneously, the temperature sensitivity of the interneurone's spike output was significantly lower than when the excitatory hairs alone were stimulated. (2) The spike output of the TCG showed very little sensitivity to temperature changes which occurred only at its wind hair inputs, the temperature of the interneurone itself remaining constant. It is therefore possible for the output of a neural circuit to be temperature compensated even though the circuit itself may be composed of temperature-sensitive units. Possible mechanisms by which temperature compensation may be produced in the TCG are discussed, and the behavioural relevance of the conditions under which TCG output is temperature compensated is considered.     

Velarium control and visual steering in box jellyfish

Directional swimming in the box jellyfish Tripedalia cystophora (cubozoa, cnidaria) is controlled by the shape of the velarium, which is a thin muscular sheet that forms the opening of the bell. It was unclear how different patterns of visual stimulation control directional swimming and that is the focus of this study. Jellyfish were tethered inside a small experimental tank, where the four vertical walls formed light panels. All four panels were lit at the start of an experiment. The shape of the opening in the velarium was recorded in response to switching off different combinations of panels. We found that under the experimental conditions the opening in the velarium assumed three distinct shapes during a swim contraction. The opening was (1) centred or it was off-centred and pocketed out either towards (2) a rhopalium or (3) a pedalium. The shape of the opening in the velarium followed the direction of the stimulus as long as the stimulus contained directional information. When the stimulus contained no directional information, the percentage of centred pulses increased and the shape of the off-centred pulses had a random orientation. Removing one rhopalium did not change the directional response of the animals, however, the number of centred pulses increased. When three rhopalia were removed, the percentage of centred pulses increased even further and the animals lost their ability to respond to directional information.     

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.     

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.     

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     

Arthropod touch reception: spider hair sensilla as rapid touch detectors

Wandering spiders like Cupiennius salei are densely covered by tactile hairs. In darkness Cupiennius uses its front legs as tactile feelers. We selected easily identifiable hairs on the tarsus and metatarsus which are stimulated during this behavior to study tactile hair properties. Both the mechanical and electrophysiological hair properties are largely independent of the direction of hair displacement. Restoring torques measure 10(-9) to 10(-8) Nm. The torsional restoring constant S changes non-linearly with deflection angle. It is of the order of 10(-8) Nm/rad, which is about 10,000 times larger than for trichobothria. Angular thresholds for the generation of action potentials are ca.1 degrees. Electrophysiology reveals a slow and a fast sensory cell, differing in adaptation time. Both cells are movement detectors mainly responding to the dynamic phase (velocity) of a stimulus. When applying behaviorally relevant stimulus velocities (up to 11 cm s(-1)) threshold deflection for the elicitation of action potentials and maximum response frequency are reached as early as 1.2 ms after stimulus onset and followed by a rapid decline of impulse frequency. Obviously these hairs inform the spider on the mere presence of a stimulus but not on details of its time-course and spatial orientation.     

The capacity of human subjects to process directional information provided at two skin sites

The ability of human subjects to discriminate direction of tactile stimulus motion on the dorsum of the hand was determined (1) in the absence and (2) in the presence of a moving stimulus delivered to a second skin site on the ipsilateral or contralateral forelimb. When the two skin sites were simultaneously contacted by stimuli moving in the same direction, directional sensitivity was typically below that predicted for a hypothetical subject who could independently process the information provided at each of the two skin sites. Even when the stimulus delivered to a second site was deliberately ignored, it could still alter a subject's perception of stimulus direction on the dorsal hand. Moreover, its influence was greatest whenever it moved in a direction opposite to that of the attended stimulus. Whenever the two moving stimuli were delivered nonsimultaneously to two skin sites, directional sensitivity rarely matched the levels predicted for a hypothetical subject who could independently process the information provided at each site. This, in part, resulted from the subjects' utilization of "long-range" cues provided by the temporal order of stimulation. Subjects frequently failed to distinguish these cues from the sensation of stimulus direction provided at each skin site.     

A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement.

The directional selectivity of retinal ganglion cell responses represents a primitive pattern recognition that operates within a retinal neural circuit. The cellular origin and mechanism of directional selectivity were investigated by selectively eliminating retinal starburst amacrine cells, using immunotoxin-mediated cell targeting techniques. Starburst cell ablation in the adult retina abolished not only directional selectivity of ganglion cell responses but also an optokinetic eye reflex derived by stimulus movement. Starburst cells therefore serve as the key element that discriminates the direction of stimulus movement through integrative synaptic transmission and play a pivotal role in information processing that stabilizes image motion.     

Central projections of labellar taste hairs in the blowfly,Phormia regina Meigen

Summary We have traced the central projections of the receptor neurons associated with each of the eleven largest taste hairs on the labellum of the blowfly, Phormia regina (Meigen), by staining them with cobaltous lysine. The eleven hairs fall into three groups which reflect their peripheral locations and their branching patterns in the subesophageal ganglion. Group 1, consisting of the anterior hairs (numbers 1 and 2) and Group 3, consisting of the posterior hairs (numbers 9–11) project bilaterally, while Group 2, consisting of the middle hairs (numbers 3–8) projects primarily ipsilaterally. The central projections of the hairs within a single group are similar. Each hair houses four chemoreceptors, which have differing chemical sensitivities and behavioral roles, and one mechanoreceptor. In some cases, there were indications that the different cells within a single hair have different central branching patterns. For some hairs, however, it was clear that a single central branching region and pattern was shared by more than one receptor cell. We failed to find either a continuous somatotopic representation of a hair's position on the periphery, or an anatomical segregation of receptors coding for different modalities. Behavioral experiments indicate that the fly is informed both of the identity of the hair stimulated and of the chemical nature of the stimulus. Our results suggest that this information is not represented on a gross anatomical level.     

Visual Responses of Crayfish Ocular Motoneurons: An Information Theoretical Analysis

Motoneuron responses were elicited by global visual motion and stepwise displacements of an illuminated stripe. Stimulus protocols were identical to those used in previous behavioral studies of compensatory eyestalk reflexes. The firing rates and directional selectivity of the motoneuron responses were measured with respect to four stimulus dimensions (spatial frequency, contrast, angular displacement and velocity). The directional selectivity of the motoneuron response was correlated to the previously measured gain of the reflex for each stimulus dimension. The information theoretical analysis is based upon Kullback-Leibler (K-L) distances which measure the dissimilarity of responses to different stimuli. K-L distances for single neurons are strongly influenced by the mean rate difference of the responses to any pair of stimuli. Because of redundancy, the joint K-L distances of pairs of neurons were less than the sum of the K-L distances of the individual neurons. Furthermore, the joint K-L distances were only weakly influenced by correlations among coactivated neurons. For most of the stimulus dimensions, the K-L distances of single motoneurons were not sufficient to account for the stimulus discriminations exhibited by the eyestalk reflex which typically required the summed output of 2 to 5 motoneurons. Thus the behaviorally relevant information is encoded in the motoneuron ensemble. The minimum time required to discriminate the direction of motion (the encoding window) for a single motoneuron is about 380 to 480 ms (including a 175 ms response latency) for stepwise displacements and up to 1.0 s for global motion. During this period a motoneuron fires 2 to 3 impulses.     

The code for stimulus direction in a cell assembly in the cockroach

Summary The cockroachPeriplaneta americana responds to the approach of a predator by turning away. A gentle wind gust, caused by the predator's approach, excites cereal wind receptors, which encode both the presence and the direction of the stimulus. These cells in turn excite a group of giant interneurons (GI's) whose axons convey the directional information to thoracic motor centers. A given wind direction is coded not by a single GI functioning as a labeled line, but rather by some relationship among the spike trains in an assembly of GI's. This paper analyzes the code in this assembly.It is shown that all three pairs of GI's with the largest axonal diameters respond differentially to wind from left front vs. right front (Figs. 3, 4; Table 2). Each GI encodes these angles by both the time of its first action potential, and the number of action potentials, relative to its contralateral homolog. It is shown that the behavioral discrimination cannot rely solely upon the leftright differences in the time of the first action potential.A model of the assembly code is developed that involves a comparison of the numbers of action potentials in the left vs. the right group of giant interneurons. The model is shown to account for a large number of pre-existing experimental data on direction discrimination. The model requires, however, the involvement of additional cells in the left and right groups, besides the specific GI's whose role had been tested in prior experiments. The model is then tested by further experiments designed to verify the involvement of these added cells. These experiments support the model.Abbreviations A abdominal ganglion - GI giant interneuron     

A Model of Filiform Hair Distribution on the Cricket Cercus

Crickets and other orthopteran insects sense air currents with a pair of abdominal appendages resembling antennae, called cerci. Each cercus in the common house cricket Acheta domesticus is covered with between 500 to 750 filiform mechanosensory hairs. The distribution of the hairs on the cerci, as well as the global patterns of their movement axes, are very stereotypical across different animals in this species, and the development of this system has been studied extensively. Although hypotheses regarding the mechanisms underlying pattern development of the hair array have been proposed in previous studies, no quantitative modeling studies have been published that test these hypotheses. We demonstrate that several aspects of the global pattern of mechanosensory hairs can be predicted with considerable accuracy using a simple model based on two independent morphogen systems. One system constrains inter-hair spacing, and the second system determines the directional movement axes of the hairs.