The halteres of the blowfly Calliphora

The movement of the halteres during fixed flight was video recorded under stroboscopic illumination phase coupled to the wing beat. The halteres swing in a rounded triangular manner through an angle of almost 80° in vertical planes tilted backwards from the transverse plane by ca. 30° (Figs. 1, 2).The physics of the halteres are described in terms of a general formula for the force acting onto the endknob of the moving haltere during rotations and linear accelerations of the fly (Eq. 1). On the basis of the experimentally determined kinematics of the haltere, the primary forces and the forces dependent on angular velocity and on angular acceleration are calculated (Figs. 3, 4).Three distinct types of angular velocity dependent (Coriolis) forces are generated by rotations about 3 orthogonal axes. Thus, in principle one haltere could detect all rotations in space (Fig. 6).The angular acceleration dependent forces have the same direction and frequency as the Coriolis forces, but they are shifted in phase by 90°. Thus, they could be evaluated in parallel and independently from the Coriolis forces. They are, however, much smaller than the Coriolis forces for oscillation frequencies of the fly up to 20 Hz (Fig. 5). From these considerations it is concluded that Coriolis forces play the major role in detecting body rotations.     

Haltere-mediated equilibrium reflexes of the fruit fly, Drosophila melanogaster.

Flies display a sophisticated suite of aerial behaviours that require rapid sensory-motor processing. Like all insects, flight control in flies is mediated in part by motion-sensitive visual interneurons that project to steering motor circuitry within the thorax. Flies, however, possess a unique flight control equilibrium sense that is encoded by mechanoreceptors at the base of the halteres, small dumb-bell-shaped organs derived through evolutionary transformation of the hind wings. To study the input of the haltere system onto the flight control system, I constructed a mechanically oscillating flight arena consisting of a cylindrical array of light-emitting diodes that generated the moving image of a 30 degrees vertical stripe. The arena provided closed-loop visual feedback to elicit fixation behaviour, an orientation response in which flies maintain the position of the stripe in the front portion of their visual field by actively adjusting their wing kinematics. While flies orientate towards the stripe, the entire arena was swung back and forth while an optoelectronic device recorded the compensatory changes in wing stroke amplitude and frequency. In order to reduce the background changes in stroke kinematics resulting from the animal's closed-loop visual fixation behaviour, the responses to eight identical mechanical rotations were averaged in each trial. The results indicate that flies possess a robust equilibrium reflex in which angular rotations of the body elicit compensatory changes in both the amplitude and stroke frequency of the wings. The results of uni- and bilateral ablation experiments demonstrate that the halteres are required for these stability reflexes. The results also confirm that halteres encode angular velocity of the body by detecting the Coriolis forces that result from the linear motion of the haltere within the rotating frame of reference of the fly's thorax. By rotating the flight arena at different orientations, it was possible to construct a complete directional tuning map of the haltere-mediated reflexes. The directional tuning of the reflex is quite linear such that the kinematic responses vary as simple trigonometric functions of stimulus orientation. The reflexes function primarily to stabilize pitch and yaw within the horizontal plane.     

Kinematic diversity suggests expanded roles for fly halteres

The halteres of flies are mechanosensory organs that provide information about body rotations during flight. We measured haltere movements in a range of fly taxa during free walking and tethered flight. We find a diversity of wing–haltere phase relationships in flight, with higher variability in more ancient families and less in more derived families. Diverse haltere movements were observed during free walking and were correlated with phylogeny. We predicted that haltere removal might decrease behavioural performance in those flies that move them during walking and provide evidence that this is the case. Our comparative approach reveals previously unknown diversity in haltere movements and opens the possibility of multiple functional roles for halteres in different fly behaviours.     

Haltere morphology and campaniform sensilla arrangement across Diptera

One of the primary specializations of true flies (order Diptera) is the modification of the hind wings into club-shaped halteres. Halteres are complex mechanosensory structures that provide sensory feedback essential for stable flight control via an array of campaniform sensilla at the haltere base. The morphology of these sensilla has previously been described in a small number of dipteran species, but little is known about how they vary across fly taxa. Using a synoptic set of specimens representing 42 families from all of the major infraorders of Diptera, we used scanning electron microscopy to map the gross and fine structures of halteres, including sensillum shape and arrangement. We found that several features of haltere morphology correspond with dipteran phylogeny: Schizophora generally have smaller halteres with stereotyped and highly organized sensilla compared to nematoceran flies. We also found a previously undocumented high variation of haltere sensillum shape in nematoceran dipterans, as well as the absence of a dorsal sensillum field in multiple families. Overall, variation in haltere sensillar morphology across the dipteran phylogeny provides insight into the evolution of a highly specialized proprioceptive organ and a basis for future studies on haltere sensory function.     

昆虫平衡棒的发育及功能

平衡棒(haltere)是双翅目昆虫后翅特化而成的结构,可在飞行中起重要作用。平衡棒基部的感受器可以检测到飞行中的惯性力,向运动神经元提供反馈,迅速地平衡身体并纠正航向。昆虫的平衡棒由成虫盘发育形成,其特化受HOX基因(Ultrabithorax, Ubx)调控。发育成熟的平衡棒由两层上皮细胞组成,末端球状结构内部充满高度空泡化的细胞,基部具有大量感器。平衡棒的运动由独立的肌肉控制,相对于同侧的翅反向移动,翅与平衡棒的协同运动对于昆虫起飞和维持平衡十分重要。近年来,平衡棒的导航原理越来越多地应用于仿生学研究中,基于果蝇平衡棒的结构和功能,研制出多种飞行器的导航设备。本文结合近年来相关领域的研究成果,就平衡棒的发育、形态结构、功能和仿生应用等方面的研究进展进行综述,为深入理解昆虫平衡棒的发育机制和生物学功能提供参考。     

Frontal cortical afferents facilitate striatal nitric oxide transmission in vivo via a NMDA receptor and neuronal NOS-dependent mechanism

Striatal nitric oxide (NO) signaling plays a critical role in modulating neural processing and motor behavior. Nitrergic interneurons receive synaptic inputs from corticostriatal neurons and are activated via ionotropic glutamate receptor stimulation. However, the afferent regulation of NO signaling is poorly characterized. The role of frontal cortical afferents in regulating NO transmission was assessed in anesthetized rats using amperometric microsensor measurements of NO efflux and local field potential recordings. Low frequency (3 Hz) electrical stimulation of the ipsilateral cortex did not consistently evoke detectable changes in striatal NO efflux. In contrast, train stimulation (30 Hz) of frontal cortical afferents facilitated NO efflux in a stimulus intensity-dependent manner. Nitric oxide efflux evoked by train stimulation was transient, reproducible over time, and attenuated by systemic administration of either the NMDA receptor antagonist MK-801 or the neuronal NO synthase inhibitors 7-nitroindazole and NG-propyl-L-arginine. The interaction between NO efflux evoked via train stimulation and local striatal neuron activity was assessed using dual microsensor and local field potential recordings carried out concurrently in the contralateral and ipsilateral striatum, respectively. Systemic administration of the non-specific NO synthase inhibitor methylene blue attenuated both evoked NO efflux and the peak oscillation frequency (within the delta band) of local field potentials recorded immediately after train stimulation. Taken together, these observations indicate that feed-forward activation of neuronal NO signaling by phasic activation of frontal cortical afferents facilitates the synchronization of glutamate driven oscillations in striatal neurons. Thus, NO signaling may act to amplify coherent corticostriatal transmission and synchronize striatal output.     

Effects of global electrosensory signals on motion processing in the midbrain of <Emphasis Type="Italic">Eigenmannia</Emphasis>

Wave-type weakly electric fish such as Eigenmannia produce continuous sinusoidal electric fields. When conspecifics are in close proximity, interaction of these electric fields can produce deficits in electrosensory function. We examined a neural correlate of such jamming at the level of the midbrain. Previous results indicate that neurons in the dorsal layers of the torus semicircularis can (1) respond to jamming signals, (2) respond to moving electrosensory stimuli, and (3) receive convergent information from the four sensory maps of the electrosensory lateral line lobe (ELL). In this study we recorded the intracellular responses of both tuberous and ampullary neurons to moving objects. Robust Gaussian-shaped or sinusoidal responses with half-height durations between 55 ms and 581 ms were seen in both modalities. The addition of ongoing global signals with temporal-frequencies of 5 Hz attenuated the responses to the moving object by 5 dB or more. In contrast, the responses to the moving object were not attenuated by the addition of signals with temporal frequencies of 20 Hz or greater. This occurred in both the ampullary and tuberous systems, despite the fact that the ampullary afferents to the torus originate in a single ELL map whereas the tuberous afferents emerge from three maps.     

Convergence of visual,haltere, and prosternai inputs at neck motor neurons of Calliphora erythrocephala

Summary Neck muscles of Calliphora erythrocephala, situated in the anterior prothorax, are innervated on each side by 8 motor neurons arising in the brain (cervical nerve neurons, CN1–8) and at least 13 motor neurons arising in the prothoracic ganglion (anterior dorsal and frontal nerve neurons, ADN1,2 and FN1-11). Three prominent motor neurons (CN6 and FN1,2) are described in detail with special emphasis on their relationships with giant visual interneurons from the lobula plate, haltere interneurons, and primary afferents from the prosternal organs and halteres. These sensory organs detect head movement and body yaw, respectively. Neuronal relationships indicate that head movement is under multimodal sensory control that includes giant motion-sensitive neurons previously supposed to mediate the optomotor response in flying flies. The described pathways provide anatomical substrates for the control of optokinetic and yaw-incurred head movements that behavioural studies have shown must exist.     

Is Function of the Drosophila Homeotic Gene Ultrabithorax Canalized?

Genetic variation affecting the expressivity of an amorphic allele of the homeotic gene Ultrabithorax, (Ubx(1)) was characterized after 11 generations of introgression into 29 different isofemale lines. Heterozygotes display a range of haploinsufficient phenotypes, from overlap with wild-type halteres to dramatic transformations such as a 50% increase in area and the presence of over 20 bristles on the anterior margin of each haltere. In both the wild-type and mutant genetic backgrounds, there is moderate genetic variance and low environmental variance/developmental asymmetry, as expected of a trait under stabilizing selection pressure. Surprisingly, there is little evidence that mutant halteres are more variable than wild-type ones, so it is unclear that haltere development is also canalized. The correlation between wild-type and Ubx haltere size is very low, indicating that interactions among modifiers of Ubx are complex, and in some cases sex-specific. The potential quantitative genetic contributions of homeotic genes to appendage morphology are discussed, noting that population-level effects of variation in key regulatory genes may be prevalent and complex but cannot be readily extrapolated to macroevolutionary diversification.     

Takeoff diversity in Diptera

The order Diptera (true flies) are named for their two wings because their hindwings have evolved into specialized mechanosensory organs called halteres. Flies use halteres to detect body rotations and maintain stability during flight and other behaviours. The most recently diverged dipteran monophyletic subsection, the Calyptratae, is highly successful, accounting for approximately 12% of dipteran diversity, and includes common families like house flies. These flies move their halteres independently from their wings and oscillate their halteres during walking. Here, we demonstrate that this subsection of flies uses their halteres to stabilize their bodies during takeoff, whereas non-Calyptratae flies do not. We find that flies of the Calyptratae are able to take off more rapidly than non-Calyptratae flies without sacrificing stability. Haltere removal decreased both velocity and stability in the takeoffs of Calyptratae, but not other flies. The loss of takeoff velocity following haltere removal in Calyptratae (but not other flies) is a direct result of a decrease in leg extension speed. A closely related non-Calyptratae species (D. melanogaster) also has a rapid takeoff, but takeoff duration and stability are unaffected by haltere removal. Haltere use thus allows for greater speed and stability during fast escapes, but only in the Calyptratae clade.     

Differential neural control of intrarenal blood flow

To test whether renal sympathetic nerve activity (RSNA) can differentially regulate blood flow in the renal medulla (MBF) and cortex (CBF) of pentobarbital sodium-anesthetized rabbits, we electrically stimulated the renal nerves while recording total renal blood flow (RBF), CBF, and MBF. Three stimulation sequences were applied 1) varying amplitude (0.5-8 V), 2) varying frequency (0.5-8 Hz), and 3) a modulated sinusoidal pattern of varying frequency (0. 04-0.72 Hz). Increasing amplitude or frequency of stimulation progressively decreased all flow variables. RBF and CBF responded similarly, but MBF responded less. For example, 0.5-V stimulation decreased CBF by 20 +/- 9%, but MBF fell by only 4 +/- 6%. The amplitude of oscillations in all flow variables was progressively reduced as the frequency of sinusoidal stimulation was increased. An increased amplitude of oscillation was observed at 0.12 and 0.32 Hz in MBF and to a lesser extent RBF, but not CBF. MBF therefore appears to be less sensitive than CBF to the magnitude of RSNA, but it is more able to respond to these higher frequencies of neural stimulation.     

The halteres of the blowfly Calliphora

We quantitatively analysed compensatory head reactions of flies to imposed body rotations in yaw, pitch and roll and characterized the haltere as a sense organ for maintaining equilibrium. During constant velocity rotation, the head first moves to compensate retinal slip and then attains a plateau excursion (Fig. 3). Below 500°/s, initial head velocity as well as final excursion depend linearily on stimulus velocities for all three axes. Head saccades occur rarely and are synchronous to wing beat saccades (Fig. 5). They are interpreted as spontaneous actions superposed to the compensatory reaction and are thus not resetting movements like the fast phase of vestibulo-ocular nystagmus in vertebrates. In addition to subjecting the flies to actual body rotations we developed a method to mimick rotational stimuli by subjecting the body of a flying fly to vibrations (1 to 200 m, 130 to 150 Hz), which were coupled on line to the fly's haltere beat. The reactions to simulated Coriolis forces, mimicking a rotation with constant velocity, are qualitatively and to a large extent also quantitatively identical to the reactions to real rotations (Figs. 3, 7–9). Responses to roll- and pitch stimuli are co-axial. During yaw stimulation (halteres and visual) the head performs both a yaw and a roll reaction (Fig. 3e,f), thus reacting not co-axial. This is not due to mechanical constraints of the neck articulation, but rather it is interpreted as an advance compensation of a banked body position during free flight yaw turns (Fig. 10).     

The effect of surface wave propagation on neural responses to vibration in primate glabrous skin

Because tactile perception relies on the response of large populations of receptors distributed across the skin, we seek to characterize how a mechanical deformation of the skin at one location affects the skin at another. To this end, we introduce a novel non-contact method to characterize the surface waves produced in the skin under a variety of stimulation conditions. Specifically, we deliver vibrations to the fingertip using a vibratory actuator and measure, using a laser Doppler vibrometer, the surface waves at different distances from the locus of stimulation. First, we show that a vibration applied to the fingertip travels at least the length of the finger and that the rate at which it decays is dependent on stimulus frequency. Furthermore, the resonant frequency of the skin matches the frequency at which a subpopulation of afferents, namely Pacinian afferents, is most sensitive. We show that this skin resonance can lead to a two-fold increase in the strength of the response of a simulated afferent population. Second, the rate at which vibrations propagate across the skin is dependent on the stimulus frequency and plateaus at 7 m/s. The resulting delay in neural activation across locations does not substantially blur the temporal patterning in simulated populations of afferents for frequencies less than 200 Hz, which has important implications about how vibratory frequency is encoded in the responses of somatosensory neurons. Third, we show that, despite the dependence of decay rate and propagation speed on frequency, the waveform of a complex vibration is well preserved as it travels across the skin. Our results suggest, then, that the propagation of surface waves promotes the encoding of spectrally complex vibrations as the entire neural population is exposed to essentially the same stimulus. We also discuss the implications of our results for biomechanical models of the skin.     

Haltere and visual inputs sum linearly to predict wing (but not gaze) motor output in tethered flying Drosophila

In the true flies (Diptera), the hind wings have evolved into specialized mechanosensory organs known as halteres, which are sensitive to gyroscopic and other inertial forces. Together with the fly''s visual system, the halteres direct head and wing movements through a suite of equilibrium reflexes that are crucial to the fly''s ability to maintain stable flight. As in other animals (including humans), this presents challenges to the nervous system as equilibrium reflexes driven by the inertial sensory system must be integrated with those driven by the visual system in order to control an overlapping pool of motor outputs shared between the two of them. Here, we introduce an experimental paradigm for reproducibly altering haltere stroke kinematics and use it to quantify multisensory integration of wing and gaze equilibrium reflexes. We show that multisensory wing-steering responses reflect a linear superposition of haltere-driven and visually driven responses, but that multisensory gaze responses are not well predicted by this framework. These models, based on populations, extend also to the responses of individual flies.     

Body rate decoupling using haltere mid-stroke measurements for inertial flight stabilization in Diptera

Halteres, the modified rear wings of Diptera, have long been recognized as sensory organs necessary for basic flight stability. These organs, which act as vibrating structure gyroscopes, are known to sense strains proportional to Coriolis accelerations. While compensatory responses have been demonstrated that indicate the ability of insects to distinguish all components of the body rate vector, the specific mechanism by which the halteres are able to decouple the body rates has not been clearly understood. The research documented in this report describes a potential mechanism, using averaged strain and strain rate at the center of the haltere stroke, to decouple the inertial rate components. Through dynamic simulation of a nonlinear model of the haltere 3-dimensional trajectory, this straightforward method was demonstrated to provide an accurate means of generating signals that are proportional to three orthogonal body rate components. Errors associated with residual nonlinearity and rate-coupling were quantified for a bilaterally reconstructed body rate vector over a full range of pitch and yaw rates and two roll rate conditions. Models that are compatible with insect physiology are proposed for performing necessary signal averaging and bilateral processing.

Information processing in a cricket ganglion: The response of giant fibres to sound pulses

The response of giant fibres in the ventral nerve cord to stimulation of cercal afferents with pulses of sound was studied in the domestic cricket, Acheta domesticus. Pulses at 450 Hz gave the highest frequency response in several classes of units, and were therefore used as stimuli in subsequent experiments. In intact animals the response of the giant fibres to bilateral cercal stimulation showed a characteristic high frequency ‘on’ response followed by steady firing of some units for the duration of the sound pulse. The end of each pulse was followed by a short period of inhibition of the tonic units.Cercal amputation and other experiments showed that input from cercal afferents excites both large and small ipsilateral giants, and excites small and inhibits large contralateral giants. Descending input from higher neural centres in intact animals tends to reduce the responses to the stimuli. It is suggested that a function of the contralateral excitatory and inhibitory effects is to sharpen the ‘on’ response of the giant fibres to sound stimuli in intact animals.     

Excitatory convergence of periaqueductal gray and somatic afferents in the solitary tract nucleus: role for neurokinin 1 receptors

Our previous studies (Boscan P, Kasparov S, and Paton JF. Eur J Neurosci 16: 907-920, 2002) showed that activation of somatic afferents attenuated the baroreceptor reflex via neurokinin type 1 (NK(1)) and GABA(A) receptors within the nucleus of the solitary tract (NTS). The periaqueductal gray matter (PAG) can also depress baroreceptor reflex function and project to the NTS. In the present study, we have tested the possibility that the dorsolateral (dl)-PAG projects to the NTS neurons that also respond to somatic afferent input. In an in situ, arterially perfused, unanesthetized decerebrate rat preparation, somatic afferents (brachial plexus), cervical spinal cord, and dl-PAG were stimulated electrically, whereas NTS neurons were recorded extracellularly. From 45 NTS neurons excited by either brachial plexus or dl-PAG stimulation, 41 received convergence excitatory inputs from both afferents. Onset latency and evoked peak discharge frequency from brachial plexus afferents were 39.4 +/- 4.7 ms and 10.7 +/- 1.1 Hz, whereas this was 43.9 +/- 6.4 ms and 7.9 +/- 1 Hz, respectively, following dl-PAG stimulation. As revealed by using a paired pulse stimulation protocol, monosynaptic connections were found in 9 of 36 neurons tested from both spinal cord and dl-PAG. We tested NK(1)-receptor sensitivity in 38 neurons that received convergent inputs from brachial plexus/PAG. Fifteen neurons were sensitive to selective antagonism of NK(1) receptors. CP-99994, the NK(1) antagonist, failed to alter ongoing firing activity but reduced the evoked peak discharge frequency following stimulation of both brachial plexus (from 12.3 +/- 1.8 to 7.2 +/- 1.3 Hz; P < 0.01) and PAG (from 7.8 +/- 1.5 to 4.5 +/- 1 Hz; P < 0.01). We conclude that 1) somatic brachial and PAG afferents can converge onto single NTS neurons; 2) this convergence occurs via either direct or indirect pathways; and 3) NK(1) receptors are activated by some of these inputs.     

Phantoms in the brain: Ambiguous representations of stimulus amplitude and timing in weakly electric fish

In wave-type weakly electric fish, two distinct types of primary afferent fibers are specialized for separately encoding modulations in the amplitude and phase (timing) of electrosensory stimuli. Time-coding afferents phase lock to periodic stimuli and respond to changes in stimulus phase with shifts in spike timing. Amplitude-coding afferents fire sporadically to periodic stimuli. Their probability of firing in a given cycle, and therefore their firing rate, is proportional to stimulus amplitude. However, the spike times of time-coding afferents are also affected by changes in amplitude; similarly, the firing rates of amplitude-coding afferents are also affected by changes in phase. Because identical changes in the activity of an individual primary afferent can be caused by modulations in either the amplitude or phase of stimuli, there is ambiguity regarding the information content of primary afferent responses that can result in ‘phantom’ modulations not present in an actual stimulus. Central electrosensory neurons in the hindbrain and midbrain respond to these phantom modulations. Phantom modulations can also elicit behavioral responses, indicating that ambiguity in the encoding of amplitude and timing information ultimately distorts electrosensory perception. A lack of independence in the encoding of multiple stimulus attributes can therefore result in perceptual illusions. Similar effects may occur in other sensory systems as well. In particular, the vertebrate auditory system is thought to be phylogenetically related to the electrosensory system and it encodes information about amplitude and timing in similar ways. It has been well established that pitch perception and loudness perception are both affected by the frequency and intensity of sounds, raising the intriguing possibility that auditory perception may also be affected by ambiguity in the encoding of sound amplitude and timing.     

Neural network mechanisms underlying stimulus driven variability reduction

It is well established that the variability of the neural activity across trials, as measured by the Fano factor, is elevated. This fact poses limits on information encoding by the neural activity. However, a series of recent neurophysiological experiments have changed this traditional view. Single cell recordings across a variety of species, brain areas, brain states and stimulus conditions demonstrate a remarkable reduction of the neural variability when an external stimulation is applied and when attention is allocated towards a stimulus within a neuron's receptive field, suggesting an enhancement of information encoding. Using an heterogeneously connected neural network model whose dynamics exhibits multiple attractors, we demonstrate here how this variability reduction can arise from a network effect. In the spontaneous state, we show that the high degree of neural variability is mainly due to fluctuation-driven excursions from attractor to attractor. This occurs when, in the parameter space, the network working point is around the bifurcation allowing multistable attractors. The application of an external excitatory drive by stimulation or attention stabilizes one specific attractor, eliminating in this way the transitions between the different attractors and resulting in a net decrease in neural variability over trials. Importantly, non-responsive neurons also exhibit a reduction of variability. Finally, this reduced variability is found to arise from an increased regularity of the neural spike trains. In conclusion, these results suggest that the variability reduction under stimulation and attention is a property of neural circuits.