The antennal system and cockroach evasive behavior. II. Stimulus identification and localization are separable antennal functions

Cockroaches ( Periplaneta americana) orient their antennae toward moving objects based on visual cues. Presumably, this allows exploration of novel objects by the antennal flagellum. We used videographic and electrophysiological methods to determine if receptors on the flagellum are essential for triggering escape, or if they enable cockroaches to discriminate threatening from non-threatening objects that are encountered. When a flagellum was removed, and replaced with a plastic fiber, deflection of a "prosthetic flagellum" still activated the descending mechanosensory interneurons associated with escape and produced typical escape responses. However, escape was essentially eliminated by constraining the movement of the scape and pedicel at the antennal base. When cockroaches approached and briefly explored the surface of a spider or another cockroach with the flagellum, they produced escape significantly more often in response to subsequent controlled contact from a spider than from a cockroach. This discrimination did not depend on visual or wind-sensory input, but required flagellar palpation of the surface. The crucial sensory cues appear to involve texture rather than surface chemicals. These results indicate that cockroaches acquire basic information on stimulus identity during exploration of surfaces with flagellar receptors, but that basal receptors are triggers for escape behavior.     

Genetic depletion of histamine from the nervous system of Drosophila eliminates specific visual and mechanosensory behavior

The role of histamine as a fast neuro-transmitter of imaginai insect photoreceptors is firmly established. In adult Drosophila, histamine is also found in mechanosensory receptors of cuticular hair sensilla and in a small number of nonreceptor neurons in head and body ganglia. Here we investigate the function of histamine by immunohistochemical and behavioral analysis of mutants deficient in the hdc gene that codes for histidine decarboxylase. The allele hdc ^JK910 appears to be a null mutation, as histamine immunoreactivity is almost entirely eliminated. Homozygous flies are blind in various behavioral paradigms. Mutant larvae, on the other hand, show normal photokinetic responses. Thus, adult Drosophila photoreceptors most likely utilize only a single substance, histamine, as a neurotransmitter, whereas larval photoreceptors apparently employ a different transmitter. With the alleles hdc ^p211 , hdc ^p217 , and hdc ^p218 , variable amounts of histamine are found in photoreceptors and mechanoreceptors, but no histamine could be detected in any of the nonreceptor neurons. These mutants show various degrees of visual and mechanosensory impairment, as determined by quantitative behavioral assays. We conclude that histamine is required for normal function of cuticular hair sensilla and for efficient grooming of the body surface. Thus, in Drosophila, histamine represents a major functional neurotransmitter for mechanosensory receptors.Abbreviations ERG electroretinogram - WT wild type     

A model of antennal wall-following and escape in the cockroach

Cockroaches exploit tactile cues from their antennae to avoid predators. During escape running the same sensors are used to follow walls. We hypothesise that selection of these mutually exclusive behaviours can be explained without representation of the stimulus or an explicit switching mechanism. A neural model is presented that embodies this hypothesis. The model incorporates behavioural and neurophysiological data and is embedded in a mobile robot in order to test the response to stimuli in the real world. The system is shown to account for data on escape direction and high-speed wall-following in the cockroach, including the counter-intuitive observation that faster running cockroaches maintain a closer distance to the wall. The wall-following behaviour is extended to include discrimination of tactile escape cues according to behavioural context. We conclude by highlighting questions arising from the robot experiments that suggest interesting hypotheses to test in the cockroach.     

Maximally efficient prediction in the early fly visual system may support evasive flight maneuvers

The visual system must make predictions to compensate for inherent delays in its processing. Yet little is known, mechanistically, about how prediction aids natural behaviors. Here, we show that despite a 20-30ms intrinsic processing delay, the vertical motion sensitive (VS) network of the blowfly achieves maximally efficient prediction. This prediction enables the fly to fine-tune its complex, yet brief, evasive flight maneuvers according to its initial ego-rotation at the time of detection of the visual threat. Combining a rich database of behavioral recordings with detailed compartmental modeling of the VS network, we further show that the VS network has axonal gap junctions that are critical for optimal prediction. During evasive maneuvers, a VS subpopulation that directly innervates the neck motor center can convey predictive information about the fly’s future ego-rotation, potentially crucial for ongoing flight control. These results suggest a novel sensory-motor pathway that links sensory prediction to behavior.     

Candidates for the mechanosensory system in bone

Some potential mechanisms by which bone cells sense mechanical loads are described and hypotheses concerning the functioning of these mechanisms are explored. It is well known that bone tissue adapts its structure to its mechanical load environment. Recent research has illuminated the biological response of bone to mechanical loading at the cellular level, but the precise mechanosensory system that signals bone cells to deposit or resorb tissue has not been identified. The purpose of this paper is to describe the current status of this research and to suggest some possible mechanosensory systems by which bone cells might sense environmental loads.     

Allatostatins in the nerves of the antennal pulsatile organ muscle of the cockroach Diploptera punctata.

The presence of allatostatins in the nerves of the antennal pulsatile organ muscle of the cockroach Diploptera punctata was confirmed by immunocytochemistry, bioassay, and HPLC. Immunocytochemical reactivity with monoclonal antibody against allatostatin I showed strong allatostatin immunoreactivity in the antennal heart nerve which innervates this muscle with varicosities along the muscle fibers and in the insertion of the muscle on the pulsatile ampullae. Bioassay of Sep-Pak purified muscle extract demonstrated inhibition of juvenile hormone synthesis by corpora allata in vitro. A dose-response curve showed maximum inhibition of juvenile hormone synthesis was achieved with 10-20 pulsatile organ muscle eq/corpora allata, and 50% inhibition achieved with an estimated 2.6 pulsatile organ muscle eq. Two successive HPLC separations of the Sep-Pak purified extract yielded bioactive fractions corresponding to the elution times of the five known allatostatins.     

Escape trajectories of the rockpool prawn (Palaemon elegans) in response to visual and mechanosensory stimuli

Small crustaceans, such as the rockpool prawn Palaemon elegans Rathke, respond to the approach of predators by executing a version of the crustacean tail-flip response, known as the ‘jack-knife’. We used two types of stimulus to investigate the escape behaviour of P. elegans, specifically the escape trajectories taken by individual prawns. The first stimulus consisted of mechanosensory cues, while the second stimulus included visual and mechanosensory cues. Responses to the two stimulus types differed, with the combined cues from the second stimulus type resulting in escapes over longer distances, and with greater directionality, compared to those following purely mechanosensory stimulation. Altering the direction of approach of the ‘predator’ affected the proportion of escapes that were to the side opposite from the eliciting stimulus and strongly influenced escape trajectories. Such unpredictability in the escape direction of P. elegans may be an example of so-called ‘Protean’ behaviour.     

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     

Reaction times for hand movements made in response to visual versus vibratory cues

Reaction times were determined for monkeys and humans who made wrist flexion and extension movements in response to vibratory and visual cues. Humans initiated movements approximately 50 msec sooner in response to vibratory as compared to visual cues. For monkeys, this difference was approximately 100 msec. Mean daily reaction times for monkeys and humans improved with practice until they reached a steady level of performance. Increased differences between vibratory and visual reaction times were weakly correlated with increased age of humans. The increase in the differences appeared to result from decreased reaction times by older subjects for vibratory-cued movements; reaction times for visually cued movements did not consistently vary across the age range of subjects tested (19-36 years). The results obtained using this novel paradigm suggest that it may be a useful tool for simultaneously testing behavioral performance or neurological function during somatosensorimotor and visuomotor tasks.     

Work of the human visual system. I. Adequate visual stimulus]

It is shown that the adequate stimulus permitting to detect the presence of colour differentiation in the visual field is the change of relative space-time differences of light actions in different retinal points. Differences only in space or only in time are not sufficient for perception.     

Impact of motor activity and antennal mechanosensory input on the intensity of proctolin-like immunoreactivity in antennal motoneurons of crickets (Gryllus bimaculatus)

The change of the intensity of proctolin immunolabeling of 2 of 17 proctolinergic antennal motoneurons [one adductor (Ad3), and one depressor (D5)] was quantitatively studied in crickets in relation to flight and antennal deafferentation. During flight, the maintained forward position of the antennae is supported by high frequency tonic firing of Ad3 but probably all motoneurons are activated. In animals sacrificed immediately after the last of five consecutive flight periods the intensity of proctolin-like immunolabeling showed a significant decrease in the Ad3 soma in comparison to the Ad3 of non-flyers. The identical result was observed in the D5 soma. In animals sacrificed 40 h after flight, no difference in the intensity of proctolin immunolabeling between the Ad3 soma of flyers and non-flyers was evident. Thus, at high motoneuron activity, the production of proctolin may not be able to keep pace with its transport from the soma. Deletion of all proprioceptors of one antenna which respond to horizontal movements only led to a significant decrease of the intensity of proctolin immunolabeling in the Ad3 soma on the operated side, but not in the soma of D5. This indicates that selected afferent input has an impact on proctolin expression in distinct motoneuron pools. Accepted: 7 February 1997     

视觉和嗅觉信号对果蝇食物搜寻行为的协同作用

为了探索视觉和嗅觉信号在昆虫食物搜寻过程中的作用, 本研究利用杨梅和橘子为引诱物, 在实验室条件下测定了嗅觉和视觉信号诱集到的黑腹果蝇Drosophila melanogaster数量, 分析了嗅觉经历对果蝇嗅觉和视觉食物搜寻的影响。发现同源性嗅觉和视觉信号存在的杨梅诱集到的果蝇数量显著大于单一的视觉信号和嗅觉信号, 但异源性嗅觉和视觉信号组合诱集到的果蝇数量和单独的嗅觉信号相似。嗅觉信号预处理不仅能够显著增加嗅觉信号诱集到的果蝇数量, 其中杨梅嗅觉信号对杨梅预处理果蝇的吸引能力与视觉和嗅觉信号存在的杨梅相似, 而且异源性嗅觉和视觉信号组合诱集到的预处理果蝇数量也不低于视觉和嗅觉信号存在的杨梅。另外杨梅嗅觉信号预处理也能够显著增强杨梅视觉信号诱集到的果蝇数量。但嗅觉预处理并不会改变同源性视觉和嗅觉信号组合诱集到的果蝇数量。本研究表明, 果蝇同时利用视觉和嗅觉信号进行食物搜寻, 因此同源性视觉和嗅觉信号在果蝇诱集过程中具有协同作用。另外果蝇具有较强的记忆和学习能力, 能够将记忆中的嗅觉信号应用于食物搜寻。本研究结果不仅有利于我们了解果蝇在自然状态下的食物搜寻机制, 而且有利于开发更有效的果蝇新型诱捕器。     

Combined effects of olfactory and mechanical inputs in antennal lobe neurons of the cockroach

Although it has been known that olfactory and mechanical inputs from the antenna converge in the antennal lobe of the deutocerebrum of the American cockroach, the capacity of antennal lobe neurons to integrate cues from these modalities was never examined. In the present study, neurons responsive to both the odor of lemon oil and to lateral displacement of the antenna were used to compare the effects of unimodal and bimodal stimulation. The combination of olfactory and mechanical stimuli produced increases over unimodal olfactory responses in 61% (30/49) of the neurons. In the remaining neurons the response either decreased (20%; 10/49), or no bimodal interaction was apparent (19%; 9/49). Dye injection (lucifer yellow) following physiological characterization revealed that these bimodal neurons are local neurons or projection neurons. The antennal lobe links the inputs from olfactory and mechanosensory systems and provides a substrate through which olfactory and mechanical stimuli influence one another's effects. Accepted: 29 September 1997     

Roles for short-term synaptic plasticity in behavior.

Short-term synaptic plasticity is phylogenetically widespread in ascending sensory systems of vertebrate brains. Such plasticity is found at all levels of sensory processing, including in sensory cortices. The functional roles of this apparently ubiquitous short-term synaptic plasticity, however, are not well understood. Data obtained in midbrain electrosensory neurons of Eigenmannia suggest that this plasticity has at least two roles in sensory processing; enhancing low-pass temporal filtering and generating phase shifts used in processing moving sensory images. Short-term synaptic plasticity may serve similar roles in other sensory modalities, including vision.     

The site of action of pyrethrin I in the nervous system of the cockroach Periplaneta americana

Spontaneous nervous activity in the sixth abdominal ganglia of the cockroach is increased by much smaller concentrations of pyrethrin I than are needed to affect conduction in giant fibre axons, suggesting that the fatal lesions caused by pyrethrin I may be within the ganglia rather than associated with axonic conduction.Pyrethrin I is about 30 times more active than allethrin (Narahashi, 1962, a & b) against conduction in giant fibres.

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Zusammenfassung Neurophysiologische Methoden wurden angewendet, um die Wirkung von Pyrethrin I auf die Leitung von Aktionspotentialen in Riesenfasern und den Umfang der Spontanaktivität im 6. Abdominalganglion erwachsener männlicher Küchenschaben festzustellen. In Versuchen an isolierten Nervenpräparaten hatten Pyrethrin I-Konzentrationen von weniger als 10^-7 M wenig Wirkung auf die Riesenfasern, während so geringe Konzentrationen wie 10^-10 M im Ganglion die Höhe der Aktivität beeinflußten. Riesenfasern von Küchenschaben, die vorher örtlich mit DL95s von Pyrethrin I behandelt worden waren, wurden 1–4 Stunden nach der Vergiftung stark beeinflußt, wenn die Insekten stark angegriffen waren, doch war die Aktivität im 6. Abdominalganglion zu diesem Zeitpunkt stark erhöht. Einige intraganglionäre Neurone sind also gegenüber der Vergiftung mit Pyrethrinen wesentlich empfindlicher als die Riesenfasern, was darauf hindeutet, daß die gefährlichen Schädigungen durch Pyrethrine wahrscheinlich eher innerhalb der Ganglien als in peripheren Nerven auftreten.Die Wirkung von Pyrethrin I an Riesenfasern ähnelt den von Narahashi (1962 a+b) für Allethrin beschriebenen, doch war Pyrethrin I etwa 30mal aktiver.

     

Pigment-dispersing hormone-immunoreactive neurons and their relation to serotonergic neurons in the blowfly and cockroach visual system

Summary The pigment-dispersing hormone (PDH) family of neuropeptides comprises a series of closely related octadecapeptides, isolated from different species of crustaceans and insects, which can be demonstrated immunocytochemically in neurons in the central nervous system and optic lobes of some representatives of these groups (Rao and Riehm 1989). In this investigation we have extended these immunocytochemical studies to include the blowfly Phormia terraenovae and the cockroach Leucophaea maderae. In the former species tissue extracts were also tested in a bioassay: extracts of blowfly brains exhibited PDH-like biological activity, causing melanophore pigment dispersion in destalked (eyestalkless) specimens of the fiddler crab Uca pugilator. Using standard immunocytochemical techniques, we could demonstrate a small number of pigment-dispersing hormone-immunoreactive (PDH-IR) neurons innervating optic lobe neuropil in the blowfly and the cockroach. In the blowfly the cell bodies of these neurons are located at the anterior base of the medulla. At least eight PDH-IR cell bodies of two size classes can be distinguished: 4 larger and 4 smaller. Branching immunoreactive fibers invade three layers in the medulla neuropil, and one stratum distal and one proximal to the lamina synaptic layer. A few fibers can also be seen invading the basal lobula and the lobula plate. The fibers distal to the lamina appear to be derived from two of the large PDH-IR cell bodies which also send processes into the medulla. These neurons share many features in their laminamedulla morphology with the serotonin immunoreactive neurons LBO-5HT described earlier (see Nässel 1988). It could be demonstrated by immunocytochemical double labeling that the serotonin and PDH immunoreactivities are located in two separate sets of neurons. In the cockroach optic lobe PDH-IR processes were found to invade the lamina synaptic region and form a diffuse distribution in the medulla. The numerous cell bodies of the lamina-medulla cells in the cockroach are located basal to the lamina in two clusters. Additional PDH-IR cell bodies could be found at the anterior base of the medulla. The distribution and morphology of serotonin-immunoreactive neurons in the cockroach lamina was found to be very similar to the PDH-IR ones. It is hence tempting to speculate that in both species the PDH-and serotonin-immunoreactive neurons are functionally coupled with common follower neurons. These neurons may be candidates for regulating large numbers of units in the visual system. In the flies photoreceptor properties may be regulated by action of the two set of neurons at sites peripheral to the lamina synaptic layer, possibly by paracrine release of messengers.     

The role of antennal hair plates in object-guided tactile orientation of the cockroach (Periplaneta americana)

The searching behavior of blinded cockroaches was examined under unrestrained conditions, in an arena, and on a treadmill. When cockroaches searching in a circular arena touched a stationary object (metal pole) with their antennae, they frequently approached the object more closely, and then climbed up it. Similar orientation behavior was observed in tethered animals in open loop conditions, walking on a Styrofoam ball. In these restrained cockroaches, a single antenna sufficed to distinguish the angular positions of an object, in the horizontal plane (0 degrees, 45 degrees, and 90 degrees). A group of mechanosensitive hairs on the basal segment of the antenna (scapal hair plate) appears to play a major role in antennal object detection in the horizontal plane, as gauged by shaving off these scapal hair plates. In unrestrained cockroaches, shaving the scapal hair plate increased the time needed to approach an object. Under tethered conditions, the ability to turn towards and to establish antennal contact with a test object was significantly impaired.     

Cold-receptor cells supply both cold- and warm-responsive projection neurons in the antennal lobe of the cockroach

The temperature receptor cells on the cockroach antennae are all excited by rapid cooling. In the antennal lobe, however, cold- as well as warm-responsive neurons occur. They are excited either by rapid step-like cooling or rapid step-like warming. Responses to such temperature transients do not show, however, whether antennal lobe neurons convey information on slowly changing temperatures typical of temperature gradients used for orientation. In contrast slow temperature changes permit an analysis of the effects of both instantaneous temperature and its rate of change. We compared the effect of slow temperature oscillations on the responses of antennal cold-receptors cells and cold- and warm-responsive projection neurons. In all cases the discharge rates were modulated by the temperature oscillations. They displayed a double dependence on instantaneous temperature and its rate of change. Information about cooling and warming, first contained in the output of a single cold-receptor cell diverges to form the parallel pathways of cold- and warm-responsive projection neurons, thereby in particular improving the detection of fluctuations in temperature.