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Integumentary sensory organs (ISOs) are densely distributed on the jaws of crocodilians and on body scales of members of the families Crocodilidae and Gavialidae. We examined the distribution, anatomy, innervation and response properties of ISOs on the face and body of crocodilians and documented related behaviors for an alligatorid (Alligator mississippiensis) and a crocodylid (Crocodylus niloticus). Each of the ISOs (roughly 4000 in A. mississippiensis and 9000 in C. niloticus) was innervated by networks of afferents supplying multiple different mechanoreceptors. Electrophysiological recordings from the trigeminal ganglion and peripheral nerves were made to isolate single-unit receptive fields and to test possible osmoreceptive and electroreceptive functions. Multiple small (<0.1 mm(2)) receptive fields, often from a single ISO, were recorded from the premaxilla, the rostral dentary, the gingivae and the distal digits. These responded to a median threshold of 0.08 mN. The less densely innervated caudal margins of the jaws had larger receptive fields (>100 mm(2)) and higher thresholds (13.725 mN). Rapidly adapting, slowly adapting type I and slowly adapting type II responses were identified based on neuronal responses. Several rapidly adapting units responded maximally to vibrations at 20-35 Hz, consistent with reports of the ISOs' role in detecting prey-generated water surface ripples. Despite crocodilians' armored bodies, the ISOs imparted a mechanical sensitivity exceeding that of primate fingertips. We conclude that crocodilian ISOs have diverse functions, including detection of water movements, indicating when to bite based on direct contact of pursued prey, and fine tactile discrimination of items held in the jaws.

Near-field disturbances in the water column are known to trigger reflex antennular flicking in the crayfish Procambarus clarkii. We have identified the hydrodynamic sensors on the lateral antennular flagellum that constitute an afferent limb of this reflex and have measured the relative directionally dependent thresholds of the sensory neurons associated with these structures to hydrodynamic stimulation. Twenty-five individual standing feathered sensilla, comprising a sparse, linearly arrayed population of near-field sensors along the lateral and medial antennular flagella, were exposed to standardized pulsatile stimuli at 20 deg intervals along a 320 deg circular track. The results indicate that the sensilla are most sensitive to such stimulation in the plane of the flagellar axis. Identification and mechanical stimulation of single feathered sensilla in some preparations consistently evoked a flick reflex at maximal response latency, indicating that these sensors constitute at least one afferent limb for the reflex behavior. Experiments in which response latencies were measured following mechanical stimulation of truncated flagella, and were compared with the latencies in respective intact flagella, suggest that summation of inputs from the feathered sensillar pathways generates reflex flicking at minimal latencies. We discuss the possible central mechanisms that may underlie detection of critically important signals from this population of highly sensitive, inherently noisy sensors.

Terrestrial pulmonates can learn olfactory-aversion tasks and retain them in their long-term memory. To elucidate the cellular mechanisms underlying learning and memory, researchers have focused on both the peripheral and central components of olfaction: two pairs of tentacles (the superior and inferior tentacles) and a pair of procerebra, respectively. Data from tentacle-amputation experiments showed that either pair of tentacles is sufficient for olfactory learning. Results of procerebrum lesion experiments showed that the procerebra are necessary for olfactory learning but that either one of the two procerebra, rather than both, is used for each olfactory learning event. Together, these data suggest that there is a redundancy in the structures of terrestrial pulmonates necessary for olfactory learning. In our commentary we exemplify and discuss functional optimization and structural redundancy in the sensory and central organs involved in olfactory learning and memory in terrestrial pulmonates.

The antennular flagella of the crayfish Procambarus clarkii each possess a linear array of near-field receptors, termed standing feathered sensilla, that are extremely sensitive to movement of the surrounding water. Previously it had been shown that, within each flagellum, the axonal conduction velocity of the sensory neuron pair associated with each feathered sensillum was linearly related to the position of the sensillum along the flagellar axis. In the current studies I show that the conduction velocity of axons within the proximal three segments of the antennules, between the flagellum and the brain, is somewhat higher than the corresponding conduction velocity of the same axons in the flagellum, especially for those whose flagellar conduction velocity is between 1 and 3 m s(-1), even though there is no net change in axonal diameter within this part of the afferent pathway. One consequence of this change in axonal conduction properties is an effective compression of the temporal spread - potentially by as much as tenfold - which otherwise would occur in arrival times of initial spikes from each sensillum following a mechanical stimulus to the antennule. Furthermore, the pattern signature of initial spike volleys at the brain following a global hydrodynamic stimulus to the flagellum is remarkably consistent and conceivably could be recognized as such by central processing centers. I conclude that conduction velocity adjustments improve temporal summation and resolution from input volleys that originate in the highly sensitive and, hence, inherently noisy near-field receptors, thereby more effectively triggering startle response circuitry at the approach of potential predators.

The European corn borer Ostrinia nubilalis (Hübner) is a model of evolution of sexual communication in insects. Two pheromone strains produce and respond to opposite ratios of the two pheromone components, Z11 and E11-tetradecenylacetate. The Z-strain uses a ratio of 97:3 of Z11:E11 tetradecenylacetate, whereas the E-strain uses a ratio of 1:99. We studied how the difference in male preference correlates with differences in wiring of olfactory input and output neurons in the antennal lobe (AL). Activity-dependent anterograde staining, intracellular recording and immunocytochemistry were used to establish the structure and function of male olfactory receptor neurons (ORNs) and AL projection neurons (PNs). Physiologically characterized neurons were reconstructed using confocal microscopy of alpha-synapsin stained ALs. The ALs of males and females in both strains had approximately 64 glomeruli. In males the macroglomerular complex (MGC) was morphologically similar in the two strains and consisted of two major compartments, a large, medial compartment folded around a smaller, lateral one. Extensive physiological and morphological analysis revealed that in both strains the major pheromone component-specific ORNs and PNs arborize in the medial MGC glomerulus, whereas those sensitive to the minor pheromone component arborize in the lateral glomerulus. In other words, the two strains have an indistinguishable MGC morphology, but a reversed topology. Apparently, the single-gene-mediated shift that causes a radical change in behavior is located upstream of the antennal lobes, i.e. at the ORN level.

Weakly electric fish generate electric fields with an electric organ and perceive them with cutaneous electroreceptors. During active electrolocation, nearby objects are detected by the distortions they cause in the electric field. The electrical properties of objects, their form and their distance, can be analysed and distinguished. Here we focus on Gnathonemus petersii (Günther 1862), an African fish of the family Mormyridae with a characteristic chin appendix, the Schnauzenorgan. Behavioural and anatomical results suggest that the mobile Schnauzenorgan and the nasal region serve special functions in electroreception, and can therefore be considered as electric foveae. We investigated passive pre-receptor mechanisms that shape and enhance the signal carrier. These mechanisms allow the fish to focus the electric field at the tip of its Schnauzenorgan where the density of electroreceptors is highest (tip-effect). Currents are funnelled by the open mouth (funnelling-effect), which leads to a homogenous voltage distribution in the nasal region. Field vectors at the trunk, the nasal region and the Schnauzenorgan are collimated but differ in the angle at which they are directed onto the sensory surface. To investigate the role of those pre-receptor effects on electrolocation, we recorded electric images of objects at the foveal regions. Furthermore, we used a behavioural response (novelty response) to assess the sensitivity of different skin areas to electrolocation stimuli and determined the receptor densities of these regions. Our results imply that both regions - the Schnauzenorgan and the nasal region - can be termed electric fovea but they serve separate functions during active electrolocation.

It is commonly assumed that the facial pit of pitvipers forms relatively sharp images and can detect small differences in environmental surface temperatures. We have visualized the temperature contrast images formed on the facial pit membrane using a detailed optical and heat transfer analysis, which includes heat transfer through the air in the pit chambers as well as via thermal infrared radiation. We find the image on the membrane to be poorly focused and of very low temperature contrast. Heat flow through the air in the pit chambers severely limits sensitivity, particularly for small animals with small facial pit chambers. The aperture of the facial pit appears to be larger than is optimal for detecting small targets such as prey at 0.5 m. Angular resolution (i.e. sharpness) and image strength and contrast vary complexly with the size of the pit opening. As a result, the patterns of natural background temperatures obscure prey items and other environmental features, creating false patterns. Consequently, snakes cannot simply target the strongest signal to strike prey. To account for observed behavioral capabilities, the sensory endings on the pit membrane apparently must respond to temperature contrasts of 0.001 degrees C or less. While neural image sharpening likely enhances imaging performance, it appears important for foraging snakes to select ambush sites offering uniform backgrounds and strong thermal contrasts. As the ancestral facial pit was likely less sensitive than the current organ, objects with strong thermal signals, such as habitat features, were needed to drive the evolution of this remarkable sense.

The primordial functional role of honey bee males (drones) is to mate with virgin queens, a behaviour relying heavily on the olfactory detection of queen pheromone. In the present work I studied olfactory processing in the drone antennal lobe (AL), the primary olfactory centre of the insect brain. In drones, the AL consists of about 103 ordinary glomeruli and four enlarged glomeruli, the macroglomeruli (MG). Two macroglomeruli (MG1 and MG2) and approximately 20 ordinary glomeruli occupy the anterior surface of the antennal lobe and are thus accessible to optical recordings. Calcium imaging was used to measure odour-evoked responses to queen pheromonal components and plant odours. MG2 responded specifically to the main component of the queen mandibular pheromone, 9-ODA. The secondary components HOB and HVA each triggered activity in one, but not the same, ordinary glomerulus. MG1 did not respond to any of the tested stimuli. Plant odours induced signals only in ordinary glomeruli in a combinatorial manner, as in workers. This study thus shows that the major queen pheromonal component is processed in the most voluminous macroglomerulus of the drone antennal lobe, and that plant odours, as well as some queen pheromonal components, are processed in ordinary glomeruli.

Even though variation in morphology is known to translate into variation in performance, studies looking at structural variability of a sensor to predict its consequences on the performance of animals are exceedingly rare. We investigated the morphological variability of air-flow-sensing receptors in wild populations of wood crickets (Nemobius sylvestris) sampled in a wide variety of habitats differing in latitude, litter structure, vegetation and predator communities. These hair receptors act as predator sensors. The observed levels of hair morphological variation were then incorporated into a biomechanical model of the hair canopy response to air flow to predict their influence on cricket predator perception. Cricket populations differ from each other, often strongly so, in the total number of hairs and in the number of hairs longer than 1 mm, which are the hairs most sensitive for the perception of approaching predators. The hair canopy response, the output of the biomechanical model, sums up over the entire canopy the angles of deflection at which a neurophysiological response is triggered and represents the sensitivity of the cercal system. It is 35% higher in the most sensitive population, compared with the least sensitive population. These large differences in perception sensitivity for a given predator signal translate into larger distances at which predators could be perceived. Thus, differences in morphology at the sensor level seem to be translated both at the perception level and subsequently at the performance level of crickets.

Pitvipers (Viperidae: Crotalinae) possess thermal radiation receptors, the facial pits, which allow them to detect modest temperature fluctuations within their environments. It was previously thought that these organs were used solely to aid in prey acquisition, but recent findings demonstrated that western diamondback rattlesnakes (Crotalus atrox) use them to direct behavioral thermoregulation, suggesting that facial pits might be general purpose organs used to drive a suite of behaviors. To investigate this further, we conducted a phylogenetic survey of viperine thermoregulatory behavior cued by thermal radiation. We assessed this behavior in 12 pitviper species, representing key nodes in the evolution of pitvipers and a broad range of thermal environments, and a single species of true viper (Viperidae: Viperinae), a closely related subfamily of snakes that lack facial pits but possess a putative thermal radiation receptor. All pitviper species were able to rely on their facial pits to direct thermoregulatory movements, while the true viper was unable to do so. Our results suggest that thermoregulatory behavior cued by thermal radiation is a universal role of facial pits and probably represents an ancestral trait among pitvipers. Further, they establish behavioral thermoregulation as a plausible hypothesis explaining the evolutionary origin of the facial pit.

In Drosophila melanogaster, antennal hearing organs mediate the detection of conspecific songs. Combining laser Doppler vibrometry, acoustic near-field measurements and anatomical analysis, we have investigated the first steps in Drosophila audition, i.e. the conversion of acoustic energy into mechanical vibrations and the subsequent transmission of vibrations to the auditory receptors in the base of the antenna. Examination of the mechanical responses of the antennal structures established that the distal antennal parts (the funiculus and the arista) together constitute a mechanical entity, the sound receiver. Unconventionally, this receiver is asymmetric, resulting in an unusual, rotatory pattern of vibration; in the presence of sound, the arista and the funiculus together rotate about the longitudinal axis of the latter. According to the mechanical response characteristics, the antennal receiver represents a moderately damped simple harmonic oscillator. The receiver's resonance frequency increases continuously with the stimulus intensity, demonstrating the presence of a non-linear stiffness that may be introduced by the auditory sense organ. This surprising, non-linear effect is relevant for close-range acoustic communication in Drosophila; by improving antennal sensitivity at low song intensities and reducing sensitivity when intensity is high, it brings about dynamic range compression in the fly's auditory system.

Lake Michigan mottled sculpin, Cottus bairdi, exhibit a naturally occurring and unconditioned orienting response that can be triggered by both live prey and chemically inert vibrating spheres, even in blinded animals. CoCl(2)-induced reductions of the orienting response demonstrate that the lateral line is required for this behavior in the absence of non-mechanosensory cues (such as vision), but shed no light on the relative contributions of superficial and canal neuromasts to this behavior. To determine the relative roles of these two subsystems, we measured the frequency with which mottled sculpin oriented towards a small vibrating sphere before and after two treatments: (i) immersion of fish in a solution of gentamicin, an aminoglycoside antibiotic that damages hair cells in canal, but not superficial, neuromasts; and (ii) scraping the skin of the fish, which damages the superficial, but not the canal, neuromasts. To ensure that both superficial and canal neuromasts were adequately stimulated, we tested at different vibration frequencies (10 and 50 Hz) near or at the best frequency for each type of neuromast. At both test frequencies, response rates before treatment were greater than 70 % and were significantly greater than 'spontaneous' response frequencies measured in the absence of sphere vibration. Response rates fell to spontaneous levels after 1 day of gentamicin treatment and did not return to pre-treatment levels for 10-15 days. In contrast, response rates stayed approximately the same after superficial neuromasts had been damaged by skin abrasion. Scanning electron microscopy confirmed hair cell damage (loss of apical cilia) in canal, but not superficial, neuromasts of gentamicin-treated animals after as little as 24 h of treatment. The sensory epithelium of canal neuromasts gradually returned to normal, following a time course similar to behavioral loss and recovery of the orienting response, whereas that of superficial neuromasts appeared normal throughout the entire period. This study shows that the orienting response of the mottled sculpin is mediated by canal neuromasts.

Male mosquitoes are attracted by the flight sounds of conspecific females. In males only, the antennal flagellum bears a large number of long hairs and is therefore said to be plumose. As early as 1855, it was proposed that this remarkable antennal anatomy served as a sound-receiving structure. In the present study, the sound-induced vibrations of the antennal flagellum in male and female Aedes aegypti were compared, and the functional significance of the flagellar hairs for audition was examined. In both males and females, the antennae are resonantly tuned mechanical systems that move as simple forced damped harmonic oscillators when acoustically stimulated. The best frequency of the female antenna is around 230 Hz; that of the male is around 380 Hz, which corresponds approximately to the fundamental frequency of female flight sounds. The antennal hairs of males are resonantly tuned to frequencies between approximately 2600 and 3100 Hz and are therefore stiffly coupled to, and move together with, the flagellar shaft when stimulated at biologically relevant frequencies around 380 Hz. Because of this stiff coupling, forces acting on the hairs can be transmitted to the shaft and thus to the auditory sensory organ at the base of the flagellum, a process that is proposed to improve acoustic sensitivity. Indeed, the mechanical sensitivity of the male antenna not only exceeds the sensitivity of the female antenna but also those of all other arthropod movement receivers studied so far.