A nonneural miRNA cluster mediates hearing via repression of two neural targets.

We show here that mir-279/996 are absolutely essential for development and function of Johnston's organ (JO), the primary proprioceptive and auditory organ in Drosophila Their deletion results in highly aberrant cell fate determination, including loss of scolopale cells and ectopic neurons, and mutants are electrophysiologically deaf. In vivo activity sensors and mosaic analyses indicate that these seed-related miRNAs function autonomously to suppress neural fate in nonneuronal cells. Finally, genetic interactions pinpoint two neural targets (elav and insensible) that underlie miRNA mutant JO phenotypes. This work uncovers how critical post-transcriptional regulation of specific miRNA targets governs cell specification and function of the auditory system.

Recording from Fly Taste Sensilla.

Gustatory systems sense chemicals upon contact and provide a model to investigate how these stimuli are encoded to inform various behavioral decisions including choice of foods, egg-laying sites, and mating partners. Multiple organs in the body house peripheral gustatory sensory neurons, the axons of which project to discrete regions in the subesophageal zone and ventral ganglion, representing both the location and quality of the taste stimulus. Taste neurons are broadly divided into subpopulations associated with either positive or negative behavioral valence, each expressing combinations of taste receptors-in some cases, more than 30 receptors-encoded by one or more chemosensory gene families that together determine their chemical response properties. Drosophila provides a powerful model to study gustatory coding because a majority of the taste sensory units (sensilla) are present in external taste organs (labellum and legs) and are accessible for electrophysiological analysis of tastant-evoked responses. Moreover, a large body of work on the basic characteristics of individual taste neurons housed in a sensillum, as well as on functional surveys of entire taste organs, provides a foundation for investigating further questions about taste coding, adaptability, and evolution. This protocol describes how to perform recordings of stimulus-evoked activity from Drosophila taste sensilla covering the basics of setting up the electrophysiology rig and stimulus-delivery device, sample preparation, and performing and analyzing the recordings.

Characterization of the expression of gastrin-releasing peptide and its receptor in the trigeminal and spinal somatosensory systems of Japanese macaque monkeys: Insight into humans.

Gastrin-releasing peptide (GRP) and its receptor (GRPR) have been identified as itch mediators in the spinal and trigeminal somatosensory systems in rodents. In primates, there are few reports of GRP/GRPR expression or function in the spinal sensory system and virtually nothing is known in the trigeminal system. The aim of the present study was to characterize GRP and GRPR in the trigeminal and spinal somatosensory system of Japanese macaque monkeys (Macaca fuscata). cDNA encoding GRP was isolated from the macaque dorsal root ganglion (DRG) and exhibited an amino acid sequence that was highly conserved among mammals and especially in primates. Immunohistochemical analysis demonstrated that GRP was expressed mainly in the small-sized trigeminal ganglion and DRG in adult macaque monkeys. Densely stained GRP-immunoreactive (ir) fibers were observed in superficial layers of the spinal trigeminal nucleus caudalis (Sp5C) and the spinal cord. In contrast, GRP-ir fibers were rarely observed in the principal sensory trigeminal nucleus and oral and interpolar divisions of the spinal trigeminal nucleus. cDNA cloning, in situ hybridization, and Western blot revealed substantial expression of GRPR mRNA and GRPR protein in the macaque spinal dorsal horn and Sp5C. Our Western ligand blot and ligand derivative stain for GRPR revealed that GRP directly bound in the macaque Sp5C and spinal dorsal horn as reported in rodents. Finally, GRP-ir fibers were also detected in the human spinal dorsal horn. The spinal and trigeminal itch neural circuits labeled with GRP and GRPR appear to function also in primates.

Valence opponency in peripheral olfactory processing.

A hallmark of complex sensory systems is the organization of neurons into functionally meaningful maps, which allow for comparison and contrast of parallel inputs via lateral inhibition. However, it is unclear whether such a map exists in olfaction. Here, we address this question by determining the organizing principle underlying the stereotyped pairing of olfactory receptor neurons (ORNs) in Drosophila sensory hairs, wherein compartmentalized neurons inhibit each other via ephaptic coupling. Systematic behavioral assays reveal that most paired ORNs antagonistically regulate the same type of behavior. Such valence opponency is relevant in critical behavioral contexts including place preference, egg laying, and courtship. Odor-mixture experiments show that ephaptic inhibition provides a peripheral means for evaluating and shaping countervailing cues relayed to higher brain centers. Furthermore, computational modeling suggests that this organization likely contributes to processing ratio information in odor mixtures. This olfactory valence map may have evolved to swiftly process ethologically meaningful odor blends without involving costly synaptic computation.

Changes in antennal gene expression underlying sensory system maturation in Rhodnius prolixus.

Triatomine bugs are the blood feeding insect vectors transmitting Chagas disease to humans, a neglected tropical disease that affects over 8 million people, mainly in Latin America. The behavioral responses to host cues and bug signals in Rhodnius prolixus are state dependent, i.e., they vary as a function of post-ecdysis age. At the molecular level, these changes in behavior are probably due to a modulation of peripheral and central processes. In the present study, we report a significant modulation of the expression of a large set of sensory-related genes. Results were generated by means of antennal transcriptomes of 5th instar larvae along the first week (days 0, 2, 4, 6 and 8) after ecdysis sequenced using the Illumina HiSeq platform. Significant age-induced changes in transcript abundance were established for more than 6120 genes (54,7% of 11,186 genes expressed) in the antenna of R. prolixus. This was especially true between the first two days after ecdysis when more than 2500 genes had their expression significantly altered. In contrast, expression profiles were almost identical between day 6 and 8, with only a few genes showing significant modulation of their expression. A total of 86 sensory receptors, odorant carriers and odorant degrading enzymes were significantly modulated across age points and clustered into three distinct expression profiles. The set of sensory genes whose expression increased with age (profile 3) may include candidates underlying the increased responsiveness to host cues shown by R. prolixus during the first days after molting. For the first time, we describe the maturation process undergone at the molecular level by the peripheral sensory system of a hemimetabolous insect.

Non-synaptic interactions between olfactory receptor neurons, a possible key feature of odor processing in flies.

When flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, they must solve several challenges, including reliably identifying mixtures of odorants and their intensities, and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and just mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these challenges. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic ("ephaptic") interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. We find that NSIs improve mixture ratio detection and plume structure sensing and do so more efficiently than the traditionally considered mechanism of lateral inhibition in the antennal lobe. The best performance is achieved when both mechanisms work in synergy. However, we also found that NSIs decrease the dynamic range of co-housed ORNs, especially when they have similar sensitivity to an odorant. These results shed light, from a functional perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.

Distributed sensory coding by cerebellar complex spikes in units of cortical segments.

Sensory processing is essential for motor control. Climbing fibers from the inferior olive transmit sensory signals to Purkinje cells, but how the signals are represented in the cerebellar cortex remains elusive. To examine the olivocerebellar organization of the mouse brain, we perform quantitative Ca2+ imaging to measure complex spikes (CSs) evoked by climbing fiber inputs over the entire dorsal surface of the cerebellum simultaneously. The surface is divided into approximately 200 segments, each composed of ∼100 Purkinje cells that fire CSs synchronously. Our in vivo imaging reveals that, although stimulation of four limb muscles individually elicits similar global CS responses across nearly all segments, the timing and location of a stimulus are derived by Bayesian inference from coordinated activation and inactivation of multiple segments on a single trial basis. We propose that the cerebellum performs segment-based, distributed-population coding that represents the conditional probability of sensory events.

Origin and significance of two pairs of head tentacles in the radiation of euthyneuran sea slugs and land snails.

The gastropod infraclass Euthyneura comprises at least 30,000 species of snails and slugs, including nudibranch sea slugs, sea hares and garden snails, that flourish in various environments on earth. A unique morphological feature of Euthyneura is the presence of two pairs of sensory head tentacles with different shapes and functions: the anterior labial tentacles and the posterior rhinophores or eyestalks. Here we combine molecular phylogenetic and microanatomical evidence that suggests the two pairs of head tentacles have originated by splitting of the original single tentacle pair (with two parallel nerve cords in each tentacle) as seen in many other gastropods. Minute deep-sea snails of Tjaernoeia and Parvaplustrum, which in our phylogeny belonged to the euthyneurans' sister group (new infraclass Mesoneura), have tentacles that are split along much of their lengths but associated nerves and epidermal sense organs are not as specialized as in Euthyneura. We suggest that further elaboration of cephalic sense organs in Euthyneura closely coincided with their ecological radiation and drastic modification of body plans. The monotypic family Parvaplustridae nov., superfamily Tjaernoeioidea nov. (Tjaernoeiidae + Parvaplustridae), and new major clade Tetratentaculata nov. (Mesoneura nov. + Euthyneura) are also proposed based on their phylogenetic relationships and shared morphological traits.

Sensory disruption and sensory inequities in the Anthropocene.

Anthropogenic disruptions to animal sensory ecology are as old as our species. But what about the effect on human sensory ecology? Human sensory dysfunction is increasing globally at great economic and health costs (mental, physical, and social). Contemporary sensory problems are directly tied to human behavioral changes and activity as well as anthropogenic pollution. The evolutionary sensory ecology and anthropogenic disruptions to three human senses (vision, audition, olfaction) are examined along with the economic and health costs of functionally reduced senses and demographic risk factors contributing to impairment. The primary goals of the paper are (a) to sew an evolutionary and ecological thread through clinical narratives on sensory dysfunction that highlights the impact of the built environment on the senses, and (b) to highlight structural, demographic, and environmental injustices that create sensory inequities in risk and that promote health disparities.

A spider in motion: facets of sensory guidance.

Spiders show a broad range of motions in addition to walking and running with their eight coordinated legs taking them towards their resources and away from danger. The usefulness of all these motions depends on the ability to control and adjust them to changing environmental conditions. A remarkable wealth of sensory receptors guarantees the necessary guidance. Many facets of such guidance have emerged from neuroethological research on the wandering spider Cupiennius salei and its allies, although sensori-motor control was not the main focus of this work. The present review may serve as a springboard for future studies aiming towards a more complete understanding of the spider's control of its different types of motion. Among the topics shortly addressed are the involvement of lyriform slit sensilla in path integration, muscle reflexes in the walking legs, the monitoring of joint movement, the neuromuscular control of body raising, the generation of vibratory courtship signals, the sensory guidance of the jump to flying prey and the triggering of spiderling dispersal behavior. Finally, the interaction of sensors on different legs in oriented turning behavior and that of the sensory systems for substrate vibration and medium flow are addressed.

C. elegans: a sensible model for sensory biology.

From Sydney Brenner's backyard to hundreds of labs across the globe, inspiring six Nobel Prize winners along the way, Caenorhabditis elegans research has come far in the past half century. The journey is not over. The virtues of C. elegans research are numerous and have been recounted extensively. Here, we focus on the remarkable progress made in sensory neurobiology research in C. elegans. This nematode continues to amaze researchers as we are still adding new discoveries to the already rich repertoire of sensory capabilities of this deceptively simple animal. Worms possess the sense of taste, smell, touch, light, temperature and proprioception, each of which is being studied in genetic, molecular, cellular and systems-level detail. This impressive organism can even detect less commonly recognized sensory cues such as magnetic fields and humidity.

Distinct subpopulations of mechanosensory chordotonal organ neurons elicit grooming of the fruit fly antennae.

Diverse mechanosensory neurons detect different mechanical forces that can impact animal behavior. Yet our understanding of the anatomical and physiological diversity of these neurons and the behaviors that they influence is limited. We previously discovered that grooming of the Drosophila melanogaster antennae is elicited by an antennal mechanosensory chordotonal organ, the Johnston's organ (JO) (Hampel et al., 2015). Here, we describe anatomically and physiologically distinct JO mechanosensory neuron subpopulations that each elicit antennal grooming. We show that the subpopulations project to different, discrete zones in the brain and differ in their responses to mechanical stimulation of the antennae. Although activation of each subpopulation elicits antennal grooming, distinct subpopulations also elicit the additional behaviors of wing flapping or backward locomotion. Our results provide a comprehensive description of the diversity of mechanosensory neurons in the JO, and reveal that distinct JO subpopulations can elicit both common and distinct behavioral responses.

Crocodile-like sensory scales in a Late Jurassic theropod dinosaur.

Early in amniote evolution, epidermal scales evolved in stem reptiles as an efficient barrier against water loss and ultraviolet radiation, making them a key development in the transition to a fully terrestrial existence [1]. Accordingly, epidermal scales are not simple inert structures but highly-evolved organs suited to perform a broad suite of functions. Here, we provide new data on the epidermal complexity of a non-avian theropod, Juravenator starki, from the Torleite Formation (upper Kimmeridgian), Bavaria, Germany [2]. Although epidermal scales have been noted previously on the tail of Juravenator, we report a unique scale type with distinctive circular nodes that we identify as integumentary sense organs, analogous to those in modern crocodylians. The surprising presence of such structures suggests the tail had a sensory function, which is nevertheless congruent with the inferred ecology of Juravenator and the evolution of integumentary sense organs among archosaurs.

Metabolism and Functions of Amino Acids in Sense Organs.

Sense organs (eyes, ears, nose, tongue, and skin) provide senses of sight, hearing, smell, taste, and touch, respectively, to aid the survival, development, learning, and adaptation of humans and other animals (including fish). Amino acids (AAs) play an important role in the growth, development, and functions of the sense organs. Recent work has identified receptor-mediated mechanisms responsible for the chemosensory transduction of five basic taste qualities (sweet, sour, bitter, umami and salty tastes). Abnormal metabolism of AAs result in a structural deformity of tissues and their dysfunction. To date, there is a large database for AA metabolism in the eye and skin under normal (e.g., developmental changes and physiological responses) and pathological (e.g., nutritional and metabolic diseases, nutrient deficiency, infections, and cancer) conditions. Important metabolites of AAs include nitric oxide and polyamines (from arginine), melanin and dopamine (from phenylalanine and tyrosine), and serotonin and melatonin (from tryptophan) in both the eye and the skin; γ-aminobutyrate (from glutamate) in the retina; and urocanic acid and histamine (from histidine) in the skin. At present, relatively little is known about the synthesis or catabolism of AAs in the ears, nose, and tongue. Future research should be directed to: (1) address this issue with regard to healthy ageing, nasal and sinus cancer, the regulation of food intake, and oral cavity health; and (2) understand how prenatal and postnatal nutrition and environmental pollution affect the growth, development and health of the sense organs, as well as their expression of genes (including epigenetics) and proteins in humans and other animals.

Temperature signaling underlying thermotaxis and cold tolerance in Caenorhabditis elegans.

Caenorhabditis elegans has a simple nervous system of 302 neurons. It however senses environmental cues incredibly precisely and produces various behaviors by processing information in the neural circuit. In addition to classical genetic analysis, fluorescent proteins and calcium indicators enable in vivo monitoring of protein dynamics and neural activity on either fixed or free-moving worms. These analyses have provided the detailed molecular mechanisms of neuronal and systemic signaling that regulate worm responses. Here, we focus on responses of C. elegans against temperature and review key findings that regulate thermotaxis and cold tolerance. Thermotaxis of C. elegans has been studied extensively for almost 50 years, and cold tolerance is a relatively recent concept in C. elegans. Although both thermotaxis and cold tolerance require temperature sensation, the responsible neurons and molecular pathways are different, and C. elegans uses the proper mechanisms depending on its situation. We summarize the molecular mechanisms of the major thermosensory circuit as well as the modulatory strategy through neural and tissue communication that enables fine tuning of thermotaxis and cold tolerance.

All in the Family - Touch Versus Olfaction in Moles.

Here I review, compare, and contrast the neurobiology and behavior of the common, eastern mole (Scalopus aquaticus) and the star-nosed mole (Condylura cristata). These two species are part of the same family (Talpidae) and have similar body size and general morphology. But they differ in sensory specializations, complexity of neocortical organization, and behavior. The star-nosed mole has an elaborate mechanosensory organ-the star-consisting of 22 epidermal appendages (rays) covered with 25,000 touch domes called Eimer's organs. This densely innervated structure is represented in the neocortex in three different somatosensory maps, each visible in flattened neocortical sections as a series of 11 modules representing the 11 rays from the contralateral body. The 11th ray is greatly magnified in primary somatosensory cortex (S1). Behavioral studies show the star is moved in a saccadic manner and the 11th ray is a high-resolution tactile fovea, allowing star-nosed moles to forage on small prey with unprecedented speed and efficiency. In contrast, common mole noses lack Eimer's organs, their neocortex contains only two cortical maps of the nose, and they cannot localize small prey. Yet common moles have exceptional olfactory abilities, sniffing in stereo to rapidly localize discrete odor sources originating from larger prey. In addition, common moles are shown to track odorant trails laid down by moving prey. These results highlight the surprising abilities of species once thought to be simple, and the usefulness of diverse species in revealing general principles of brain organization and behavior. Anat Rec, 2019. © 2019 American Association for Anatomy.

Seismic air guns damage rock lobster mechanosensory organs and impair righting reflex.

The effects of anthropogenic aquatic noise on marine invertebrates are poorly understood. We investigated the impact of seismic surveys on the righting reflex and statocyst morphology of the palinurid rock lobster, Jasus edwardsii, using field-based exposure to air gun signals. Following exposure equivalent to a full-scale commercial assay passing within 100-500 m, lobsters showed impaired righting and significant damage to the sensory hairs of the statocyst. Reflex impairment and statocyst damage persisted over the course of the experiments-up to 365 days post-exposure and did not improved following moulting. These results indicate that exposure to air gun signals caused morphological damage to the statocyst of rock lobsters, which can in turn impair complex reflexes. This damage and impairment adds further evidence that anthropogenic aquatic noise has the potential to harm invertebrates, necessitating a better understanding of possible ecological and economic impacts.

Acoustic Pattern Recognition and Courtship Songs: Insights from Insects.

Across the animal kingdom, social interactions rely on sound production and perception. From simple cricket chirps to more elaborate bird songs, animals go to great lengths to communicate information critical for reproduction and survival via acoustic signals. Insects produce a wide array of songs to attract a mate, and the intended receivers must differentiate these calls from competing sounds, analyze the quality of the sender from spectrotemporal signal properties, and then determine how to react. Insects use numerically simple nervous systems to analyze and respond to courtship songs, making them ideal model systems for uncovering the neural mechanisms underlying acoustic pattern recognition. We highlight here how the combination of behavioral studies and neural recordings in three groups of insects-crickets, grasshoppers, and fruit flies-reveals common strategies for extracting ethologically relevant information from acoustic patterns and how these findings might translate to other systems.

Functional Consequences of Keratan Sulfate Sulfation in Electrosensory Tissues and in Neuronal Regulation.

Keratan sulfate (KS) is a functional electrosensory and neuro-instructive molecule. Recent studies have identified novel low sulfation KS in auditory and sensory tissues such as the tectorial membrane of the organ of Corti and the Ampullae of Lorenzini in elasmobranch fish. These are extremely sensitive proton gradient detection systems that send signals to neural interfaces to facilitate audition and electrolocation. High and low sulfation KS have differential functional roles in song learning in the immature male zebra song-finch with high charge density KS in song nuclei promoting brain development and cognitive learning. The conductive properties of KS are relevant to the excitable neural phenotype. High sulfation KS interacts with a large number of guidance and neuroregulatory proteins. The KS proteoglycan microtubule associated protein-1B (MAP1B) stabilizes actin and tubulin cytoskeletal development during neuritogenesis. A second 12 span transmembrane synaptic vesicle associated KS proteoglycan (SV2) provides a smart gel storage matrix for the storage of neurotransmitters. MAP1B and SV2 have prominent roles to play in neuroregulation. Aggrecan and phosphacan have roles in perineuronal net formation and in neuroregulation. A greater understanding of the biology of KS may be insightful as to how neural repair might be improved.

Does hunger sharpen senses? A psychophysics investigation on the effects of appetite in the timing of reinforcement-oriented actions.

Evidence exists about the influence of interoception on time-keeping functions. In the current study we further addressed this topic by testing the effect of fasting and snack on the ability to estimate the duration of reinforcement-oriented grasping actions. We found that, after fasting, the time estimation for the grasping of a primary reinforcement (i.e., a muffin) was positively influenced by moderate hunger. By contrast, high hunger after fasting interfered with the timing estimation for the grasping of a neutral object (i.e., a notepad). We also reported that, after snack, individuals with high residual levels of hunger showed higher variability of responses for the timing of primary-reinforcement-oriented actions; conversely, those with low level of hunger (after snack) showed higher response variability in the timing of secondary-reinforcement-oriented actions. Finally, timing variability in the fasting condition negatively correlated with the Body Mass Index of our participants. Overall, our results indicate that both the modification of the physiological state and individual traits related to appetite might affect the subjective experience of time. This is in line with the accumulating evidence documenting the influence of interoception in temporal processing and, more in general, with the New Look in Perception theoretical view, stating that the perception of external events might be influenced by motivational states.