The wing membrane of the big brown bat (Eptesicus fuscus) is covered by a sparse grid of microscopic hairs. We showed previously that various tactile receptors (e.g., lanceolate endings and Merkel ...cell neurite complexes) are associated with wing-hair follicles. Furthermore, we found that depilation of these hairs decreased the maneuverability of bats in flight. In the present study, we investigated whether somatosensory signals arising from the hairs carry information about airflow parameters. Neural responses to calibrated air puffs on the wing were recorded from primary somatosensory cortex of E. fuscus Single units showed sparse, phasic, and consistently timed spikes that were insensitive to air-puff duration and magnitude. The neurons discriminated airflow from different directions, and a majority responded with highest firing rates to reverse airflow from the trailing toward the leading edge of the dorsal wing. Reverse airflow, caused by vortices, occurs commonly in slowly flying bats. Hence, the present findings suggest that cortical neurons are specialized to monitor reverse airflow, indicating laminar airflow disruption (vorticity) that potentially destabilizes flight and leads to stall.
Bat wings are adaptive airfoils that enable demanding flight maneuvers. The bat wing is sparsely covered with sensory hairs, and wing-hair removal results in reduced flight maneuverability. Here, we report for the first time single-neuron responses recorded from primary somatosensory cortex to airflow stimulation that varied in amplitude, duration, and direction. The neurons show high sensitivity to the directionality of airflow and might act as stall detectors.
The bat wing is a highly adaptive airfoil that enables demanding flight maneuvers that are performed with robustness under turbulent conditions, and stability at slow flight speeds. The bat wing is ...covered with microscopically small, tactile hairs that have been shown to be involved in sensing air flow for improved flight maneuverability in 2 bat species, the frugivorous–nectarivorous Carollia perspicillata and the insectivorous Eptesicus fuscus. Here, we provide comparative data on the anatomy of these hairs and their distribution on the wing surface in 4 species of bats (C. perspicillata, Desmodus rotundus, E. fuscus, and Rousettus aegyptiacus), based on scanning electron microscopy analyses. Hairs were found on both the dorsal and ventral surfaces of the wing in all species, including the bony structures. They were generally sparsely distributed (1–3 hairs/mm2) and often found arranged in single file along elastin bands that extend through the wing membrane. Fringes of hairs also were found at the leading edge of the propatagium. The hairs were strongly tapered in all species. Their length varied from 0.08 mm (E. fuscus) to 3 mm (R. aegyptiacus). Hair length correlated positively with the body mass and wing loading value of each species, but not with aspect ratio, flight speed, or diet. We conclude that the hairs are spaced so that viscous coupling is negligible, at least for single-file hairs, and that they are scaled to the boundary layer of airflow limited to the first few millimeters close to the wing surface.
Animals can use different sensory signals to localize objects in the environment. Depending on the situation, the brain either integrates information from multiple sensory sources or it chooses the ...modality conveying the most reliable information to direct behavior. This suggests that somehow, the brain has access to a modality-invariant representation of external space. Accordingly, neural structures encoding signals from more than one sensory modality are best suited for spatial information processing. In primates, the posterior parietal cortex (PPC) is a key structure for spatial representations. One substructure within human and macaque PPC is the ventral intraparietal area (VIP), known to represent visual, vestibular, and tactile signals. In the present study, we show for the first time that macaque area VIP neurons also respond to auditory stimulation. Interestingly, the strength of the responses to the acoustic stimuli greatly depended on the spatial location of the stimuli i.e., most of the auditory responsive neurons had surprisingly small spatially restricted auditory receptive fields (RFs). Given this finding, we compared the auditory RF locations with the respective visual RF locations of individual area VIP neurons. In the vast majority of neurons, the auditory and visual RFs largely overlapped. Additionally, neurons with well aligned visual and auditory receptive fields tended to encode multisensory space in a common reference frame. This suggests that area VIP constitutes a part of a neuronal circuit involved in the computation of a modality-invariant representation of external space.
Bat wings are highly adaptive airfoils that enable demanding flight maneuvers, which are performed with astonishing robustness under turbulent conditions, and stability at slow flight velocities. The ...bat wing is sparsely covered with microscopically small, sensory hairs that are associated with tactile receptors. In a previous study we demonstrated that bat wing hairs are involved in sensing airflow for improved flight maneuverability. Here, we report physical measurements of these hairs and their distribution on the wing surface of the big brown bat, Eptesicus fuscus, based on scanning electron microscopy analyses. The wing hairs are strongly tapered, and are found on both the dorsal and ventral wing surfaces. Laser scanning vibrometry tests of 43 hairs from twelve locations across the wing of the big brown bat revealed that their natural frequencies inversely correlate with length and range from 3.7 to 84.5 kHz. Young's modulus of the average wing hair was calculated at 4.4 GPa, which is comparable with rat whiskers or arthropod airflow-sensing hairs.
Bats are the only mammals capable of true powered flight. The bat wing exhibits specializations, allowing these animals to perform complicated flight maneuvers like landing upside-down, and hovering. ...The wing membrane contains various tactile receptors, including hair-associated Merkel receptors that might be involved in stabilizing bat flight. Here, we studied the neuronal representation of the wing membrane in the primary somatosensory cortex (S1) of the anesthetized Big Brown Bat,
Eptesicus fuscus
, using tactile stimulation with calibrated monofilaments (von Frey hairs) while recording from multi-neuron clusters. We also measured cortical response thresholds to tactile stimulation of the wings.The body surface is mapped topographically across the surface of S1, with the head, foot, and wing being overrepresented. The orientation of the wing representation is rotated compared to the hand representaion of terrestrial mammals, confirming results from other bat species. Although different wing membrane parts derive embryologically from different body parts, including the flank (plagiopatagium), the tactile sensitivity of the entire flight membrane (0.2–1.2 mN) is remarkably close or even higher (dactylopatagium) than the average tactile sensitivity of the human fingertip.
How do neurons in the inferior colliculus (IC) encode the spatial location of sound? We have addressed this question using a virtual auditory environment. For this purpose, the individual ...head-related transfer functions (HRTFs) of 18 guinea pigs were measured under free-field conditions for 122 locations covering the upper hemisphere. From 257 neurons, 94% responded to the short (50-ms) white noise stimulus at 70 dB sound pressure level (SPL). Out of these neurons, 80% were spatially tuned with a receptive field that is smaller than a hemifield (at 70 dB). The remainder responded omnidirectionally or showed fractured receptive fields. The majority of the neurons preferred directions in the contralateral hemisphere. However, preference for front or rear positions and high elevations occurred frequently. For stimulation at 70 dB SPL, the average diameter of the receptive fields, based on half-maximal response, was less than a quarter of the upper hemisphere. Neurons that preferred frontal directions responded weakly or showed no response to posterior directions and vice versa. Hence, front/back discrimination is present at the single-neuron level in the IC. When nonindividual HRTFs were used to create the stimuli, the spatial receptive fields of most neurons became larger, split into several parts, changed position, or the response became omnidirectional. Variation of absolute sound intensity had little effect on the preferred directions of the neurons over a range of 20 to 40 dB above threshold. With increasing intensity, most receptive fields remained constant or expanded. Furthermore, we tested the influence of binaural decorrelation and stimulus bandwidth on spatial tuning. The vast majority of neurons with a low characteristic frequency (<2.5 kHz) lost spatial tuning under stimulation with binaurally uncorrelated noise, whereas high-frequency units were mostly unaffected. Most neurons that showed spatial tuning under broadband stimulation (white noise and 1 octave wide noise) turned omnidirectional when stimulated with 1/3 octave wide noise.
A major cue for the localization of sound in space is the interaural time difference (ITD). We examined the role of inhibition in the shaping of ITD responses in the inferior colliculus (IC) by ...iontophoretically ejecting gamma-aminobutyric acid (GABA) antagonists and GABA itself using a multibarrel pipette. The GABA antagonists block inhibition, whereas the applied GABA provides a constant level of inhibition. The effects on ITD responses were evaluated before, during and after the application of the drugs. If GABA-mediated inhibition is involved in shaping ITD tuning in IC neurons, then applying additional amounts of this inhibitory transmitter should alter ITD tuning. Indeed, for almost all neurons tested, applying GABA reduced the firing rate and consequently sharpened ITD tuning. Conversely, blocking GABA-mediated inhibition increased the activity of IC neurons, often reduced the signal-to-noise ratio and often broadened ITD tuning. Blocking GABA could also alter the shape of the ITD function and shift its peak suggesting that the role of inhibition is multifaceted. These effects indicate that GABAergic inhibition at the level of the IC is important for ITD coding.
Sensory systems across the brain are specialized for their input, yet some principles of neural organization are conserved across modalities. The pattern of anatomical connections from the primate ...auditory cortex to the temporal, parietal, and prefrontal lobes suggests a possible division into dorsal and ventral auditory processing streams, with the dorsal stream originating from more caudal areas of the auditory cortex, and the ventral stream originating from more rostral areas. These streams are hypothesized to be analogous to the well-established dorsal and ventral streams of visual processing. In the visual system, the dorsal processing stream shows substantially faster neural response latencies than does the ventral stream. However, the relative timing of putative dorsal and ventral stream processing has yet to be explored in other sensory modalities. Here, we compare distributions of neural response latencies from 10 different areas of macaque auditory cortex, confirmed by individual anatomical reconstructions, to determine whether a similar timing advantage is found for the hypothesized dorsal auditory stream. Across three varieties of auditory stimuli (clicks, noise, and pure tones), we find that latencies increase with hierarchical level, as predicted by anatomical connectivity. Critically, we also find a pronounced timing differential along the caudal-to-rostral axis within the same hierarchical level, with caudal (dorsal stream) latencies being faster than rostral (ventral stream) latencies. This observed timing differential mirrors that found for the dorsal stream of the visual system, suggestive of a common timing advantage for the dorsal stream across sensory modalities.
Bronx waltzer mice lose a great proportion of their cochlear inner hair cells during early development. Hair cell counts revealed that these mice lacked on average 86% of their inner hair cells. ...Outer hair cells were present in a normal number, but appeared disarranged. The effect of this inner hair cell loss on the properties of central auditory neurons was investigated by recording neuronal responses in the inferior colliculus. Neuronal thresholds were on average elevated by 40 dB compared to CBA controls. The frequency tuning curves of the mutants were broad, and in part (18.5%) multi-peaked. The tonotopy found in the inferior colliculus of the Bronx waltzer mice appeared diffuse. Both the driven and spontaneous discharge rates were not statistically significantly different from the controls. However, the average first spike latency was significantly longer in the Bronx waltzer mice.
Flight maneuvers require rapid sensory integration to generate adaptive motor output. Bats achieve remarkable agility with modified forelimbs that serve as airfoils while retaining capacity for ...object manipulation. Wing sensory inputs provide behaviorally relevant information to guide flight; however, components of wing sensory-motor circuits have not been analyzed. Here, we elucidate the organization of wing innervation in an insectivore, the big brown bat, Eptesicus fuscus. We demonstrate that wing sensory innervation differs from other vertebrate forelimbs, revealing a peripheral basis for the atypical topographic organization reported for bat somatosensory nuclei. Furthermore, the wing is innervated by an unusual complement of sensory neurons poised to report airflow and touch. Finally, we report that cortical neurons encode tactile and airflow inputs with sparse activity patterns. Together, our findings identify neural substrates of somatosensation in the bat wing and imply that evolutionary pressures giving rise to mammalian flight led to unusual sensorimotor projections.
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•Segmental organization of wing innervation differs from known vertebrate forelimbs•The bat wing has an atypical dermatome map that can be explained by its ontogeny•Bat wings are equipped with an unusual repertoire of somatosensory receptors•Sparse cortical coding represents inputs from biological airflow and touch sensors
In bats, microscopic wing hairs provide sensory inputs to guide flight behaviors. Marshall et al. report the identities, distribution, and peripheral organization of sensory neurons that innervate bat wings. Electrophysiological recordings from primary somatosensory cortex reveal that tactile and airflow stimuli are represented centrally with a sparse temporal code.
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