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The inner ear, which mediates the senses of hearing and balance, derives from a simple ectodermal vesicle in the vertebrate embryo. In the zebrafish, the otic placode and vesicle express a whole suite of genes required for ciliogenesis and ciliary motility. Every cell of the otic epithelium is ciliated at early stages; at least three different ciliary subtypes can be distinguished on the basis of length, motility, genetic requirements and function. In the early otic vesicle, most cilia are short and immotile. Long, immotile kinocilia on the first sensory hair cells tether the otoliths, biomineralized aggregates of calcium carbonate and protein. Small numbers of motile cilia at the poles of the otic vesicle contribute to the accuracy of otolith tethering, but neither the presence of cilia nor ciliary motility is absolutely required for this process. Instead, otolith tethering is dependent on the presence of hair cells and the function of the glycoprotein Otogelin. Otic cilia or ciliary proteins also mediate sensitivity to ototoxins and coordinate responses to extracellular signals. Other studies are beginning to unravel the role of ciliary proteins in cellular compartments other than the kinocilium, where they are important for the integrity and survival of the sensory hair cell. This article is part of the Theo Murphy meeting issue ‘Unity and diversity of cilia in locomotion and transport’.

Sensory hair cells are specialized secondary sensory cells that mediate our senses of hearing, balance, linear acceleration, and angular acceleration (head rotation). In addition, hair cells in fish and amphibians mediate sensitivity to water movement through the lateral line system, and closely related electroreceptive cells mediate sensitivity to lowvoltage electric fields in the aquatic environment of many fish species and several species of amphibian. Sensory hair cells share many structural and functional features across all vertebrate groups, while at the same time they are specialized for employment in a wide variety of sensory tasks. The complexity of hair cell structure is large, and the diversity of hair cell applications in sensory systems exceeds that seen for most, if not all, sensory cell types. The intent of this review is to summarize the more significant structural features and some of the more interesting and important physiological mechanisms that have been elucidated thus far. Outside vertebrates, hair cells are only known to exist in the coronal organ of tunicates. Electrical resonance, electromotility, and their exquisite mechanical sensitivity all contribute to the attractiveness of hair cells as a research subject.

Increases in water temperature due to global climate change are known to alter the course and timing of fish development. The mechanosensory lateral line (LL) system mediates flow-sensing behaviors vital for survival in fishes, but the effects of increased water temperatures resulting from climate change on its development have not been examined. Here LL development was documented in a cold-water salmonid (brook trout, Salvelinus fontinalis ) reared at the thermograph of a long-term study stream (ambient) and two higher temperatures (+ 2 and + 4 °C) that reflect projected increases within their native range. At these two higher temperatures, fish reach crucial early life history transitions earlier (e.g., hatch, “swim-up” from gravel nests into the water column) and are larger in size through the parr (juvenile) stage. Early forming canal neuromast receptor organs are larger, and the process of canal morphogenesis is also accelerated suggesting potential consequences for neuromast function and presumably for LL-mediated behaviors. A potential mismatch between the timing of transitions in early life history stages, the ability to carry out LL-mediated behaviors (e.g., prey detection), and the timing of the seasonal emergence of their preferred prey, could have serious implications for cold-water salmonid ecology and survival.

The mechanosensory (lateral line) and electrosensory systems are two important non-visual sensory modalities, especially in low light environments. Despite their importance, these sensory systems have received little attention in deepwater chondrichthyans. Here, we describe the morphological organisation of the peripheral lateral line and electrosensory systems in two species of chimaeras; the pale ghost shark Hydrolagus bemisi (Chimaeridae) and the Australasia narrow-nosed spookfish Harriotta avia (Rhinochimaeridae), occupying depth ranges of 400–1,100 m and 260–1,278 m, respectively. Using topographic mapping, computed tomography, histology, and scanning electron microscopy, the distribution, abundance, size, and microstructure of lateral line grooves and organs (neuromasts), and ampullary organs (pores, canals, and bulbs) are described. The arrangement of the peripheral sense organs in both these systems may reflect comparable feeding strategies for detecting benthic prey. While the elongated rostrum of Harriotta avia is likely used as a sensory probe, providing spatially-resolved information about minute hydrodynamic disturbances and electric fields of potential prey beneath the animal, the arrangement of sense organs in Hydrolagus bemisi indicates that this species may rely less on electroreception. The study compares the morphology and provides information on the relative importance of two (non-visual) sensory modalities in two demersal holocephalans that remain vulnerable to anthropogenic disturbances.

With the mechanosensory lateral line system, fish and semi-aquatic amphibians detect water movements and pressure gradients. Hydrodynamic information picked up by the lateral line receptors is relayed via peripheral nerves to the lateral line brainstem and from there to the midbrain torus semicircularis. Most prior electrophysiological studies of the lateral line were done under still-water conditions, even though natural environments encountered by fish include bulk-flow. Flow velocity and direction sensing are likely important to fish as they navigate variable, turbulent environments, but to date, only few studies have gathered information on the processing of bulk water flow by midbrain units. Here, we recorded from lateral line units in the torus semicircularis while presenting various bulk flow velocities in anterior-to-posterior and posterior-to-anterior flow directions. We studied (1) the temporal spike patterns of mechanosensory midbrain units, (2) the processing of bulk water flow velocity by these units, and (3) the processing of bulk water flow direction. We found that midbrain mechanosensory units alter their discharge rate during bulk water flow – some units responded to flow by increasing their discharge rate but did not vary this rate significantly with flow velocity, while others exhibited increasing discharge rates with increasing flow velocity. Units directly coding for flow direction were not found.

Detection of water motion by the lateral line relies on mechanotransduction complexes at stereocilia tips. This sensory system is comprised of neuromasts, patches of hair cells with stereociliary bundles arranged with morphological mirror symmetry that are mechanically responsive to two opposing directions. Here, we find that transmembrane channel-like 2b (Tmc2b) is differentially required for mechanotransduction in the zebrafish lateral line. Despite similarities in neuromast hair cell morphology, three classes of these cells can be distinguished by their Tmc2b reliance. We map mechanosensitivity along the lateral line using imaging and electrophysiology to determine that a hair cell’s Tmc2b dependence is governed by neuromast topological position and hair bundle orientation. Overall, water flow is detected by molecular machinery that can vary between hair cells of different neuromasts. Moreover, hair cells within the same neuromast can break morphologic symmetry of the sensory organ at the stereocilia tips.  In fish, water motion is detected by mechanosensitive hair cells located in the lateral line. Here the authors show that the molecular machinery for mechanotransduction, including transmembrane channel-like 2b (Tmc2b), varies depending on both hair cell location and hair bundle orientation.

Otolith organs in the inner ear and neuromasts in the fish lateral-line harbor two populations of hair cells oriented to detect stimuli in opposing directions. The underlying mechanism is highly conserved: the transcription factor EMX2 is regionally expressed in just one hair cell population and acts through the receptor GPR156 to reverse cell orientation relative to the other population. In mouse and zebrafish, loss of Emx2 results in sensory organs that harbor only one hair cell orientation and are not innervated properly. In zebrafish, Emx2 also confers hair cells with reduced mechanosensory properties. Here, we leverage mouse and zebrafish models lacking GPR156 to determine how detecting stimuli of opposing directions serves vestibular function, and whether GPR156 has other roles besides orienting hair cells. We find that otolith organs in Gpr156 mouse mutants have normal zonal organization and normal type I-II hair cell distribution and mechano-electrical transduction properties. In contrast, gpr156 zebrafish mutants lack the smaller mechanically evoked signals that characterize Emx2-positive hair cells. Loss of GPR156 does not affect orientation-selectivity of afferents in mouse utricle or zebrafish neuromasts. Consistent with normal otolith organ anatomy and afferent selectivity, Gpr156 mutant mice do not show overt vestibular dysfunction. Instead, performance on two tests that engage otolith organs is significantly altered – swimming and off-vertical-axis rotation. We conclude that GPR156 relays hair cell orientation and transduction information downstream of EMX2, but not selectivity for direction-specific afferents. These results clarify how molecular mechanisms that confer bi-directionality to sensory organs contribute to function, from single hair cell physiology to animal behavior.

Animals modulate sensory processing in concert with motor actions. Parallel copies of motor signals, called corollary discharge (CD), prepare the nervous system to process the mixture of externally and self-generated (reafferent) feedback that arises during locomotion. Commonly, CD in the peripheral nervous system cancels reafference to protect sensors and the central nervous system from being fatigued and overwhelmed by self-generated feedback. However, cancellation also limits the feedback that contributes to an animal’s awareness of its body position and motion within the environment, the sense of proprioception. We propose that, rather than cancellation, CD to the fish lateral line organ restructures reafference to maximize proprioceptive information content. Fishes’ undulatory body motions induce reafferent feedback that can encode the body’s instantaneous configuration with respect to fluid flows. We combined experimental and computational analyses of swimming biomechanics and hair cell physiology to develop a neuromechanical model of how fish can track peak body curvature, a key signature of axial undulatory locomotion. Without CD, this computation would be challenged by sensory adaptation, typified by decaying sensitivity and phase distortions with respect to an input stimulus. We find that CD interacts synergistically with sensor polarization to sharpen sensitivity along sensors’ preferred axes. The sharpening of sensitivity regulates spiking to a narrow interval coinciding with peak reafferent stimulation, which prevents adaptation and homogenizes the otherwise variable sensor output. Our integrative model reveals a vital role of CD for ensuring precise proprioceptive feedback during undulatory locomotion, which we term external proprioception.

The artificial lateral line system, composed of velocity and pressure sensors, is the sensing system for fish-like robots by mimicking the lateral line system of aquatic organisms. However, accurately estimating the self-motion of the fish-like robot remains challenging due to the complex flow field generated by its movement. In this study, we employ the mode decomposition method to estimate the motion states based on artificial lateral lines for the fish-like robot. We find that primary decomposed modes are strongly correlated with the velocity components and can be interpreted through Lighthill’s theoretical pressure model. Moreover, our decomposition analysis indicates the redundancy of the sensor array design, which is verified by further synthetic analysis and explained by flow visualization. Finally, we demonstrate the generalizability of our method by accurately estimating the self-states of the fish-like robot under varying oscillation parameters, analyzing three-dimensional pressure data from the computational fluid dynamics simulations of boxfish ( Ostracion cubicus ) and eel-like ( Anguilla anguilla ) models, and robustly estimating the self-velocity in complex flows with vortices caused by a neighboring robot. Our interpretable and generalizable data-driven pipeline could be beneficial in generating hydrodynamic sensing hypotheses in biofluids and enhancing artificial-lateral-line-based perception in autonomous underwater robotics. Accurately estimating the self-motion of fish-like robots in complex environments remains a challenge for current sensing systems based on artificial lateral lines. Here, authors employ a mode decomposition method to estimate the motion states of the robot, enhancing the sensing capabilities of fish-like robotic systems.

During active movements, neural replicas of the underlying motor commands may assist in adapting motion-detecting sensory systems to an animal’s own behaviour. The transmission of such motor efference copies to the mechanosensory periphery offers a potential predictive substrate for diminishing sensory responsiveness to self-motion during vertebrate locomotion. Here, using semi-isolated in vitro preparations of larval Xenopus , we demonstrate that shared efferent neural pathways to hair cells of vestibular endorgans and lateral line neuromasts express cyclic impulse bursts during swimming that are directly driven by spinal locomotor circuitry. Despite common efferent innervation and discharge patterns, afferent signal encoding at the two mechanosensory peripheries is influenced differentially by efference copy signals, reflecting the different organization of body/water motion-detecting processes in the vestibular and lateral line systems. The resultant overall gain reduction in sensory signal encoding in both cases, which likely prevents overstimulation, constitutes an adjustment to increased stimulus magnitudes during locomotion. Corollary discharges inform the central nervous system about impending motor activity. Here, Chagnaud et al . show that, in Xenopus tadpoles, shared efferent neural pathways to the inner ear and lateral line adjust the sensitivity of sensory afferents during locomotor activity.