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How the brain computes accurate estimates of our self-motion relative to the world and our orientation relative to gravity in order to ensure accurate perception and motor control is a fundamental neuroscientific question. Recent experiments have revealed that the vestibular system encodes this information during everyday activities using pathway-specific neural representations. Furthermore, new findings have established that vestibular signals are selectively combined with extravestibular information at the earliest stages of central vestibular processing in a manner that depends on the current behavioural goal. These findings have important implications for our understanding of the brain mechanisms that ensure accurate perception and behaviour during everyday activities and for our understanding of disorders of vestibular processing.In addition to ensuring stable gaze and posture, the vestibular system contributes to the perception of self-motion and orientation. In this Review, Cullen provides a comprehensive overview of recent advances in our understanding of sensory encoding and integration in the vestibular pathways.

Motor circuits develop in sequence from those governing fast movements to those governing slow. Here we examine whether upstream sensory circuits are organized by similar principles. Using serial-section electron microscopy in larval zebrafish, we generated a complete map of the gravity-sensing (utricular) system spanning from the inner ear to the brainstem. We find that both sensory tuning and developmental sequence are organizing principles of vestibular topography. Patterned rostrocaudal innervation from hair cells to afferents creates an anatomically inferred directional tuning map in the utricular ganglion, forming segregated pathways for rostral and caudal tilt. Furthermore, the mediolateral axis of the ganglion is linked to both developmental sequence and neuronal temporal dynamics. Early-born pathways carrying phasic information preferentially excite fast escape circuits, whereas later-born pathways carrying tonic signals excite slower postural and oculomotor circuits. These results demonstrate that vestibular circuits are organized by tuning direction and dynamics, aligning them with downstream motor circuits and behaviors. How sensory systems are organized during development remains unclear. Here, the authors used electron microscopy to examine the gravity-sensing system in zebrafish, finding that directional tuning and developmental age are organizing principles of the transformation from vestibular sensation to motor control.

Self-motion triggers complementary visual and vestibular reflexes supporting image-stabilization and balance. Translation through space produces one global pattern of retinal image motion (optic flow), rotation another. We examined the direction preferences of direction-sensitive ganglion cells (DSGCs) in flattened mouse retinas in vitro . Here we show that for each subtype of DSGC, direction preference varies topographically so as to align with specific translatory optic flow fields, creating a neural ensemble tuned for a specific direction of motion through space. Four cardinal translatory directions are represented, aligned with two axes of high adaptive relevance: the body and gravitational axes. One subtype maximizes its output when the mouse advances, others when it retreats, rises or falls. Two classes of DSGCs, namely, ON-DSGCs and ON-OFF-DSGCs, share the same spatial geometry but weight the four channels differently. Each subtype ensemble is also tuned for rotation. The relative activation of DSGC channels uniquely encodes every translation and rotation. Although retinal and vestibular systems both encode translatory and rotatory self-motion, their coordinate systems differ. Global mapping shows that mouse retinal neurons prefer visual motion produced when the animal moves along two behaviourally relevant axes, allowing the encoding of the animal’s every translation and rotation. All eyes on motion encoding The local wiring that allows some retinal neurons to detect motion direction in visual stimuli has been well studied, but how their ensemble encodes optic flow more generally has not. Now David Berson and colleagues have performed a global mapping of direction preferences in mouse direction-sensitive ganglion cells (DSGCs) and show that they align with just two ethologically relevant axes: the body axis and the gravitational axis. Relative activation of the sixteen resulting channels, that is four cardinal directions multiplied by two DSGC types (ON vs ON-OFF) for two eyes, allows for the unique encoding of every translation and rotation associated with the animal's self-motion. This creates a visual feedback that complements the bio-mechanical vestibular system in controlling image stabilization and balance.

Walking is a complex motor programme involving coordinated and distributed activity across the brain and the spinal cord. Halting appropriately at the correct time is a critical component of walking control. Despite progress in identifying neurons driving halting 1 – 6 , the underlying neural circuit mechanisms responsible for overruling the competing walking state remain unclear. Here, using connectome-informed models 7 – 9 and functional studies, we explain two fundamental mechanisms by which Drosophila implement context-appropriate halting. The first mechanism (‘walk-OFF’) relies on GABAergic neurons that inhibit specific descending walking commands in the brain, whereas the second mechanism (‘brake’) relies on excitatory cholinergic neurons in the nerve cord that lead to an active arrest of stepping movements. We show that two neurons that deploy the walk-OFF mechanism inhibit distinct populations of walking-promotion neurons, leading to differential halting of forward walking or turning. The brake neurons, by constrast, override all walking commands by simultaneously inhibiting descending walking-promotion neurons and increasing the resistance at the leg joints. We characterized two behavioural contexts in which the distinct halting mechanisms were used by the animal in a mutually exclusive manner: the walk-OFF mechanism was engaged for halting during feeding and the brake mechanism was engaged for halting and stability during grooming. Two halting mechanisms, ‘walk-OFF’ and ‘brake’, are shown to be engaged by distinct neural circuits in Drosophila , in a context dependent manner.

In tactile sensing, decoding the journey from afferent tactile signals to efferent motor commands is a significant challenge primarily due to the difficulty in capturing population-level afferent nerve signals during active touch. This study integrates a finite element hand model with a neural dynamic model by using microneurography data to predict neural responses based on contact biomechanics and membrane transduction dynamics. This research focuses specifically on tactile sensation and its direct translation into motor actions. Evaluations of muscle synergy during in -vivo experiments revealed transduction functions linking tactile signals and muscle activation. These functions suggest similar sensorimotor strategies for grasping influenced by object size and weight. The decoded transduction mechanism was validated by restoring human-like sensorimotor performance on a tendon-driven biomimetic hand. This research advances our understanding of translating tactile sensation into motor actions, offering valuable insights into prosthetic design, robotics, and the development of next-generation prosthetics with neuromorphic tactile feedback. The study explores the pathway from tactile signals to motor control using the integration of hand modeling and neural dynamics, enhancing understanding of sensorimotor mechanisms. These results aim to improve prosthetic design and robotic applications.

The precision of skilled movement depends on sensory feedback and its refinement by local inhibitory microcircuits. One specialized set of spinal GABAergic interneurons forms axo–axonic contacts with the central terminals of sensory afferents, exerting presynaptic inhibitory control over sensory–motor transmission. The inability to achieve selective access to the GABAergic neurons responsible for this unorthodox inhibitory mechanism has left unresolved the contribution of presynaptic inhibition to motor behaviour. We used Gad2 as a genetic entry point to manipulate the interneurons that contact sensory terminals, and show that activation of these interneurons in mice elicits the defining physiological characteristics of presynaptic inhibition. Selective genetic ablation of Gad2 -expressing interneurons severely perturbs goal-directed reaching movements, uncovering a pronounced and stereotypic forelimb motor oscillation, the core features of which are captured by modelling the consequences of sensory feedback at high gain. Our findings define the neural substrate of a genetically hardwired gain control system crucial for the smooth execution of movement. A population of spinal interneurons that form axo–axonic connections with the terminals of proprioceptive afferents are shown to mediate presynaptic inhibition; their ablation elicits harmonic oscillations during goal-directed forelimb movements, which can be modelled as the consequence of an increase in sensory feedback gain. How presynaptic inhibition ensures smooth limb movement Humans and other animals execute limb movements with a seemingly effortless precision that relies on sensory feedback and its refinement by inhibitory microcircuits. A new study identifies presynaptic inhibition in the spinal cord, a regulatory filter mediated by Gad2 -expressing GABAergic interneurons that form connections with the terminals of sensory afferents, as part of a hardwired gain control system crucial for the smooth execution of movement. Thomas Jessell and colleagues demonstrate that activation of Gad2 -expressing neurons inhibits neurotransmitter release from sensory afferents. Selective ablation of these neurons in mice causes pronounced oscillations during goal-directed forelimb reaching movements, a behaviour captured by a model of sensory feedback at high gain.

Land-walking vertebrates maintain a desirable posture by finely controlling muscles. It is unclear whether fish also finely control posture in the water. Here, we showed that larval zebrafish have fine posture control. When roll-tilted, fish recovered their upright posture using a reflex behavior, which was a slight body bend near the swim bladder. The vestibular-induced body bend produces a misalignment between gravity and buoyancy, generating a moment of force that recovers the upright posture. We identified the neural circuits for the reflex, including the vestibular nucleus (tangential nucleus) through reticulospinal neurons (neurons in the nucleus of the medial longitudinal fasciculus) to the spinal cord, and finally to the posterior hypaxial muscles, a special class of muscles near the swim bladder. These results suggest that fish maintain a dorsal-up posture by frequently performing the body bend reflex and demonstrate that the reticulospinal pathway plays a critical role in fine postural control. The postural control mechanism in fish is unclear. Here, authors show that larval zebrafish recover upright posture after roll tilts by a body bend that produces corrective rotational torque. They also reveal the associated neural circuits and muscles.

Accurate internal estimates of self-motion and orientation relative to gravity are fundamental for stabilizing gaze, controlling posture, and navigating through dynamic environments. Prevailing theories propose that the cerebellar nodulus and uvula (NU) employ internal models to suppress sensory input arising from predictable, self-generated motion. However, this assumption has never been directly tested. Here, we recorded NU Purkinje cell activity in rhesus monkeys during active and passive head movements. We found neurons responsive to passive translations remained equally sensitive to self-generated movements, encoding net head motion in space irrespective of its source. Furthermore, external perturbation did not influence these ground-truth encoding. When active head motion was blocked, Purkinje cell activity remained unchanged – demonstrating a lack of efference copy integration. During active tilts, NU neurons encoded both dynamic motion and static orientation relative to gravity. These findings challenge the internal model hypothesis and establish the NU as a ground-truth, context-invariant estimator of self-motion, supporting stable behavior in dynamic environments. How the brain meets these competing demands–and where such a veridical “ground-truth” representation is computed–remains unknown. Here authors show that the cerebellar nodulus/uvula–a region essential for postural control–provides a stable, ground-truth representation of self-motion during voluntary movement, rather than suppressing self-generated signals.