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HOME > Res Vestib Sci > Volume 24(3); 2025 > Article
Review Article
The vestibular system and the encoding of self-motion: from basic science to clinical applications
Kathleen E. Cullen1,2,3,4orcid
Research in Vestibular Science 2025;24(3):117-138.
DOI: https://doi.org/10.21790/rvs.2025.008
Published online: September 15, 2025

1Department of Biomedical Engineering, Whiting School of Engineering and School of Medicine, Johns Hopkins University, Baltimore, MD, USA

2Department of Otolaryngology, School of Medicine, Johns Hopkins University, Baltimore, MD, USA

3Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, USA

4Kavli Neuroscience Discovery Institute, Johns Hopkins University, Baltimore, MD, USA

Corresponding author: Kathleen E. Cullen Department of Biomedical Engineering, Whiting School of Engineering and School of Medicine, Johns Hopkins University, Rm. 720, Ross Building, 720 Rutland Ave., Baltimore, MD 21205, USA. E-mail: Kathleen.Cullen@jhu.edu
• Received: March 15, 2025   • Revised: April 24, 2025   • Accepted: May 7, 2025

© 2025 The Korean Balance Society

This is an open access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • The vestibular system plays a fundamental role in stabilizing gaze, maintaining balance, and providing spatial orientation by encoding head motion in all 6 degrees of freedom. At the earliest stages of central processing, it integrates multimodal signals from proprioceptive, oculomotor, and predictive pathways, allowing for dynamic motor control and adaptive compensation for sensory deficits. This review examines the neural coding strategies underlying vestibular processing, with a focus on how the vestibular system encodes self-motion and contributes to multisensory integration and motor control. While traditional linear models have provided valuable insights into afferent response properties, these neural pathways encode head motion in a context-dependent manner, such that vestibular reflex pathways are suppressed during active behaviors. The vestibulocerebellum plays a crucial role in modulating vestibular reflexes through predictive mechanisms and experience-dependent plasticity, enabling accurate motor control as well as adaptation following vestibular injury or dysfunction. Beyond reflexive control, vestibular pathways also contribute to higher-order voluntary behaviors such as reaching, steering, and spatial navigation, integrating with cognitive and motor systems. Finally, this review explores the clinical implications of vestibular dysfunction in aging and neurodegenerative diseases, along with emerging vestibular prostheses that leverage neuroengineering advances to restore lost function. These innovations hold great promise for improving sensory encoding and rehabilitation strategies, offering new hope for individuals with balance and spatial orientation impairments.
  • Keywords: Vestibular system; Gaze stabilization; Postural balance; Spatial orientation; Compensation and redress; Multimodal integration
The vestibular system is essential for stabilizing gaze, maintaining posture, and enabling a sense of movement and spatial orientation. This sensory system detects and encodes head motion in all six dimensions (i.e., three axes of rotation and three axes of linear acceleration) to effectively represent the full movement of the head relative to space. It achieves this using two distinct types of sensory organs: the semicircular canals and otoliths (Fig. 1A).
The three semicircular canals (horizontal, anterior, and posterior) are arranged orthogonally, thereby providing sensory feedback about rotational head movements in three dimensions. In contrast, the otolith organs (utricle and saccule) detect linear acceleration and therefore provide sensory information about the direction and magnitude of gravity, as well as transient accelerations due to movement. The geometry of receptor cells within their neuroepithelia differentiates the function of the utricle and saccule: the utricle is sensitive to horizontal linear motion, while the saccule responds to vertical linear motion. Together, these five sensory organs provide complete feedback regarding the head’s orientation and movement relative to space during our everyday activities. Individual afferents within the vestibulocochlear nerve (cranial nerve VIII) then transmit sensory information from a single semicircular canal or otoliths to the vestibular nuclei in the brainstem. In turn, neurons in the vestibular nuclei comprise the first central stage of the vestibular pathways that ensure stable gaze, the maintenance of balance and posture, support voluntary movements, and facilitate navigation (Fig. 1B).
This review examines how vestibular pathways encode self-motion information to achieve essential functions and explores the implications for clinical practice. A distinguishing feature of vestibular processing is the early and extensive integration of multimodal inputs within the vestibular nuclei, where afferent signals from the inner ear are combined with proprioceptive, oculomotor, and predictive inputs from the brainstem, cerebellum, and cortex. This integration enables adaptive motor control, allowing for dynamic reflex modulation during voluntary actions and compensation for vestibular deficits. Advances in our understanding of central vestibular processing have provided key insights into both normal function and the mechanisms underlying clinical impairments, informing emerging rehabilitation and neuroengineering approaches.
Vestibular reflex pathways are vital for survival, as they ensure stable vision during head movements through the vestibuloocular reflex (VOR) and maintain balance and posture via vestibulospinal reflexes (VSRs), forming the foundation for all coordinated and adaptive motor behaviors. Traditional approaches to understanding vestibular motor reflex pathways have relied heavily on linear systems analysis [1,2]. In this approach, sinusoidal head motion is applied, firing rates are measured, and neural response gains and phases are then computed for different frequencies of stimulation. The application of linear systems analysis to individual semicircular canal and otolith afferents (Fig. 2A) has revealed that vestibular afferent response gains increase as a function of frequency—a characteristic referred to as high-pass tuning (Fig. 2A, top right panel). Likewise, afferent response phases increase as a function of frequency (Fig. 2A, bottom right panel). Overall, irregular afferents are significantly more sensitive to motion than regular afferents, showing up to 10 times greater response gains in the otolith system at higher frequencies [3,4]. In addition, irregular afferents are more dynamic, producing responses that increasingly lead to rotational and linear head motion as the frequency of movement increases.
Neurons in the vestibular nuclei integrate inputs from both regular and irregular afferents [5]. This integration is essential for coding multidimensional natural head movements, which simultaneously activate semicircular canal and otolith afferents [6-10]. Vestibular nuclei neurons fall into two functional subclasses: (1) VOR neurons and (2) vestibular-only (VO) neurons. VOR neurons include position-vestibular-pause (PVP) neurons and floccular target neurons (FTNs), which as discussed in more detail in the section below mediate and modulate the VOR, ensuring gaze stability during head motion [11,12]. In contrast, VO neurons do not participate in VOR pathways but instead project (i) to the spinal cord, controlling posture and balance via VSR [13] and (ii) to neurons within the ventral posterolateral area of the thalamus that in turn project to vestibular cortical area (reviewed in [14,15]). This latter pathway underlies the generation of the representations of self-motion and spatial orientation that are required for accurately coordinating perception and voluntary action (reviewed in [16]).
Regular afferents primarily drive VOR neurons (i.e., PVPs and FTNs) to stabilize gaze, whereas irregular afferents predominantly drive VO neurons to generate robust postural responses. The application of linear systems analysis to vestibular nuclei neurons has demonstrated that both PVP and VO neurons exhibit high-pass gain tuning and phase leads that increase with frequency, consistent with their afferent input. In the case of PVPs, their neural tuning is required to ensure that the VOR remains compensatory across the frequency range of natural head motion [17]. In the case of VO neurons, their neural tuning helps to overcome the high inertia of the body to generate rapid postural corrections [18,19].
Importantly, however, linear systems analysis has limitations for understanding vestibular processing during natural head movements, which often exceed the relatively low-intensity stimuli used in laboratory settings. Rotational and linear head movements during daily activities can reach intensities up to 15,000°/sec and 8× g, respectively, and include significant power at frequencies up to 20 Hz (Fig. 2B) [8]. Recent studies have shown that neural coding is optimized to account for the statistics of these natural movements [20-23].
During high intensity motion, vestibular afferent and vestibular nuclei neuron responses display nonlinearities such as saturation and rectification, which can be approximated by a sigmoid (Fig. 2C) [24-26]. As a result, afferent responses to head motion are best represented using linear-nonlinear (LN) cascade models [23,27]. These models use a linear filter to characterize a neuron’s response within its linear range and a nonlinear function (e.g., sigmoid) to account for saturation and rectification. LN models have been instrumental in developing vestibular prosthetics for patients with bilateral vestibular loss (BVL), enabling more accurate neural stimulation and compensatory motor responses (reviewed in [27]). Additionally, irregular afferents and VO neurons also encode head motion using precise spike timing, allowing for discrimination of motion waveforms with millisecond precision (Fig. 2D) [4,28]. This timing-based coding likely further supports transient compensatory behaviors, particularly in vestibulospinal pathways. Specifically, precise spike timing at the single neuron level likely induces greater synchrony at the VO population level that in turn better compensates for the inertia of the head-neck system (reviewed in [2]).
The VOR is an essential sensorimotor reflex that stabilizes gaze during the head movements made by generating compensatory eye movements opposite in direction to the head’s motion. This reflex allows the visual axis of gaze to remain stable relative to the world, ensuring clear vision during dynamic activities. Without the VOR, even simple actions like walking or running would blur the visual field due to retinal image motion induced by head movements.
The rotational VOR compensates for rotational head movements and is primarily mediated by a simple yet highly efficient three-neuron pathway (Fig. 3A). This pathway includes projections from the vestibular afferents to vestibular nuclei neurons, which in turn project to the extraocular motoneurons that drive the eye muscles (reviewed in [29]). Due to the direct nature of this pathway, the VOR exhibits an extraordinarily short latency of 5–6 msec [17]. This minimal delay is a result of the summation of fixed synaptic and neural transmission times, as well as the activation time of extraocular muscles.
When the head rotates, the rotational VOR generates compensatory eye movements in the opposite direction via a push-pull mechanism across the semicircular canals. For example, a leftward head rotation excites afferents from the left horizontal semicircular canal, which activate PVP neurons in the left vestibular nucleus. These neurons cross the midline to stimulate motoneurons driving the right lateral rectus muscle, producing a rightward compensatory eye movement. Simultaneously, inhibition suppresses antagonist muscles (Fig. 3A). These smooth, reflexive movements, known as the VOR slow phase, stabilize gaze by countering head rotation. When the eyes reach eccentric orbital positions, reflexive VOR quick phases reset them in the direction of head motion, preventing orbital limit. During sustained head motion, alternating slow and quick phases create the characteristic sawtooth pattern of nystagmus (Fig. 3B).
The rotational VOR provides robust compensation across a broad range of head rotation frequencies (about 0.1 to 25 Hz) and velocities (up to 500°/sec), typical of everyday activities [8,17]. This capability arises from the high-pass tuning of vestibular afferents and central VOR neurons, which ensures phase compensation at higher frequencies, maintaining eye-head synchronization despite the VOR’s fixed 5-msec latency. However, for very low-frequency head movements (<0.1 Hz), the rotational VOR is less effective. Instead, the optokinetic reflex (OKR), driven by visual motion, plays a complementary role. While the OKR has a longer latency (about 50 msec), it works in tandem with the VOR to stabilize gaze across the full range of natural head movements (reviewed in [29]). Together with the rotational VOR, the translational VOR also helps to compensate for linear head movements such as side-to-side, forward-backward, or up-down motions. These movements require the eyes to adjust for parallax effects, scaling their response based on the distance of the visual target. Unlike the rotational VOR, the translational VOR has a longer latency (>10 msec) and is mediated by more complex polysynaptic pathways, making it less effective at stabilizing gaze during rapid translational motions (reviewed in [29]).
While essential for stabilizing gaze during most activities, the efficacy of VOR pathways is modulated in real time in a context-dependent manner. Specifically, the VOR is actively suppressed when our current goal is to redirect our gaze using head (as well as eye) movements rather than stabilize gaze. Since gaze = eye in orbit and head-in-space, this suppression of the VOR effectively prevents the generation of compensatory eye movements that would be counterproductive (in the opposite direction) to the current goal of redirecting gaze. Single-unit recording experiments in monkeys have revealed that this suppression occurs at the level of the PVP neurons within the vestibular nuclei, and is mediated by inhibitory inputs from the brainstem premotor saccadic circuitry (Fig. 3C, solid red line) [30,31]. Furthermore, VOR pathway suppression is most pronounced at the onset of a gaze shift, with the VOR gradually recovering by the end of the movement [32]. A similar mechanism suppresses the VOR during smooth pursuit of moving targets, enabling the eyes to track the target without interference from head motion [33].
Clinical Implications: Nystagmus
Nystagmus is a normal subclass of eye movements as described above, but pathological forms impair visual stability, balance, and motor control (reviewed in [34]). Pathological nystagmus can result from abnormalities in the peripheral or central vestibular pathways. While congenital forms, such as those linked to albinism or early-onset esotropia, arise from disrupted visual development, acquired nystagmus typically signals dysfunction in the vestibular periphery or central pathways due to trauma, disease, or drug toxicity.
Acute unilateral vestibular loss produces nystagmus due to imbalanced vestibular input that typically resolves within weeks via central compensation. In contrast, cerebellar and vestibular brainstem dysfunction can lead to forms of persistent nystagmus, such as periodic alternating nystagmus (PAN) or downbeat nystagmus. PAN, a jerk nystagmus, reverses direction approximately every 2 minutes and likely reflects cerebellar compensation for central vestibular imbalance. Downbeat nystagmus, also a jerk nystagmus linked to cerebellar dysfunction, is characterized by an upward drift of the eyes after a downward saccade.
The VSR plays an essential role in maintaining balance and postural stability by coordinating the activation of neck, trunk, and limb muscles in response to vestibular input. These reflexes are mediated by two main descending pathways (Fig. 4A): the medial vestibulospinal tract, which primarily targets the cervical spinal cord to stabilize the head, and the lateral vestibulospinal tract, which projects to lower spinal levels to control the torso and limbs. The vestibulocollic reflex (VCR), a specialized subset of VSR, operates through a combination of direct (three-neuron arc) and indirect pathways involving spinal interneurons and reticulospinal projections [35], effectively activating the neck muscles to stabilize the head in space in response to vestibular input [36]. Studies applying noninvasive electrical activation of the vestibular afferents via galvanic vestibular stimulation (GVS) have shown that the VCR generates head stabilizing commands for high-frequency stimulation up to 70–80 Hz [37].
Recent work has advanced our understanding of the VCR pathway’s functional role by directly measuring single motor unit responses in primate neck muscles during rapid yaw rotations. This study revealed robust vestibular-driven activity patterns at frequencies up to 20 Hz [36], showing that neck motor unit responses increased with frequency in normal animals but were entirely absent following bilateral peripheral vestibular loss. Additionally, autonomic arousal, quantified via pupil size, further enhanced these vestibular-evoked responses, highlighting the integration of autonomic and vestibular inputs in stabilizing head posture. Together, these findings underscore the essential role of vestibular inputs in driving the VCR across the frequency range encountered in daily life. During locomotion, the VCR compensates for head pitch and vertical displacements caused by stride dynamics [38,39]. Both VCR and VSR pathways generate postural adjustments by integrating vestibular signals with proprioceptive feedback. For instance, GVS elicits rapid electromyographic responses in limb muscles, modulated by head-body alignment and the direction and intensity of the vestibular disturbance [40,41].
While the VSR pathways are essential for generating compensatory postural responses to maintain balance, such as reacting to a sudden slip on ice, their modulation is suppressed when the primary goal is movement rather than stability. This suppression occurs because, during voluntary actions like walking or reaching, activating stabilizing reflexes would interfere with intentional movement, making them counterproductive. Single-unit recordings in monkeys have shown that this suppression occurs at the level of the VO neurons within the vestibular nuclei (Fig. 4B). In contrast, vestibular afferents encode both active and unexpected head motion similarly [42-46].
Importantly, the response of VO neurons in the vestibular nuclei is suppressed for head motion comprising rotations [47,48], translations [6], static changes in head orientations [49], as well as multidimensional head movements [7]. Moreover, VO neurons selectively encode passive self-motion even when concurrent with active motion, demonstrating specificity in gating by active motion signals [47,50]. Thus, when active and unexpected head movements occur simultaneously, suppression is specific to vestibular ‘reafference’—the self-generated component of head motion—while neurons continue to respond to vestibular ‘exafference,’ which originates from externally imposed motion or environmental forces. Recent studies have further established that reafferent cancellation suppresses actively generated vestibular input only when the sensory signal aligns with the brain’s internal estimate of expected movement consequences [50,51] (reviewed in [52,53]). As is reviewed in more detail below, the suppression of vestibular feedback during self-generated movements is mediated by inhibitory inputs from the cerebellum [54].
Clinical Implications: Assessing Otolith Function via Vestibular-Evoked Myogenic Potentials and Vestibular Sensory-Evoked Potentials
Semicircular canal function is typically clinically assessed by measuring compensatory VOR eye movements evoked by head rotation. A widely used test for detecting canal dysfunction is the videography head impulse test, which evaluates compensatory eye movements during brief, high-acceleration head rotations (reviewed in [34]). In contrast, to assess otolith function, vestibular-evoked myogenic potentials (VEMPs) have become a popular clinical test. VEMPs are short-latency electromyographic responses to transient acoustic stimuli, comprising two main types: (i) cervical VEMPs (cVEMPs) and (i) ocular VEMPs (oVEMPs). cVEMPs, recorded from the ipsilateral sternocleidomastoid muscle, are mediated by the VCR reflex pathway and thought to primarily reflect saccular function. On the other hand, oVEMPs, recorded via surface electromyographic electrodes under the contralateral eye, are mediated by the VOR pathway and thought to primarily reflect utricular function. (reviewed in [55,56]).
Additionally, vestibular sensory-evoked potentials (VsEPs) have become a key tool for assessing vestibular function in genetic rodent models such as knockout mice (reviewed in [57]). Evoked by repetitive transient linear acceleration, they are thought to elicit synchronized firing of irregular otolith afferents [58-60], which as reviewed above are highly motion-sensitive and encode dynamic stimuli via precise spike timing. In response to high-frequency stimuli, irregular afferent modulation leads to acceleration, effectively encoding its derivative—jerk. Consequently, VsEP intensity is proportional to jerk magnitude [61]. VsEPs have the potential to serve as a valuable clinical diagnostic tool, but their success will be dependent on the development of patient-adapted protocols.
Clinical Implications: Galvanic Vestibular Stimulation
GVS is a noninvasive method used in humans to activate vestibular afferents via surface electrodes placed behind the ears. In experimental studies, GVS has been used to probe vestibular contributions to postural control and self-motion perception (reviewed in [62]). Studies in rhesus monkeys (Fig. 5A) have shown that GVS equally activates both semicircular canal and otolith afferents [37,63,64]. Irregular afferents from both classes of sensory organs show greater sensitivity to GVS than regular afferents, with response gains increasing with frequency, though less than for natural motion (Fig. 5B, solid lines compare with dashed lines). GVS activates vestibulospinal pathways, including the VCR reflex, which stabilizes head position. In macaques, high-frequency up to 300 GVS evokes robust VCR responses Hz, peaking at 70–80 Hz, suggesting a significant role in head stabilization across a wide motion range [37].
Research and clinical applications have generally used three main types of stimulation waveforms: sinusoids, current steps, and stochastic (noisy) GVS (Fig. 5C). Afferent responses to GVS current steps exhibit pronounced asymmetries, with cathodal currents eliciting stronger responses than anodal currents (Fig. 5C, middle panel) that are evident in the evoked eye movement responses [63]. Noisy GVS (Fig. 5C, right panel), preferred for its comfort and efficiency, is now commonly applied in humans in an effort to improve the balance (reviewed in [62]). To date, however, its success, as well as the mechanisms underlying any potential improvement, remain debated [65-67]. Human imaging studies have further shown that afferent stimulation via GVS activates key vestibular processing areas, including the cerebellum, thalamus, and cortical regions (reviewed in [62]). Notably, in patients with bilateral vestibulopathy, GVS enhances resting-state activity in vestibular cortical areas, correlating with improved balance (Fig. 2A) [68,69].
Throughout life, the VOR exhibits remarkable adaptability—also termed motor learning-allowing it to adjust to changes in visual and vestibular inputs. For example, the VOR can recalibrate to compensate for altered visual input caused by corrective lenses (e.g., for myopia) or prism glasses. In a striking demonstration of this adaptability, studies with participants wearing dove prisms that inverted their visual field showed that the VOR gain could reverse direction following prolonged adaptation over time [70]. As discussed in the section below on the cerebellum, this adaptability of the VOR depends on plasticity within the floccular complex, which modulates its gain by adjusting Purkinje cell responses to vestibular and visual inputs (reviewed in [12]). Similarly, VCR/VSR pathways, like the VOR, exhibit remarkable plasticity throughout life, enabling adaptation to changing environmental conditions. This adaptability relies on plasticity within the anterior vermis, which fine-tunes Purkinje cell responses based on postural error signals.
Following unilateral peripheral vestibular loss, the VOR and VCR/VSR undergo partial recovery as a result of central compensation mechanisms in the brainstem. First, the commissural vestibular system, which connects the vestibular nuclei on both sides of the brainstem via reciprocal inhibitory pathways [71,72], plays a key role in restoring function. These reciprocal pathways rebalance the synaptic weights of inhibitory inputs, compensating for the asymmetry created by the loss of vestibular input from one side. This mechanism facilitates the rapid recalibration of firing rates in the vestibular nuclei within days of injury [73,74], though compensation is constrained by parallel increases in neural variability, leading to reduced signal-to-noise ratios [75].
Second, vestibular nuclei neurons also exhibit responses to extra-vestibular inputs that are not present before the lesion, specifically to proprioceptive and motor-related inputs (reviewed in [76,77]). Within 24 hours of peripheral vestibular loss, proprioceptive inputs are unmasked in both the VOR and vestibulospinal pathways [73,74]. This sensory substitution, mediated by homeostatic plasticity within the vestibular nuclei, enables neurons to integrate congruent feedback from the body’s musculature during self-motion, compensating for reduced vestibular reliability. Over the following month, motor-related inputs are then similarly unmasked [73,74,78], further enhancing VOR and vestibulospinal pathway performance. Notably, these extra-vestibular inputs not only aid recovery but also improve coding precision and reflex response gains [46,75].
Additionally, the floccular lobe and anterior vermis of the cerebellum contribute to the long-term recalibration of VOR and VCR/VSR pathways, promoting gradual recovery (reviewed in [76,79]). However, while these compensation mechanisms are impressive, they remain incomplete. For instance, while VOR responses to lower-frequency head movements improve over weeks, those to high-frequency and high-velocity head movements often remain impaired, highlighting the challenges of fully restoring VOR function [80,81]. In addition, the loss of peripheral vestibular input alters the movement strategies of patients during walking as well as orienting and dynamic balance tasks [82-85].
The vestibular cerebellum is an essential hub for integrating sensory inputs to fine-tune motor responses required for balance, gaze stability, and postural control. It processes vestibular and extra-vestibular self-motion cues (proprioceptive, visual, and motor signals) to compute internal models for motor coordination. Three major cerebellar regions process vestibular input—the floccular complex, anterior vermis, and nodulus/ventral uvula (Fig. 6A)—each playing a distinct role in maintaining stability and orientation (reviewed in [86]). The floccular lobe integrates vestibular and visual signals to calibrate eye movements for stable gaze, while the anterior vermis combines vestibular and proprioceptive inputs to coordinate head and body movements, ensuring postural stability. Similarly, the nodulus and ventral uvula (posterior vermis) integrate semicircular canal and otolith signals to regulate head orientation relative to gravity, facilitating spatial orientation and balance control.
Like all regions of the cerebellar cortex, the vestibular cerebellum receives two distinct types of input: mossy fibers, which relay sensory and motor information to granule cells; and climbing fibers, which arise from the inferior olivary nucleus and synapse on Purkinje cells—the sole output of the cerebellar cortex (Fig. 6B). Climbing fibers encode sensory prediction errors, signaling discrepancies between expected and actual sensory feedback. These error signals drive adaptive plasticity in Purkinje cells, refining motor commands to improve coordination and compensate for changes in the body or environment. Purkinje cells integrate these signals, firing simple and complex spikes in response to their mossy and climbing fiber inputs, respectively, allowing the cerebellum to continuously update motor control based on ongoing experience.
Accordingly, patients with cerebellar dysfunction exhibit impairments in navigation, dysmetria, head motion detection, and verticality perception, often developing an increased reliance on visual cues due to diminished vestibular function. These deficits highlight the critical role of the vestibular cerebellum in integrating multisensory signals to ensure accurate motor control and spatial orientation.
The Floccular Complex: Calibrating the Vestibuloocular Reflex and Gaze Stability
The floccular complex (flocculus and ventral paraflocculus) is essential for VOR motor learning and gaze stabilization. Lesions disrupt the VOR and OKR as well as their adaptation, leading to gaze instability during daily activities. In nonhuman primates, lesion studies have shown that the ventral paraflocculus plays a greater role than the flocculus in VOR motor learning [87,88]. The floccular complex receives mossy fiber inputs from vestibular nuclei neurons encoding head motion and brainstem nuclei neurons encoding eye movement effectively comprising an indirect pathway that combined with the direct VOR pathway to modulates the final VOR command to the extraocular motoneurons (Fig. 7A). These signals are relayed via parallel fibers to Purkinje cells, driving their simple spike activity [12]. Climbing fibers from the inferior olive convey retinal slip signals, triggering complex spikes in Purkinje cells. This input also induces long-term depression at parallel fiber-Purkinje cell synapses, a key mechanism for motor learning [89]. Additional plasticity mechanisms in the granular and molecular layers of the floccular lobe and vestibular nuclei further refine motor learning and behavior (reviewed in [12,90]).
These plasticity mechanisms allow the floccular complex to recalibrate the VOR when head motion and compensatory eye movements are mismatched, such as during adaptation to new corrective lenses or recovery from vestibular loss. By modulating VOR gain through inhibitory projections to the vestibular nuclei, the floccular complex forms a feedback loop crucial for both short-term stabilization and long-term adaptation (Fig. 7B). Over time, it consolidates cerebellar-driven plasticity by transferring gain modifications to the vestibular nuclei, ensuring sustained VOR adaptation [87]. This enables rapid gaze stabilization in dynamic environments and gradual compensation for visual or vestibular changes across the lifespan.
Clinically, floccular lobe dysfunction impairs VOR adaptation, smooth pursuit, and OKRs, leading to blurred vision and gaze instability during head movements. These deficits highlight the floccular lobe’s role in maintaining visual stability. Targeted rehabilitation strategies, such as adaptive gaze stabilization exercises [91-93], could enhance VOR adaptation and improve functional recovery following vestibular loss, aging, or disease.
Anterior Vermis: Integrating Vestibular and Proprioceptive Signals for Postural Control
The anterior vermis (lobules I–V) integrates vestibular and proprioceptive inputs to maintain posture and balance. Mossy fiber inputs relay information from the vestibular system and proprioceptors in the neck, trunk, and limbs [94,95]. Anterior vermis Purkinje cells, in turn, send inhibitory projections to the rostral fastigial nucleus and vestibular nuclei, which then send descending projections to premotor and motor areas of the brainstem and spinal cord, coordinating trunk and limb movements. By integrating vestibular and proprioceptive signals, Purkinje cells dynamically encode an intermediate representation of motion [83], transitioning between head- and body-centered reference frames at the level of their target neurons in the deep cerebellar nuclei (Fig. 8) [96]. This transformation is essential, as vestibular signals are inherently centered, while postural adjustments must account for head-body orientation to maintain stability.
Beyond transforming vestibular signals into a body-centered reference frame, the anterior vermis also plays a central role in distinguishing reafferent (self-generated) from exafferent (externally applied) vestibular inputs. This distinction is essential for suppressing reflexive vestibulospinal responses during voluntary movements, such as active head turns. By generating an internal model of voluntary actions, the anterior vermis predicts their sensory consequences, thereby preventing unnecessary reflexive responses [54]. A population of approximately 40 Purkinje cells is sufficient to account for VSR pathway suppression during self-motion. Notably, this reafferent vestibular suppression occurs only when predicted and actual sensory feedback align. If a discrepancy arises, such as in novel or unexpected conditions, the anterior vermis computes the mismatch, adapting to generate compensatory motor commands accordingly (Fig. 9) [50,51].
Understanding the anterior vermis’s role in these computations has important clinical implications. By modulating vestibulospinal pathways, the anterior vermis enables adaptive balance control, allowing for adjustments during tasks such as walking on uneven terrain or carrying shifting loads. It continuously calibrates these pathways, compensating for sensorimotor errors to maintain long-term postural stability. Damage to the anterior vermis or fastigial nucleus results in postural instability, increased sway, unsteady gait, impaired balance during locomotion, and limb coordination deficits [97,98]. Additional insights into the neural mechanisms underlying the computation of internal model can further inform targeted rehabilitation strategies and neuroprosthetic designs aimed at restoring balance and posture in individuals with cerebellar degeneration. Ongoing research into its cellular mechanisms holds promise for refining therapeutic approaches and improving patient outcomes.
Nodulus and Uvula: Computing Spatial Orientation Relative to Gravity
The nodulus and ventral uvula (lobules IX and X of the posterior vermis) are specialized regions of the vestibular cerebellum that integrate semicircular canal and otolith organ inputs to compute spatial orientation relative to gravity. Notably, these cerebellar regions are essential for distinguishing between tilt and translation [99]. Both movements produce identical otolith forces, this region resolves the resulting sensory ambiguity by integrating otolith afferents with semicircular canal inputs, which encode rotational motion. In turn, the nodulus and ventral uvula serves two key vestibular motor functions: (i) these regions mediate eye realignment relative to gravity following sudden head motion cessation [100,101] and (ii) they also contribute to velocity storage, by extending VOR responses to low-frequency stimuli to enabling compensatory eye movements during sustained head rotations [102]. Consequently, lesions in the nodulus and ventral uvula impair gravity-dependent vestibular-induced eye movements, compromising spatial orientation and postural control.
Unique among cerebellar regions, the nodulus and uvula receive direct mossy fiber input from both otolith and semicircular canal afferents, processing raw peripheral vestibular signals, in addition to secondary input from the vestibular nuclei (reviewed in [29]). Recent studies in macaque monkeys have further revealed that the vast majority of vestibular-sensitive Purkinje cells in the nodulus and ventral uvula also robustly encode neck proprioceptive [103], similar to anterior vermis as described above 9 (Fig. 8). Notably, the directional tuning across vestibular and proprioceptive modalities in this cerebellar region is aligned so as to enhance self-motion encoding [103]. Collectively, Purkinje cell population activity enables the computation of body motion in space, highlighting the nodulus and uvula’s critical role in integrating multisensory inputs to maintain spatial stability.
While much of the vestibular system’s role has been traditionally associated with reflexive behaviors, recent research has highlighted its contributions to voluntary motor control, including reaching, steering, and navigation. These behaviors require the integration of vestibular signals with visual, proprioceptive, and motor-related information at higher levels of central processing to plan and execute precise movements (Fig. 1, yellow box).
Reaching Movements
Accurate reaching during self-motion, such as picking up a coffee cup while turning, relies on vestibular feedback to compensate for spatial displacement and external forces like Coriolis and centrifugal forces. The vestibular system provides real-time feedback to motor pathways, ensuring precise coordination of limb movements despite body motion [104-107]. GVS studies confirm that vestibular input is essential for reaching accuracy, compensating for displacement due to self-motion [108,109]. Additionally, vestibular signals contribute to postural stability during reach preparation [110].
Neural pathways supporting this process include vestibular projections to the parietal and somatosensory cortices [111-113]. For example, the parietal reach region, which plays a key role in reach planning and execution, receives vestibular input [114]. Moreover, neurons in this region respond robustly to vestibular stimulation, as well as proprioceptive, visual, and motor-related signals to support high-level sensorimotor transformations necessary for precise reaching movements [115-117]. Overall, this integration enables the brain to seamlessly adjust for the self-motion that results from body and limb kinematics, ensuring that reaching movements remain accurate.
Steering and Navigation
The vestibular system also plays a key role in providing continuous feedback for steering and navigation. Accurate steering relies on the integration of vestibular, visual (optic flow), and proprioceptive cues (reviewed in [2,118]). Human studies have demonstrated that manual steering precision is directly linked to vestibular sensory accuracy. For instance, individuals with lower vestibular perceptual thresholds perform better in a manual control task, using a joystick to maintain their chair’s upright position [119]. Moreover, the vestibular system plays an important role in navigation by encoding heading direction and contributing to spatial map formation in the brain. As a result, patients with peripheral vestibular lesions exhibit deficits in spatial orientation and navigation tasks, highlighting the system’s importance (reviewed in [120]). Two main ascending vestibular pathways support these higher-order functions (Fig. 1, reviewed in [15]): the posterior thalamocortical pathway, which projects to vestibular cortical areas, including the parietal-insular vestibular cortex and dorsal (dorsal part of the medial superior temporal area, MSTd), and the anterior thalamocortical pathway, which connects to the navigation system’s head direction (HD) network.
VO neurons in the vestibular nuclei project not only to the spinal cord but also to the posterior thalamocortical pathway, transmitting vestibular information to cortical regions such as the parietal cortices, including the parietal-insular vestibular cortex and dorsal MSTd, via the posterior thalamus. Single-unit recording studies in rhesus monkeys have shown that VO neurons respond during voluntary steering tasks as if head motion were externally applied rather than self-generated, in contrast to their suppression during active voluntary head movements [47,48,50,51]. Similarly, MSTd neurons encode vestibular signals during voluntary steering while also responding to optic flow [115,121,122]. Further research is needed to determine how the brain integrates vestibular, proprioceptive, and visual cues with motor commands for precise steering, as well as how training may enhance this integration.
The vestibular system plays a vital role in spatial navigation by encoding HD and contributing to spatial mapping in the brain. Input from early vestibular pathways is essential for the HD system, a neural network that encodes directional heading independent of location and behavior. Lesion studies show that disrupting the peripheral vestibular system impairs HD cell signals in the anterior thalamocortical pathway (reviewed [15,123,124]). HD cells, in turn, contribute to the medial entorhinal grid cell system, whose function is also disrupted by vestibular loss. Importantly, as reviewed above, the vestibular nuclei do not merely encode purely vestibular information during active behaviors, making the information relayed to the cortex more complex. For example, vestibular signals from active movements are suppressed in the posterior thalamocortical pathway, while the anterior thalamocortical pathway integrates eye movement signals with vestibular inputs. Understanding how the HD system processes these multisensory inputs during navigation to compute directional heading relative to space remains a challenge for future research.
Clinical Implications: Vestibular Dysfunction and Cognitive Decline in Aging and Alzheimers
Emerging evidence links peripheral vestibular dysfunction to cognitive impairment [125,126], with cognitively impaired patients exhibiting poorer vestibular function, particularly in otolith responses, compared to age-matched controls [125]. Vestibular dysfunction is also common with aging and may contribute to cognitive decline [127,128].
In this context, it is noteworthy that Alzheimer disease is characterized by early hippocampal degeneration, leading to postural imbalance, spatial disorientation, and wandering. The hippocampus, essential for spatial navigation, is activated during both real and virtual navigation [129,130], and vestibular input supports this function, as evidenced by hippocampal activation during caloric stimulation [131]. Notably, chronic BVL leads to hippocampal atrophy and correlates with spatial memory deficits, while larger hippocampal volume is associated with better navigation performance [132,133]. Advancing our understanding of vestibular contributions to hippocampal integrity and cognitive decline in aging and neurodegeneration will be crucial for improving interventions and outcomes.
As discussed in the ‘Fine-tuning and Adapting Vestibulo-Motor Reflexes’ section above, central compensation restores partial vestibular function after unilateral loss. However, it is important to emphasize that recovery remains incomplete, resulting in altered motor behavior during daily activities of life, including orienting, balance, and gait [82-85]. The commissural vestibular system and extra-vestibular inputs help rebalance neural activity and enhance reflexes, but increased neural variability reduces signal fidelity. While the upweighting of proprioceptive and motor-related inputs aids recovery (Fig. 10A) [73,74,78], they cannot fully replace the precision of intact vestibular signals, leaving residual deficits in motion perception and postural control [46,75].
The recent development of vestibular prostheses has significantly improved the lives of patients with BVL [134]. These devices deliver biphasic pulsatile electrical stimulation to vestibular afferents, with the goal of replicating natural head motion signals using LN cascade models (Fig. 2C). Patients with BVL often experience persistent postural instability, oscillopsia, and impaired spatial navigation, and traditional rehabilitation is often insufficient, making vestibular prostheses a promising alternative. However, several challenges remain in optimizing patient outcomes. Recall that regular afferents primarily drive VOR neurons (i.e., PVPs and FTNs) to stabilize gaze, while irregular afferents primarily drive VO neurons to generate robust postural responses (Fig. 10B). Pulsatile stimulation approaches indiscriminately activate both regular and irregular afferents, leading to functional trade-offs. Stimulation mappings that mimic the regular afferent input could enhance visual stability via VOR pathways [135], whereas those that mimic irregular afferents may better support postural control.
Another challenge is that vestibular pathways encode prosthetic signals differently from natural inputs. Specifically, studies in monkeys show that while standard stimulation protocols reliably activate afferents in a predictable manner (Fig. 10C) [136,137], this same stimulation rapidly reduces efficacy at the afferent-vestibular nuclei synapse—by over 50% within minutes—compromising VORs and VSRs [136,138]. This maladaptive effect likely results from long-term depression induced by unnatural synchrony in afferents due to prosthetic stimulation. While inhibitory commissural plasticity partially offsets this decline, optimizing stimulation parameters remains crucial to mitigating these effects and improving outcomes [27]. Personalized stimulation paradigms, computational modeling, and large-scale neural recordings will be essential for advancing prosthesis function and improving patient outcomes.

Funding/Support

This work was supported by the National Institute on Deafness and Other Communication Disorders (R01-DC002390 and R01-DC018061), as well as a Johns Hopkins University Discovery Grant.

Conflicts of Interest

No potential conflict of interest relevant to this article was reported.

Availability of Data and Materials

The datasets are not publicly available but are available from the corresponding author upon reasonable request.

Acknowledgments

I thank Jerome Carriot for his contributions and support in creating the illustrations.

Fig. 1.
(A) The mammalian vestibular system comprises five sensory organs: three semicircular canals and two otolith organs (utricle and saccule). Each organ contains specialized neuroepithelia where hair cells, the primary receptor cells, detect head motion. (B) Afferent fibers of the VIII cranial nerve innervate these hair cells, transmitting head movement signals to the vestibular nuclei and cerebellum. Regular afferents exhibit a relatively steady resting discharge, whereas irregular afferents display more variable resting activity. VO, vestibular-only; EH, eye-head; PVP, position-vestibular-pause; VSR, vestibulospinal reflex; VOR, vestibuloocular reflex.
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Fig. 2.
Encoding of natural head motion by vestibular afferents. (A) Left: Example responses of regular and irregular semicircular canal afferents to sinusoidal head rotations at 0.5 Hz and 15 Hz. The right insets are schematic representations of response gain differences between regular and irregular semicircular canal afferents. Irregular afferents exhibit higher gains that increase sharply at higher frequencies, whereas regular afferents maintain more stable gains. (B) Natural vestibular stimuli reach higher intensities (yellow area) than those used in clinical vestibular testing, which typically operates within the linear range of afferent responses (gray bar). (C) Testing that spans the natural range of stimulus intensities reveals that afferents display nonlinear responses that can be well described by their responses within the linear range cascading with a sigmoidal nonlinearity (solid red line), which deviates from the unity line (dashed). This representation is called a linear-nonlinear cascade model. (D) Irregular afferents also utilize a precise spike timing code, whereas regular afferents primarily encode motion through firing rate modulation.
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Fig. 3.
The vestibuloocular reflex (VOR). (A) Schematic of horizontal VOR pathways during leftward head rotation. Excitatory (solid blue lines) and inhibitory (dashed blue lines) pathways are shown, with the thick solid line representing the direct pathway. Leftward head motion increases activation of the right lateral and left medial rectus muscles while suppressing their antagonists. (B) Prolonged rotations elicit a sawtooth pattern of slow compensatory phases (slow phases) and rapid resetting phases (quick phases), collectively referred to as vestibular nystagmus. (C) Context-dependent gating of the VOR pathway at the vestibular nuclei. When the goal is to redirect rather than stabilize gaze, position-vestibular-pause (PVP) neurons, the central link in the direct VOR pathway, are strongly inhibited by premotor saccadic pathways. This gating mechanism suppresses VOR activity when the behavioral goal shifts from gaze stabilization to voluntary redirection, as during coordinated eye-head gaze shifts. ABD, abducens nucleus; FR, firing rate; VO, vestibular-only.
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Fig. 4.
The vestibulospinal reflex (VSR). (A) The vestibular nuclei send both direct and indirect projections to the spinal cord, forming key pathways that mediate postural control and balance. Direct projections originate from the vestibular nuclei and extend to the spinal cord, while indirect projections involve intermediary relay structures (e.g., reticular formation and INC) before reaching the spinal cord. (B) Context-dependent gating in vestibular-only (VO) neurons. During voluntary head motion, VO neurons receive an inhibitory cancellation signal when the expected sensory consequence of neck motor commands matches actual proprioceptive feedback. This gating mechanism suppresses vestibular reafference, effectively isolating sensory inputs related to passive motion. A “gate” symbolically represents this cancellation mechanism. PVP, position-vestibular-pause; VO, vestibular-only; INC, interstitial nucleus of Cajal; MN, motoneuron; FR, firing rate.
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Fig. 5.
Effects of galvanic vestibular stimulation (GVS) on the peripheral vestibular system. (A) Schematic of the setup used to apply GVS in the nonhuman primate model. Stimulation is applied between surface electrodes placed on the mastoid processes behind the ears, while the animal’s eye movements and neural activity are recorded. (B) Comparison of response gains to sinusoidal GVS for regular and irregular (blue and red, respectively) canal afferents. Dashed lines illustrating the corresponding responses to actual rotational motion are shown for comparison. (C) Schematic of regular and irregular (blue and red, respectively) canal afferent responses to sinusoidal GVS, constant current GVS (center) and stochastic or ‘noisy’ GVS (right, 0–300 Hz). Note that current steps evoke asymmetric changes in afferent firing rates during stimuli of opposing polarity, primarily for irregular afferents. Schematic of the asymmetric responses (gray) of an irregular afferent is shown, respectively. The blue and red traces show the response fit to cathodal stimulation (solid), and the mirrored fit superimposed on the anodal response (dashed).
rvs-2025-008f5.jpg
Fig. 6.
Organization of the vestibular cerebellum. (A) Schematic showing five main regions receiving vestibular input: (i) anterior lobe lobules I–V (green), (ii) nodulus and ventral uvula (blue), (iii) flocculus and ventral paraflocculus (pink), (iv) fastigial deep cerebellar nucleus and vestibular nuclei (yellow), and (v) posterior lobe oculomotor vermis (gray), which receives some vestibular input. (B) Purkinje cells receive two specific sources of input, each of which differentially affects the Purkinje cell responses. Mossy fiber (MF) inputs act via interneurons to induce high-frequency simple spike responses. In contrast, climbing fiber inputs induce low-frequency complex spikes. Purkinje cells provide the sole output of the cerebellar cortex and project to the deep cerebellar and vestibular nuclei. Unipolar brush cells, a class of local circuit neurons that are abundant in the nodulus/uvula and flocculonodular lobes, are thought to amplify the MF input via feedforward excitation.
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Fig. 7.
Vestibuloocular reflex (VOR) motor learning and computations underlying gaze stability. (A) Two pathways control the gain of the VOR. First, the direct reflex pathway (red) comprises a three-neuron arc: vestibular afferents project to vestibular nuclei neurons that in turn project to the eye muscle motoneurons. This direct pathway is paralleled by an inhibitory side loop (blue) through the floccular lobe. As a result, the total gain is determined by the net drive from these two pathways. (B) During visually induced VOR motor learning, climbing fibers encode a visual error signal, which induces learning at the synapses of vestibular parallel fibers onto the Purkinje cells (red star). Then, over time, motor learning is consolidated via modification of synapses in the target neurons of the vestibular nuclei (green star). FTN, floccular target neuron; PVP, position-vestibular-pause.
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Fig. 8.
(A) The vestibular responses of Purkinje cells in the anterior vermis are modulated as a function of head-on-body position. (B) Distribution of head and body sensitivity ratios for anterior vermis and nodulus/uvula Purkinje cells, in comparison to pure head-centered (red star) and body-centered (blue star) motion coding. Purkinje cells in the posterior vermis (nodulus and ventral uvula) display similar response properties.
rvs-2025-008f8.jpg
Fig. 9.
Computations underlying the selective coding of actively generated vestibular stimulation. The anterior vermis compares neck proprioceptive inputs with the expected sensory consequence of neck motor command (internal model). If these signals match, a cancellation signal is sent to vestibular-only (VO) neurons in the vestibular nuclei to remove the component of vestibular stimulation that this the result of active self-generated motion (i.e., vestibular ‘reafference’). In turn, these neurons, as well as neurons they target in the vestibular thalamocortical pathway, selectively encode unexpected motion (i.e., vestibular ‘exafference’). SPE, sensory prediction error.
rvs-2025-008f9.jpg
Fig. 10.
(A) Both position-vestibular-pause (PVP) and vestibular-only (VO) neurons in the vestibular nuclei display increasingly enhanced responses to active versus passive head movements, due to the unmasking of a second extra-vestibular input that transmits a motor efference copy. (B) The nerve bundle of each semicircular canal is targeted by an electrode array, allowing for canal-specific stimulation. Stimulation of each of the three individual canals evokes eye movements consistent with its activation axis. Example eye velocity traces are shown for stimulation of the horizontal canal electrode. (C) Adaptation to prosthetic pulses at the afferent-vestibular nuclei synapses is problematic. The efficacy of the vestibular afferent-central vestibular nuclei neuron synapse is reduced by 50% within minutes of the baseline stimulation used in clinical trials. This is the case for both PVP (blue) and VO (green) neurons in the vestibular nuclei.
rvs-2025-008f10.jpg
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        The vestibular system and the encoding of self-motion: from basic science to clinical applications
        Res Vestib Sci. 2025;24(3):117-138.   Published online September 15, 2025
        DOI: https://doi.org/10.21790/rvs.2025.008
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      The vestibular system and the encoding of self-motion: from basic science to clinical applications
      Image Image Image Image Image Image Image Image Image Image
      Fig. 1. (A) The mammalian vestibular system comprises five sensory organs: three semicircular canals and two otolith organs (utricle and saccule). Each organ contains specialized neuroepithelia where hair cells, the primary receptor cells, detect head motion. (B) Afferent fibers of the VIII cranial nerve innervate these hair cells, transmitting head movement signals to the vestibular nuclei and cerebellum. Regular afferents exhibit a relatively steady resting discharge, whereas irregular afferents display more variable resting activity. VO, vestibular-only; EH, eye-head; PVP, position-vestibular-pause; VSR, vestibulospinal reflex; VOR, vestibuloocular reflex.
      Fig. 2. Encoding of natural head motion by vestibular afferents. (A) Left: Example responses of regular and irregular semicircular canal afferents to sinusoidal head rotations at 0.5 Hz and 15 Hz. The right insets are schematic representations of response gain differences between regular and irregular semicircular canal afferents. Irregular afferents exhibit higher gains that increase sharply at higher frequencies, whereas regular afferents maintain more stable gains. (B) Natural vestibular stimuli reach higher intensities (yellow area) than those used in clinical vestibular testing, which typically operates within the linear range of afferent responses (gray bar). (C) Testing that spans the natural range of stimulus intensities reveals that afferents display nonlinear responses that can be well described by their responses within the linear range cascading with a sigmoidal nonlinearity (solid red line), which deviates from the unity line (dashed). This representation is called a linear-nonlinear cascade model. (D) Irregular afferents also utilize a precise spike timing code, whereas regular afferents primarily encode motion through firing rate modulation.
      Fig. 3. The vestibuloocular reflex (VOR). (A) Schematic of horizontal VOR pathways during leftward head rotation. Excitatory (solid blue lines) and inhibitory (dashed blue lines) pathways are shown, with the thick solid line representing the direct pathway. Leftward head motion increases activation of the right lateral and left medial rectus muscles while suppressing their antagonists. (B) Prolonged rotations elicit a sawtooth pattern of slow compensatory phases (slow phases) and rapid resetting phases (quick phases), collectively referred to as vestibular nystagmus. (C) Context-dependent gating of the VOR pathway at the vestibular nuclei. When the goal is to redirect rather than stabilize gaze, position-vestibular-pause (PVP) neurons, the central link in the direct VOR pathway, are strongly inhibited by premotor saccadic pathways. This gating mechanism suppresses VOR activity when the behavioral goal shifts from gaze stabilization to voluntary redirection, as during coordinated eye-head gaze shifts. ABD, abducens nucleus; FR, firing rate; VO, vestibular-only.
      Fig. 4. The vestibulospinal reflex (VSR). (A) The vestibular nuclei send both direct and indirect projections to the spinal cord, forming key pathways that mediate postural control and balance. Direct projections originate from the vestibular nuclei and extend to the spinal cord, while indirect projections involve intermediary relay structures (e.g., reticular formation and INC) before reaching the spinal cord. (B) Context-dependent gating in vestibular-only (VO) neurons. During voluntary head motion, VO neurons receive an inhibitory cancellation signal when the expected sensory consequence of neck motor commands matches actual proprioceptive feedback. This gating mechanism suppresses vestibular reafference, effectively isolating sensory inputs related to passive motion. A “gate” symbolically represents this cancellation mechanism. PVP, position-vestibular-pause; VO, vestibular-only; INC, interstitial nucleus of Cajal; MN, motoneuron; FR, firing rate.
      Fig. 5. Effects of galvanic vestibular stimulation (GVS) on the peripheral vestibular system. (A) Schematic of the setup used to apply GVS in the nonhuman primate model. Stimulation is applied between surface electrodes placed on the mastoid processes behind the ears, while the animal’s eye movements and neural activity are recorded. (B) Comparison of response gains to sinusoidal GVS for regular and irregular (blue and red, respectively) canal afferents. Dashed lines illustrating the corresponding responses to actual rotational motion are shown for comparison. (C) Schematic of regular and irregular (blue and red, respectively) canal afferent responses to sinusoidal GVS, constant current GVS (center) and stochastic or ‘noisy’ GVS (right, 0–300 Hz). Note that current steps evoke asymmetric changes in afferent firing rates during stimuli of opposing polarity, primarily for irregular afferents. Schematic of the asymmetric responses (gray) of an irregular afferent is shown, respectively. The blue and red traces show the response fit to cathodal stimulation (solid), and the mirrored fit superimposed on the anodal response (dashed).
      Fig. 6. Organization of the vestibular cerebellum. (A) Schematic showing five main regions receiving vestibular input: (i) anterior lobe lobules I–V (green), (ii) nodulus and ventral uvula (blue), (iii) flocculus and ventral paraflocculus (pink), (iv) fastigial deep cerebellar nucleus and vestibular nuclei (yellow), and (v) posterior lobe oculomotor vermis (gray), which receives some vestibular input. (B) Purkinje cells receive two specific sources of input, each of which differentially affects the Purkinje cell responses. Mossy fiber (MF) inputs act via interneurons to induce high-frequency simple spike responses. In contrast, climbing fiber inputs induce low-frequency complex spikes. Purkinje cells provide the sole output of the cerebellar cortex and project to the deep cerebellar and vestibular nuclei. Unipolar brush cells, a class of local circuit neurons that are abundant in the nodulus/uvula and flocculonodular lobes, are thought to amplify the MF input via feedforward excitation.
      Fig. 7. Vestibuloocular reflex (VOR) motor learning and computations underlying gaze stability. (A) Two pathways control the gain of the VOR. First, the direct reflex pathway (red) comprises a three-neuron arc: vestibular afferents project to vestibular nuclei neurons that in turn project to the eye muscle motoneurons. This direct pathway is paralleled by an inhibitory side loop (blue) through the floccular lobe. As a result, the total gain is determined by the net drive from these two pathways. (B) During visually induced VOR motor learning, climbing fibers encode a visual error signal, which induces learning at the synapses of vestibular parallel fibers onto the Purkinje cells (red star). Then, over time, motor learning is consolidated via modification of synapses in the target neurons of the vestibular nuclei (green star). FTN, floccular target neuron; PVP, position-vestibular-pause.
      Fig. 8. (A) The vestibular responses of Purkinje cells in the anterior vermis are modulated as a function of head-on-body position. (B) Distribution of head and body sensitivity ratios for anterior vermis and nodulus/uvula Purkinje cells, in comparison to pure head-centered (red star) and body-centered (blue star) motion coding. Purkinje cells in the posterior vermis (nodulus and ventral uvula) display similar response properties.
      Fig. 9. Computations underlying the selective coding of actively generated vestibular stimulation. The anterior vermis compares neck proprioceptive inputs with the expected sensory consequence of neck motor command (internal model). If these signals match, a cancellation signal is sent to vestibular-only (VO) neurons in the vestibular nuclei to remove the component of vestibular stimulation that this the result of active self-generated motion (i.e., vestibular ‘reafference’). In turn, these neurons, as well as neurons they target in the vestibular thalamocortical pathway, selectively encode unexpected motion (i.e., vestibular ‘exafference’). SPE, sensory prediction error.
      Fig. 10. (A) Both position-vestibular-pause (PVP) and vestibular-only (VO) neurons in the vestibular nuclei display increasingly enhanced responses to active versus passive head movements, due to the unmasking of a second extra-vestibular input that transmits a motor efference copy. (B) The nerve bundle of each semicircular canal is targeted by an electrode array, allowing for canal-specific stimulation. Stimulation of each of the three individual canals evokes eye movements consistent with its activation axis. Example eye velocity traces are shown for stimulation of the horizontal canal electrode. (C) Adaptation to prosthetic pulses at the afferent-vestibular nuclei synapses is problematic. The efficacy of the vestibular afferent-central vestibular nuclei neuron synapse is reduced by 50% within minutes of the baseline stimulation used in clinical trials. This is the case for both PVP (blue) and VO (green) neurons in the vestibular nuclei.

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      The vestibular system and the encoding of self-motion: from basic science to clinical applications
      Res Vestib Sci : Research in Vestibular Science
      © Korean Balance Society.
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