Human proprioceptive gaze stabilization during passive body rotations underneath a fixed head.

The present study explored the presence of torsional gaze-stabilization to proprioceptive neck activation in humans. Thirteen healthy subjects (6 female, mean age 25) were exposed to passive body rotations while maintaining a head-fixed, gravitationally upright, position. Participants were seated in a mechanical sled, their heads placed in a chin rest embedded in a wooden beam while wearing an eye tracker attached to the beam using strong rubber bands to ensure head stability. The body was passively rotated underneath the head both in darkness and while viewing a projected visual scene. Static torsional gaze positions were compared between the baseline position prior to the stimulation, and immediately after the final body tilt had been reached. Results showed that passive neck flexion produced ocular torsion when combined with a visual background. The eyes exhibited rotations in the opposite direction of the neck's extension, matching a hypothetical head tilt in the same direction as the sled. This corresponded with a predicted head rotation aimed at straightening the head in relation to the body. No such response was seen during trials in darkness. Altogether, these findings suggest that proprioception may produce a predictive gaze-stabilizing response in humans.

Temporal dynamics of ocular torsion and vertical vergence during visual, vestibular, and visuovestibular rotations.

Ocular torsion and vertical divergence reflect the brain's sensorimotor integration of motion through the vestibulo-ocular reflex (VOR) and the optokinetic reflex (OKR) to roll rotations. Torsion and vergence however express different response patterns depending on several motion variables, but research on their temporal dynamics remains limited. This study investigated the onset times of ocular torsion (OT) and vertical vergence (VV) during visual, vestibular, and visuovestibular motion, as well as their relative decay rates following prolonged optokinetic stimulations. Temporal characteristics were retrieved from three separate investigations where the level of visual clutter and acceleration were controlled. Video eye-tracking was used to retrieve the eye-movement parameters from a total of 41 healthy participants across all trials. Ocular torsion consistently initiated earlier than vertical vergence, particularly evident under intensified visual information density, and higher clutter levels were associated with more balanced decay rates. Additionally, stimulation modality and accelerations affected the onsets of both eye movements, with visuovestibular motion triggering earlier responses compared to vestibular motion, and increased accelerations leading to earlier onsets for both movements. The present study showed that joint visuovestibular responses produced more rapid onsets, indicating a synergetic sensorimotor process. It also showed that visual content acted as a fusional force during the decay period, and imposed greater influence over the torsional onset compared to vergence. Acceleration, by contrast, did not affect the temporal relationship between the two eye movements. Altogether, these findings provide insights into the sensorimotor integration of the vestibulo-ocular and optokinetic reflex arcs.

The motor apparatus of head movements in the Oleander hawkmoth (Daphnis nerii, Lepidoptera).

Head movements of insects play a vital role in diverse locomotory behaviors including flying and walking. Because insect eyes move minimally within their sockets, their head movements are essential to reduce visual blur and maintain a stable gaze. As in most vertebrates, gaze stabilization behavior in insects requires the integration of both visual and mechanosensory feedback by the neck motor neurons. Although visual feedback is derived from the optic flow over the retina of their compound eyes, mechanosensory feedback is derived from their organs of balance, similar to the vestibular system in vertebrates. In Diptera, vestibular feedback is derived from the halteres-modified hindwings that evolved into mechanosensory organs-and is integrated with visual feedback to actuate compensatory head movements. However, non-Dipteran insects, including Lepidoptera, lack halteres. In these insects, vestibular feedback is obtained from the antennal Johnston's organs but it is not well-understood how it integrates with visual feedback during head movements. Indeed, although head movements are well-studied in flies, the underlying motor apparatus in non-Dipteran taxa has received relatively less attention. As a first step toward understanding compensatory head movements in the Oleander hawkmoth Daphnis nerii, we image the anatomy and architecture of their neck joint sclerites and muscles using X-ray microtomography, and the associated motor neurons using fluorescent dye fills and confocal microscopy. Based on these morphological data, we propose testable hypotheses about the putative function of specific neck muscles during head movements, which can shed light on their role in neck movements and gaze stabilization.

Drosophila flying in augmented reality reveals the vision-based control autonomy of the optomotor response.

For walking, swimming, and flying animals, the optomotor response is essential to stabilize gaze. How flexible is the optomotor response? Classic work in Drosophila has argued that flies adapt flight control under augmented visual feedback conditions during goal-directed bar fixation. However, whether the lower-level, reflexive optomotor response can similarly adapt to augmented visual feedback (partially autonomous) or not (autonomous) over long timescales is poorly understood. To address this question, we developed an augmented reality paradigm to study the vision-based control autonomy of the yaw optomotor response of flying fruit flies (Drosophila). Flies were placed in a flight simulator, which permitted free body rotation about the yaw axis. By feeding back body movements in real time to a visual display, we augmented and inverted visual feedback. Thus, this experimental paradigm caused a constant visual error between expected and actual visual feedback to study potential adaptive visuomotor control. By combining experiments with control theory, we demonstrate that the optomotor response is autonomous during augmented reality flight bouts of up to 30 min, which exceeds the reported learning epoch during bar fixation. Agreement between predictions from linear systems theory and experimental data supports the notion that the optomotor response is approximately linear and time invariant within our experimental assay. Even under positive visual feedback, which revealed the stability limit of flies in augmented reality, the optomotor response was autonomous. Our results support a hierarchical motor control architecture in flies with fast and autonomous reflexes at the bottom and more flexible behavior at higher levels.

Neural mechanisms to incorporate visual counterevidence in self-movement estimation.

In selecting appropriate behaviors, animals should weigh sensory evidence both for and against specific beliefs about the world. For instance, animals measure optic flow to estimate and control their own rotation. However, existing models of flow detection can be spuriously triggered by visual motion created by objects moving in the world. Here, we show that stationary patterns on the retina, which constitute evidence against observer rotation, suppress inappropriate stabilizing rotational behavior in the fruit fly Drosophila. In silico experiments show that artificial neural networks (ANNs) that are optimized to distinguish observer movement from external object motion similarly detect stationarity and incorporate negative evidence. Employing neural measurements and genetic manipulations, we identified components of the circuitry for stationary pattern detection, which runs parallel to the fly's local motion and optic-flow detectors. Our results show how the fly brain incorporates negative evidence to improve heading stability, exemplifying how a compact brain exploits geometrical constraints of the visual world.

Multisensory gaze stabilization in response to subchronic alteration of vestibular type I hair cells.

The functional complementarity of the vestibulo-ocular reflex (VOR) and optokinetic reflex (OKR) allows for optimal combined gaze stabilization responses (CGR) in light. While sensory substitution has been reported following complete vestibular loss, the capacity of the central vestibular system to compensate for partial peripheral vestibular loss remains to be determined. Here, we first demonstrate the efficacy of a 6-week subchronic ototoxic protocol in inducing transient and partial vestibular loss which equally affects the canal- and otolith-dependent VORs. Immunostaining of hair cells in the vestibular sensory epithelia revealed that organ-specific alteration of type I, but not type II, hair cells correlates with functional impairments. The decrease in VOR performance is paralleled with an increase in the gain of the OKR occurring in a specific range of frequencies where VOR normally dominates gaze stabilization, compatible with a sensory substitution process. Comparison of unimodal OKR or VOR versus bimodal CGR revealed that visuo-vestibular interactions remain reduced despite a significant recovery in the VOR. Modeling and sweep-based analysis revealed that the differential capacity to optimally combine OKR and VOR correlates with the reproducibility of the VOR responses. Overall, these results shed light on the multisensory reweighting occurring in pathologies with fluctuating peripheral vestibular malfunction.

Columnar neurons support saccadic bar tracking in Drosophila.

Tracking visual objects while maintaining stable gaze is complicated by the different computational requirements for figure-ground discrimination, and the distinct behaviors that these computations coordinate. Drosophila melanogaster uses smooth optomotor head and body movements to stabilize gaze, and impulsive saccades to pursue elongated vertical bars. Directionally selective motion detectors T4 and T5 cells provide inputs to large-field neurons in the lobula plate, which control optomotor gaze stabilization behavior. Here, we hypothesized that an anatomically parallel pathway represented by T3 cells, which provide inputs to the lobula, drives bar tracking body saccades. We combined physiological and behavioral experiments to show that T3 neurons respond omnidirectionally to the same visual stimuli that elicit bar tracking saccades, silencing T3 reduced the frequency of tracking saccades, and optogenetic manipulation of T3 acted on the saccade rate in a push-pull manner. Manipulating T3 did not affect smooth optomotor responses to large-field motion. Our results show that parallel neural pathways coordinate smooth gaze stabilization and saccadic bar tracking behavior during flight.

Role of locomotor efference copy in vertebrate gaze stabilization.

Vertebrate locomotion presents a major challenge for maintaining visual acuity due to head movements resulting from the intimate biomechanical coupling with the propulsive musculoskeletal system. Retinal image stabilization has been traditionally ascribed to the transformation of motion-related sensory feedback into counteracting ocular motor commands. However, extensive exploration of spontaneously active semi-intact and isolated brain/spinal cord preparations of the amphibian Xenopus laevis, have revealed that efference copies (ECs) of the spinal motor program that generates axial- or limb-based propulsion directly drive compensatory eye movements. During fictive locomotion in larvae, ascending ECs from rostral spinal central pattern generating (CPG) circuitry are relayed through a defined ascending pathway to the mid- and hindbrain ocular motor nuclei to produce conjugate eye rotations during tail-based undulatory swimming in the intact animal. In post-metamorphic adult frogs, this spinal rhythmic command switches to a bilaterally-synchronous burst pattern that is appropriate for generating convergent eye movements required for maintaining image stability during limb kick-based rectilinear forward propulsion. The transition between these two fundamentally different coupling patterns is underpinned by the emergence of altered trajectories in spino-ocular motor coupling pathways that occur gradually during metamorphosis, providing a goal-specific, morpho-functional plasticity that ensures retinal image stability irrespective of locomotor mode. Although the functional impact of predictive ECs produced by the locomotory CPG matches the spatio-temporal specificity of reactive sensory-motor responses, rather than contributing additively to image stabilization, horizontal vestibulo-ocular reflexes (VORs) are selectively suppressed during intense locomotor CPG activity. This is achieved at least in part by an EC-mediated attenuation of mechano-electrical encoding at the vestibular sensory periphery. Thus, locomotor ECs and their potential suppressive impact on vestibular sensory-motor processing, both of which have now been reported in other vertebrates including humans, appear to play an important role in the maintenance of stable vision during active body displacements.

Effects of Gaze Stabilization Exercises on Gait, Plantar Pressure, and Balance Function in Post-Stroke Patients: A Randomized Controlled Trial.

This study aims to explore the effects of gaze stabilization exercises (GSEs) on gait, plantar pressure, and balance function in post-stroke patients (≤6 months). Forty post-stroke patients were randomly divided into an experimental group (n = 20) and a control group (n = 20). The experimental group performed GSEs combined with physical therapy, while the control group only performed physical therapy, once a day, 5 days a week, for 4 weeks. The Berg Balance Scale (BBS) was used to test the balance function and the risk of falling, which was the primary outcome. The Timed Up and Go test (TUGT) evaluated the walking ability and the fall risk. The envelope ellipse area and the plantar pressure proportion of the affected side were used to measure the patient's supporting capacity and stability in static standing. The anterior−posterior center of pressure displacement velocity was used to test the weight-shifting capacity. Compared to the control group, the swing phase of the affected side, swing phase's absolute symmetric index, envelope ellipse area when eyes closed, and TUGT of the experimental group had significantly decreased after GSEs (p < 0.05); the BBS scores, TUGT, the anterior−posterior COP displacement velocity, and the plantar pressure proportion of the affected side had significantly increased after 4 weeks of training (p < 0.05). In conclusion, GSEs combined with physical therapy can improve the gait and balance function of people following stroke. Furthermore, it can enhance the weight-shifting and one-leg standing capacity of the affected side, thus reducing the risk of falling.

Small-amplitude head oscillations result from a multimodal head stabilization reflex in hawkmoths.

In flying insects, head stabilization is an essential reflex that helps to reduce motion blur during fast aerial manoeuvres. This reflex is multimodal and requires the integration of visual and antennal mechanosensory feedback in hawkmoths, each operating as a negative-feedback-control loop. As in any negative-feedback system, the head stabilization system possesses inherent oscillatory dynamics that depend on the rate at which the sensorimotor components of the reflex operate. Consistent with this expectation, we observed small-amplitude oscillations in the head motion (or head wobble) of the oleander hawkmoth, Daphnis nerii, which are accentuated when sensory feedback is aberrant. Here, we show that these oscillations emerge from the inherent dynamics of the multimodal reflex underlying gaze stabilization, and that the amplitude of head wobble is a function of both the visual feedback and antennal mechanosensory feedback from the Johnston's organs. Our data support the hypothesis that head wobble results from a multimodal, dynamically stabilized reflex loop that mediates head positioning.

Restructuring of the Optokinetic Reflex during Metamorphosis in Pelobates fuscus Laur.

The restructuring of the gaze stabilization system in Pelobates fuscus was investigated by quantitative analysis of the optomotor response using video imaging. Gaze stabilization is an important component in the system of neural mechanisms of visual depth perception. It was shown that the optomotor response in aquatic tadpoles of P. fuscus is similar to that of fish (movement of the animal in the direction of the visual background movement and eye nystagmus consisting of a fast and a slow phase). During metamorphosis (transition from the aquatic to the terrestrial lifestyle), froglets of P. fuscus responded to the movement of the visual background by eyes and head movements. One year after metamorphosis, P. fuscus responded to movement of the visual background as adult Anura: only by head movements (a slow and a fast phase), while eye movements were absent. Possible causes of the loss of active eye movements by Anura amphibians in the process of evolution are discussed.

Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths.

During flight maneuvers, insects exhibit compensatory head movements which are essential for stabilizing the visual field on their retina, reducing motion blur, and supporting visual self-motion estimation. In Diptera, such head movements are mediated via visual feedback from their compound eyes that detect retinal slip, as well as rapid mechanosensory feedback from their halteres - the modified hindwings that sense the angular rates of body rotations. Because non-Dipteran insects lack halteres, it is not known if mechanosensory feedback about body rotations plays any role in their head stabilization response. Diverse non-Dipteran insects are known to rely on visual and antennal mechanosensory feedback for flight control. In hawkmoths, for instance, reduction of antennal mechanosensory feedback severely compromises their ability to control flight. Similarly, when the head movements of freely flying moths are restricted, their flight ability is also severely impaired. The role of compensatory head movements as well as multimodal feedback in insect flight raises an interesting question: in insects that lack halteres, what sensory cues are required for head stabilization? Here, we show that in the nocturnal hawkmoth Daphnis nerii, compensatory head movements are mediated by combined visual and antennal mechanosensory feedback. We subjected tethered moths to open-loop body roll rotations under different lighting conditions, and measured their ability to maintain head angle in the presence or absence of antennal mechanosensory feedback. Our study suggests that head stabilization in moths is mediated primarily by visual feedback during roll movements at lower frequencies, whereas antennal mechanosensory feedback is required when roll occurs at higher frequency. These findings are consistent with the hypothesis that control of head angle results from a multimodal feedback loop that integrates both visual and antennal mechanosensory feedback, albeit at different latencies. At adequate light levels, visual feedback is sufficient for head stabilization primarily at low frequencies of body roll. However, under dark conditions, antennal mechanosensory feedback is essential for the control of head movements at high frequencies of body roll.

Downbeat nystagmus becomes attenuated during walking compared to standing.

Downbeat nystagmus (DBN) is a common form of acquired fixation nystagmus related to vestibulo-cerebellar impairments and associated with impaired vision and postural imbalance. DBN intensity becomes modulated by various factors such as gaze direction, head position, daytime, and resting conditions. Further evidence suggests that locomotion attenuates postural symptoms in DBN. Here, we examined whether walking might analogously influence ocular-motor deficits in DBN. Gaze stabilization mechanisms and nystagmus frequency were examined in 10 patients with DBN and 10 age-matched healthy controls with visual fixation during standing vs. walking on a motorized treadmill. Despite their central ocular-motor deficits, linear and angular gaze stabilization in the vertical plane were functional during walking in DBN patients and comparable to controls. Notably, nystagmus frequency in patients was considerably reduced during walking compared to standing (p < 0.001). The frequency of remaining nystagmus during walking was further modulated in a manner that depended on the specific phase of the gait cycle (p = 0.015). These attenuating effects on nystagmus intensity during walking suggest that ocular-motor control disturbances are selectively suppressed during locomotion in DBN. This suppression is potentially mediated by locomotor efference copies that have been shown to selectively govern gaze stabilization during stereotyped locomotion in animal models.

Conservation of locomotion-induced oculomotor activity through evolution in mammals.

Efference copies are neural replicas of motor outputs used to anticipate the sensory consequences of a self-generated motor action or to coordinate neural networks involved in distinct motor behaviors.1 An established example of this motor-to-motor coupling is the efference copy of the propulsive motor command, which supplements classical visuo-vestibular reflexes to ensure gaze stabilization during amphibian larval locomotion.2 Such feedforward replica of spinal pattern-generating circuits produces a spino-extraocular motor coupled activity that evokes eye movements, spatiotemporally coordinated to tail undulation independently of any sensory signal.3,4 Exploiting the developmental stages of the frog,1 studies in metamorphing Xenopus demonstrated the persistence of this spino-extraocular motor command in adults and its developmental adaptation to tetrapodal locomotion.5,6 Here, we demonstrate for the first time the existence of a comparable locomotor-to-ocular motor coupling in the mouse. In neonates, ex vivo nerve recordings of brainstem-spinal cord preparations reveal a spino-extraocular motor coupled activity similar to the one described in Xenopus. In adult mice, trans-synaptic rabies virus injections in lateral rectus eye muscle label cervical spinal cord neurons closely connected to abducens motor neurons. Finally, treadmill-elicited locomotion in decerebrated preparations7 evokes rhythmic eye movements in synchrony with the limb gait pattern. Overall, our data are evidence for the conservation of locomotor-induced eye movements in vertebrate lineages. Thus, in mammals as in amphibians, CPG-efference copy feedforward signals might interact with sensory feedback to ensure efficient gaze control during locomotion.

Gaze stabilization exercises can improve balance after a stroke / 中华物理医学与康复杂志

Objective:To observe the effect of gaze stabilization exercises on the balance of stroke patients.Methods:Forty stroke patients were randomly divided into an experimental group ( n=20) and a control group ( n=20). Both groups were given conventional rehabilitation therapy, while the experimental group was additionally provided with gaze stabilization exercises, once a day, five days a week, for a total of four weeks. Each session lasted 30 minutes. Before and after the four weeks, both groups were evaluated in terms of their envelope ellipse area and the plantar pressure distribution on the affected side in static standing and using the anterior-posterior center of pressure displacement velocity (AP-COPV). They were also assessed using the Berg Balance Scale (BBS), the timed up-and-go test (TUGT), and the Activities-specific Balance Confidence Scale (ABC). Results:After the gaze stabilization exercises, the average envelope ellipse area, the plantar pressure distribution of the affected side with the eyes open and closed, AP-COPV, BBS score, TUGT time and ABC score of the experimental group were significantly superior to the control group′s averages and to the results four weeks previously.Conclusions:Gaze stabilization exercises can improve balance, weight shifting and one-leg standing after a stroke. That should enhance balance confidence and reduce the risk of falling.

Design and Development of a Rotating Chair to Measure the Cervico-Ocular Reflex.

Eye reflexes that stabilize gaze are essential in navigating daily life. One such reflex is the cervico-ocular reflex (COR). An important neural structure involved in the COR is the cerebellum, which facilitates proper gaze stability through sensorimotor integration to adjust eye movements accordingly. This reflex is tested by fixating the head in space and rotating the body around the neck. Thus, a rotating chair is needed to elicit proper cervical rotation while keeping the head fixed. The chair that was developed for this project was able to rotate to the specified amplitude (±0.5º of accuracy) and frequency. The parameters of the rotation amount, frequency, and amplitude can be adjusted as desired by the project guidelines. Our project aimed to improve upon existing chair models and develop a chair that can be used to assess the COR in neck pain populations.

Inflight head stabilization associated with wingbeat cycle and sonar emissions in the lingual echolocating Egyptian fruit bat, Rousettus aegyptiacus.

Sensory processing of environmental stimuli is challenged by head movements that perturb sensorimotor coordinate frames directing behaviors. In the case of visually guided behaviors, visual gaze stabilization results from the integrated activity of the vestibuloocular reflex and motor efference copy originating within circuits driving locomotor behavior. In the present investigation, it was hypothesized that head stabilization is broadly implemented in echolocating bats during sustained flight, and is temporally associated with emitted sonar signals which would optimize acoustic gaze. Predictions from these hypotheses were evaluated by measuring head and body kinematics with motion sensors attached to the head and body of free-flying Egyptian fruit bats. These devices were integrated with ultrasonic microphones to record sonar emissions and elucidate the temporal association with periods of head stabilization. Head accelerations in the Earth-vertical axis were asymmetric with respect to wing downstroke and upstroke relative to body accelerations. This indicated that inflight head and body accelerations were uncoupled, outcomes consistent with the mechanisms that limit vertical head acceleration during wing downstroke. Furthermore, sonar emissions during stable flight occurred most often during wing downstroke and head stabilization, supporting the conclusion that head stabilization behavior optimized sonar gaze and environmental interrogation via echolocation.

Fast tuning of posture control by visual feedback underlies gaze stabilization in walking Drosophila.

Locomotion requires a balance between mechanical stability and movement flexibility to achieve behavioral goals despite noisy neuromuscular systems, but rarely is it considered how this balance is orchestrated. We combined virtual reality tools with quantitative analysis of behavior to examine how Drosophila uses self-generated visual information (reafferent visual feedback) to control gaze during exploratory walking. We found that flies execute distinct motor programs coordinated across the body to maximize gaze stability. However, the presence of inherent variability in leg placement relative to the body jeopardizes fine control of gaze due to posture-stabilizing adjustments that lead to unintended changes in course direction. Surprisingly, whereas visual feedback is dispensable for head-body coordination, we found that self-generated visual signals tune postural reflexes to rapidly prevent turns rather than to promote compensatory rotations, a long-standing idea for visually guided course control. Together, these findings support a model in which visual feedback orchestrates the interplay between posture and gaze stability in a manner that is both goal dependent and motor-context specific.

Mechanisms of punctuated vision in fly flight.

To guide locomotion, animals control gaze via movements of their eyes, head, and/or body, but how the nervous system controls gaze during complex motor tasks remains elusive. In many animals, shifts in gaze consist of periods of smooth movement punctuated by rapid eye saccades. Notably, eye movements are constrained by anatomical limits, which requires resetting eye position. By studying tethered, flying fruit flies (Drosophila), we show that flies perform stereotyped head saccades to reset gaze, analogous to optokinetic nystagmus in primates. Head-reset saccades interrupted head smooth movement for as little as 50 ms-representing less than 5% of the total flight time-thereby enabling punctuated gaze stabilization. By revealing the passive mechanics of the neck joint, we show that head-reset saccades leverage the neck's natural elastic recoil, enabling mechanically assisted redirection of gaze. The consistent head orientation at saccade initiation, the influence of the head's angular position on saccade rate, the decrease in wing saccade frequency in head-fixed flies, and the decrease in head-reset saccade rate in flies with their head range of motion restricted together implicate proprioception as the primary trigger of head-reset saccades. Wing-reset saccades were influenced by head orientation, establishing a causal link between neck sensory signals and the execution of body saccades. Head-reset saccades were abolished when flies switched to a landing state, demonstrating that head movements are gated by behavioral state. We propose a control architecture for active vision systems with limits in sensor range of motion. VIDEO ABSTRACT.