Active Head Movements Research Articles

Penguin head movement detected using small accelerometers: a proxy of prey encounter rate

Determining temporal and spatial variation in feeding rates is essential for understanding the relationship between habitat features and the foraging behavior of top predators. In this study we examined the utility of head movement as a proxy of prey encounter rates in medium-sized Antarctic penguins, under the presumption that the birds should move their heads actively when they encounter and peck prey. A field study of free-ranging chinstrap and gentoo penguins was conducted at King George Island, Antarctica. Head movement was recorded using small accelerometers attached to the head, with simultaneous monitoring for prey encounter or body angle. The main prey was Antarctic krill (>99% in wet mass) for both species. Penguin head movement coincided with a slow change in body angle during dives. Active head movements were extracted using a high-pass filter (5 Hz acceleration signals) and the remaining acceleration peaks (higher than a threshold acceleration of 1.0 g) were counted. The timing of head movements coincided well with images of prey taken from the back-mounted cameras: head movement was recorded within ±2.5 s of a prey image on 89.1±16.1% (N=7 trips) of images. The number of head movements varied largely among dive bouts, suggesting large temporal variations in prey encounter rates. Our results show that head movement is an effective proxy of prey encounter, and we suggest that the method will be widely applicable for a variety of predators.

The Effects of Head Movement and Accurate Proprioceptive Feedback in Training of Sound Localization

We investigated the effects of listeners' head movement and proprioceptive feedback on the accuracy of sound localization. The effects were examined under the conditions that their head movement was restricted (study 1) or unrestricted (study 2) on the sound localization training. In both experiments, participants divided into two groups: training group performed the sound localization training with accurate proprioceptive feedback, while control group conducted the training with no-feedback. The results indicated that: (1) sound localization training under active head movements increased the accuracy of sound localization; (2) accurate proprioceptive feedback facilitated the sound localization during the initial training phase; and (3) training with the feedback dominantly decreased the rate of vertical localization errors in sound localization performance.

Temporal processing of active and passive head movement

The brain can know about an active head movement even in advance of its execution by means of an efference copy signal. In fact, sensory correlates of active movements appear to be suppressed. Passive disturbances of the head, however, can be detected only by sensory feedback. Might the perceived timing of an active head movement be speeded relative to the perception of a passive movement due to the efferent copy (anticipation hypothesis) or delayed because of sensory suppression (suppression hypothesis)? We compared the perceived timing of active and passive head movement using other sensory events as temporal reference points. Participants made unspeeded temporal order and synchronicity judgments comparing the perceived onset of active and passive head movement with the onset of tactile, auditory and visual stimuli. The comparison stimuli had to be delayed by about 45ms to appear coincident with passive head movement or by about 80ms to appear aligned with an active head movement. The slow perceptual reaction to vestibular activation is compatible with our earlier study using galvanic stimulation (Barnett-Cowan and Harris 2009). The unexpected additional delay in processing the timing of an active head movement is compatible with the suppression hypothesis and is discussed in relation to suppression of vestibular signals during self-generated head movement.

Characteristics of Head-Mounted Displays and Their Effects on Simulator Sickness

We examined the effects of several display characteristics of head-mounted displays (HMDs) on simulator sickness (SS). Technological limitations, such as display delay and reduced field of view (FOV), affect perception when using an HMD and are often thought to be related to SS. Few studies have examined the relationship between FOV and geometric FOV (image scale factor) or how HMD characteristics may interact. Participants made active head movements to locate objects when viewing a live video via an HMD. Compared with no added delay, an additional 200 ms of display delay did not result in increased SS, as measured by the Simulator Sickness Questionnaire. Furthermore, an effect of image scale factor on SS was not revealed. However, SS was greater when peripheral vision was occluded than when it was not. Peripheral vision moderated the effects of image scale factor and delay on head movement velocity. Occluding peripheral vision may subject HMD users to the potential detrimental consequences of HMD characteristics more than when peripheral vision of the external environment is available, resulting in more SS. Future research should investigate to what extent peripheral vision can be occluded without increasing SS and without sacrificing realism and presence. To reduce the occurrence of SS, a degree of peripheral vision of the external world should be provided. Furthermore, users and designers should be aware that head movement behavior may be affected by HMD characteristics.

Vestibular control of the head: possible functions of the vestibulocollic reflex

Here, we review the angular vestibulocollic reflex (VCR) focusing on its function during unexpected and voluntary head movements. Theoretically, the VCR could (1) stabilize the head in space during body movements and/or (2) dampen head oscillations that could occur as a result of the head's underdamped mechanics. The reflex appears unaffected when the simplest, trisynaptic VCR pathways are severed. The VCR's efficacy varies across species; in humans and monkeys, head stabilization is ineffective during low-frequency body movements in the yaw plan. While the appearance of head oscillations after the attenuation of semicircular canal function suggests a role in damping, this interpretation is complicated by defects in the vestibular input to other descending motor pathways such as gaze premotor circuits. Since the VCR should oppose head movements, it has been proposed that the reflex is suppressed during voluntary head motion. Consistent with this idea, vestibular-only (VO) neurons, which are possible vestibulocollic neurons, respond vigorously to passive, but not active, head rotations. Although VO neurons project to the spinal cord, their contribution to the VCR remains to be established. VCR cancelation during active head movements could be accomplished by an efference copy signal negating afferent activity related to active motion. Oscillations occurring during active motion could be eliminated by some combination of reflex actions and voluntary motor commands that take into account the head's biomechanics. A direct demonstration of the status of the VCR during active head movements is required to clarify the function of the reflex.

Multimodal Integration After Unilateral Labyrinthine Lesion: Single Vestibular Nuclei Neuron Responses and Implications for Postural Compensation

Plasticity in neuronal responses is necessary for compensation following brain lesions and adaptation to new conditions and motor learning. In a previous study, we showed that compensatory changes in the vestibuloocular reflex (VOR) following unilateral vestibular loss were characterized by dynamic reweighting of inputs from vestibular and extravestibular modalities at the level of single neurons that constitute the first central stage of VOR signal processing. Here, we studied another class of neurons, i.e., the vestibular-only neurons, in the vestibular nuclei that mediate vestibulospinal reflexes and provide information for higher brain areas. We investigated changes in the relative contribution of vestibular, neck proprioceptive, and efference copy signals in the response of these neurons during compensation after contralateral vestibular loss in Macaca mulata monkeys. We show that the time course of recovery of vestibular sensitivity of neurons corresponds with that of lower extremity muscle and tendon reflexes reported in previous studies. More important, we found that information from neck proprioceptors, which did not influence neuronal responses before the lesion, were unmasked after lesion. Such inputs influenced the early stages of the compensation process evidenced by faster and more substantial recovery of the resting discharge in proprioceptive-sensitive neurons. Interestingly, unlike our previous study of VOR interneurons, the improvement in the sensitivity of the two groups of neurons did not show any difference in the early or late stages after lesion. Finally, neuronal responses during active head movements were not different before and after lesion and were attenuated relative to passive movements over the course of recovery, similar to that observed in control conditions. Comparison of compensatory changes observed in the vestibuloocular and vestibulospinal pathways provides evidence for similarities and differences between the two classes of neurons that mediate these pathways at the functional and cellular levels.

Eye-head coordination in the guinea pig II. Responses to self-generated (voluntary) head movements

Retinal image stability is essential for vision but may be degraded by head movements. The vestibulo-ocular reflex (VOR) compensates for passive perturbations of head position and is usually assumed to be the major neural mechanism for ocular stability. During our recent investigation of vestibular reflexes in guinea pigs free to move their heads (Shanidze et al. in Exp Brain Res, 2010), we observed compensatory eye movements that could not have been initiated either by vestibular or neck proprioceptive reflexes because they occurred with zero or negative latency with respect to head movement. These movements always occurred in association with self-generated (active) head or body movements and thus anticipated a voluntary movement. We found the anticipatory responses to differ from those produced by the VOR in two significant ways. First, anticipatory responses are characterized by temporal synchrony with voluntary head movements (latency approximately 1 versus approximately 7 ms for the VOR). Second, the anticipatory responses have higher gains (0.80 vs. 0.46 for the VOR) and thus more effectively stabilize the retinal image during voluntary head movements. We suggest that anticipatory responses act synergistically with the VOR to stabilize retinal images. Furthermore, they are independent of actual vestibular sensation since they occur in guinea pigs with complete peripheral vestibular lesions. Conceptually, anticipatory responses could be produced by a feed-forward neural controller that transforms efferent motor commands for head movement into estimates of the sensory consequences of those movements.

High-Velocity Angular Vestibulo-Ocular Reflex Adaptation to Position Error Signals

Vestibular rehabilitation strategies including gaze stabilization exercises have been shown to increase gain of the angular vestibulo-ocular reflex (aVOR) using a retinal slip error signal (ES). The identification of additional ESs capable of promoting substitution strategies or aVOR adaptation is an important goal in the management of vestibular hypofunction. Position ESs have been shown to increase both aVOR gain and recruitment of compensatory saccades (CSs) during passive whole body rotation. This may be a useful compensatory strategy for gaze instability during active head rotation as well. In vestibular rehabilitation, the imaginary target exercise is often prescribed to improve gaze stability. This exercise uses a position ES; however, the mechanism for its effect has not been investigated. We compared aVOR gain adaptation using 2 types of small position ES: constant versus incremental. Ten subjects with normal vestibular function were assessed with unpredictable and active head rotations before and after a 20-minute training session. Subjects performed 9 epochs of 40 active, high-velocity head impulses using a position ES stimulus to increase aVOR gain. Five subjects demonstrated significant aVOR gain increases with the constant-position ES (mean, 2%; range, -18% to 12%) compared with another 5 subjects showing significant aVOR gain increases to the incremental-position ES (mean, 3.7%; range, -2% to 22.6%). There was no difference in aVOR gain adaptation or CS recruitment between the 2 paradigms. These findings suggest that some subjects can increase their aVOR gain in response to high-velocity active head movement training using a position ES. The primary mechanism for this seems to be aVOR gain adaptation because CS use was not modified. The overall low change in aVOR gain adaptation with position ES suggests that retinal slip is a more powerful aVOR gain modifier.

Effect of Drivers' Active Head Movements on Motion Sickness

Effect of Drivers' Active Head Movements on Motion Sickness

Effect of Driver's Head Tilt Strategy on Motion Sickness Incidence

Car drivers receive the acceleration stimulation and the rotational stimulation when negotiating with a curve. In such a situation, the driver controls his/her posture such as the head and the body appropriately. It is known that the driver tilts his/her head toward the curve direction while the passengers’ head movement is likely to occur in the opposite direction. There are some interpretations of the role of the driver's active head movement such as increasing visibility and decreasing of effect of the inertial force to the body including the trunk and the neck. The goals of this research are to understand relationship between head tilt strategy and motion sickness incidence and apply its result to the design of comfortable vehicle motion. First, we derive a mathematical model of the motion sickness incidence caused by the head movement in 3D space based on subjective vertical conflict. Then, we analyze effect of the head movement on decrease of motion sickness incidence using the mathematical model.

Methodological approach and road safety system evaluation

Car drivers receive the acceleration stimulation and the rotational stimulation when negotiating with a curve. In such a situation, the driver controls his/her posture such as the head and the body appropriately. It is known that the driver tilts his/her head toward the curve direction while the passengers’ head movement is likely to occur in the opposite direction. There are some interpretations of the role of the driver's active head movement such as increasing visibility and decreasing of effect of the inertial force to the body including the trunk and the neck. The goals of this research are to understand relationship between head tilt strategy and motion sickness incidence and apply its result to the design of comfortable vehicle motion. First, we derive a mathematical model of the motion sickness incidence caused by the head movement in 3D space based on subjective vertical conflict. Then, we analyze effect of the head movement on decrease of motion sickness incidence using the mathematical model.

Neurophysiology and computational neuroscience

Issues 3–4 of the 200th volume of Experimental Brain Research are devoted to neurophysiology and computational neuroscience. Neurophysiology has remained a major focus of Experimental Brain Research since the founding of the journal in 1966 by an editorial board that included Sir John Eccles. Issue 3 continues this long tradition by including two reviews and Wve original articles that use or consider neurophysiological approaches to provide insights into sensory processing and sensorimotor integration by the nervous system. Issue 3 begins with a review by Green and Angelaki regarding the processing of sensory inputs by the vestibular system. The vestibular system is vital for motor control and spatial motion perception. Over the years, studies of the vestibular system have served as an excellent model framework for investigating the basic strategies by which sensory signals are transformed into central representations that give rise to behavior. For this reason, Experimental Brain Research has published over 1,000 manuscripts related to the vestibular system. In the review by Green and Angelaki, the authors describe recent advances in identifying the neural correlates for a number of fundamental computations and transformations of vestibular signals implemented by brainstem–cerebellar circuits. These include the sensorimotor transformations for reXex generation, the neural computations for inertial motion estimation, the distinction between active and passive head movements, as well as the integration of vestibular and proprioceptive information for body motion estimation. The authors emphasize why the study of these problems has revealed important organizational principles (e.g., the concept of “internal models”, multisensory integration, reaVerence, reference frame transformations) that are generally relevant for all sensorimotor systems. Although explicit neural correlates for such computations (e.g., internal models) have often been diYcult to identify in other systems (e.g., limb control circuits), this review emphasizes the signiWcant advances made in so doing in the vestibular system. As a result, studies of this system continue to have great potential to yield new insights into common neural processing strategies relevant for both reXexive and goal-directed, voluntary movement as well as perception. A second review by Rizzolatti and Fabbri-Destro on the mirror neurone system begins with a short historical account of the important role of Experimental Brain Research in publishing much of the early animal work on mirror neurons at the end of the 1980s and early 1990s. Professor Rizzolatti recalls that in those days, Nature failed to recognize the importance of the work and declined publication. He was in good company: the same journal had earlier rejected the Nobel prize-winning work of Otto Krebs on the citric acid cycle. The bulk of the review focuses on the rapidly expanding literature on the mirror neurone system in humans which has been made possible by advances in neuroimaging, transcranial brain stimulation and clever behavioral experiments. These have led to an explosion of interest that had never been anticipated in the early days. Indeed, the relevance of the mirror neuron system to cognition J. C. Rothwell (&) UCL Institute of Neurology, Queen Square, London WC1N 3BG, UK e-mail: j.rothwell@ion.ucl.ac.uk

Internal models and neural computation in the vestibular system.

The vestibular system is vital for motor control and spatial self-motion perception. Afferents from the otolith organs and the semicircular canals converge with optokinetic, somatosensory and motor-related signals in the vestibular nuclei, which are reciprocally interconnected with the vestibulocerebellar cortex and deep cerebellar nuclei. Here, we review the properties of the many cell types in the vestibular nuclei, as well as some fundamental computations implemented within this brainstem-cerebellar circuitry. These include the sensorimotor transformations for reflex generation, the neural computations for inertial motion estimation, the distinction between active and passive head movements, as well as the integration of vestibular and proprioceptive information for body motion estimation. A common theme in the solution to such computational problems is the concept of internal models and their neural implementation. Recent studies have shed new insights into important organizational principles that closely resemble those proposed for other sensorimotor systems, where their neural basis has often been more difficult to identify. As such, the vestibular system provides an excellent model to explore common neural processing strategies relevant both for reflexive and for goal-directed, voluntary movement as well as perception.

Visual fields, eye movements, and scanning behavior of a sit-and-wait predator, the black phoebe (Sayornis nigricans)

Foraging mode influences the dominant sensory modality used by a forager and likely the strategies of information gathering used in foraging and anti-predator contexts. We assessed three components of visual information gathering in a sit-and-wait avian predator, the black phoebe (Sayornis nigricans): configuration of the visual field, degree of eye movement, and scanning behavior through head-movement rates. We found that black phoebes have larger lateral visual fields than similarly sized ground-foraging passerines, as well as relatively narrower binocular and blind areas. Black phoebes moved their eyes, but eye movement amplitude was relatively smaller than in other passerines. Black phoebes may compensate for eye movement constraints with head movements. The rate of head movements increased before attacking prey in comparison to non-foraging contexts and before movements between perches. These findings suggest that black phoebes use their lateral visual fields, likely subtended by areas of high acuity in the retina, to track prey items in a three-dimensional space through active head movements. These head movements may increase depth perception, motion detection and tracking. Studying information gathering through head movement changes, rather than body posture changes (head-up, head-down) as generally presented in the literature, may allow us to better understand the mechanisms of information gathering from a comparative perspective.

Effects of canal plugging on the vestibuloocular reflex and vestibular nerve discharge during passive and active head rotations.

Mechanical occlusion (plugging) of the slender ducts of semicircular canals has been used in the clinic as well as in basic vestibular research. Here, we investigated the effect of canal plugging in two macaque monkeys on the horizontal vestibuloocular reflex (VOR) and the responses of vestibular-nerve afferents during passive head rotations. Afferent responses to active head movements were also studied. The horizontal VOR gain decreased after plugging to <0.1 for frequencies <2 Hz but rose to about 0.6 as frequency was increased to 15 Hz. Afferents innervating plugged horizontal canals had response sensitivities that increased with the frequency of passive rotations from <0.01 (spikes/s)/( degrees/s) at 0.5 Hz to values of about 0.2 and 0.5 (spikes/s)/( degrees/s) at 8 Hz for regular and irregular afferents, respectively (<50% of responses in controls). An increase in phase lead was also noted following plugging in afferent discharge, but not in the VOR. Because the phase discrepancy between the VOR and afferent discharge is much larger than that seen in control animals, this suggests that central adaptation shapes VOR dynamics following plugging. The effect of canal plugging on afferent responses can be modeled as an increase in stiffness and a reduction in the dominant time constant and gain in the transfer function describing canal dynamics. Responses were also evident during active head rotations, consistent with the frequency content of these movements. We conclude that canal plugging in macaques is effective only at frequencies <2 Hz. At higher frequencies, afferents show significant responses, with a nearly 90 degrees phase lead, such that they encode near-rotational acceleration. Our results demonstrate that afferents innervating plugged canals respond robustly during voluntary movements, a finding that has implications for understanding the effects of canal plugging in clinical practice.

How Actions Alter Sensory Processing

Our vestibular organs are simultaneously activated by our own actions as well as by stimulation from the external world. The ability to distinguish sensory inputs that are a consequence of our own actions (vestibular reafference) from those that result from changes in the external world (vestibular exafference) is essential for perceptual stability and accurate motor control. Recent work in our laboratory has focused on understanding how the brain distinguishes between vestibular reafference and exafference. Single-unit recordings were made in alert rhesus monkeys during passive and voluntary (i.e., active) head movements. We found that neurons in the first central stage of vestibular processing (vestibular nuclei), but not the primary vestibular afferents, can distinguish between active and passive movements. In order to better understand how neurons differentiate active from passive head motion, we systematically tested neuronal responses to different combinations of passive and active motion resulting from rotation of the head-on-body and/or head-and-body in space. We found that during active movements, a cancellation signal was generated when the activation of proprioceptors matched the motor-generated expectation.

Different neural strategies for multimodal integration: comparison of two macaque monkey species

The integration of neck proprioceptive and vestibular inputs underlies the generation of accurate postural and motor control. Recent studies have shown that central mechanisms underlying the integration of these sensory inputs differ across species. Notably, in rhesus monkey (Macaca mulata), an Old World monkey, neurons in the vestibular nuclei are insensitive to passive stimulation of neck proprioceptors. In contrast, in squirrel monkey, a New World monkey, stimulation produces robust modulation. This has led to the suggestion that there are differences in how sensory information is integrated during self-motion in Old versus New World monkeys. To test this hypothesis, we recorded from neurons in the vestibular nuclei of another species in the Macaca genus [i.e., M. fascicularis (cynomolgus monkey)]. Recordings were made from vestibular-only (VO) and position-vestibular-pause (PVP) neurons. The majority (53%) of neurons in both groups were sensitive to neck proprioceptive and vestibular stimulation during passive body-under-head and whole-body rotation, respectively. Furthermore, responses during passive rotations of the head-on-body were well predicted by the linear summation of vestibular and neck responses (which were typically antagonistic). During active head movement, the responses of VO and PVP neurons were further attenuated (relative to a model based on linear summation) for the duration of the active head movement or gaze shift, respectively. Taken together, our findings show that the brain's strategy for the central processing of sensory information can vary even within a single genus. We suggest that similar divergence may be observed in other areas in which multimodal integration occurs.

Vestibular guidance of active head movements

Vestibular sensors provide precise and timely information about head velocity in space. It is well established that this information is used to stabilize eyes, head and body against movements from outside, i.e., passive movements. Here, we investigate whether vestibular information also helps to monitor and guide active head movements during gaze shifts. We measured head movements during large gaze shifts toward briefly flashed targets in humans with complete vestibular loss (vestibular subjects) and in healthy controls before and after increasing their head moment of inertia. Whereas normally head movements oscillate neither in vestibular subjects nor in controls, the increase in head moment of inertia caused marked head oscillations only in vestibular subjects. We conclude that vestibular information plays an important role in the on-line guidance of active head movements and helps to correct for unexpected changes such as additional torque imposed by an increase in moment of inertia.

Gaze stabilization and gait performance in vestibular dysfunction

Background The gaze stability test (GST) quantifies the ability of a person to recognize a target projected on a personal computer monitor during active head movement. Purpose The purpose of this study was to determine if there was a relationship between clinical measures of walking performance and the GST in patients with vestibular disorders and in healthy subjects. We hypothesized that impairment of the ability to keep objects in focus during active head movement would be correlated with walking performance. Subjects Twenty older asymptomatic adults acted as controls and 12 patients with either unilateral or bilateral vestibular disease participated. Methods The GST quantifies the maximum velocity that a person can move their head in the pitch and yaw planes while retaining the ability to read an optotype that is momentarily projected onto a computer screen. Subjects were scored while performing the Dynamic Gait Index (DGI) and the Timed “Up & Go” (TUG) tests. Results Walking performance on the DGI and TUG were significantly associated with GST results in subjects with vestibular disorders, but not in control subjects. Abnormalities of gait could be identified by GST cutoff values of 65° s −1 in the pitch plane and 63° s −1 in the yaw plane. Discussion/conclusion In older subjects with vestibular disorders, gaze stability, as assessed by the GST, is associated with reduced test scores on measures of gait performance.

Cervical helical axis characteristics and its center of rotation during active head and upper arm movements—comparisons of whiplash-associated disorders, non-specific neck pain and asymptomatic individuals

The helical axis model can be used to describe translation and rotation of spine segments. The aim of this study was to investigate the cervical helical axis and its center of rotation during fast head movements (side rotation and flexion/extension) and ball catching in patients with non-specific neck pain or pain due to whiplash injury as compared with matched controls. The aim was also to investigate correlations with neck pain intensity. A finite helical axis model with a time-varying window was used. The intersection point of the axis during different movement conditions was calculated. A repeated-measures ANOVA model was used to investigate the cervical helical axis and its rotation center for consecutive levels of 15° during head movement. Irregularities in axis movement were derived using a zero-crossing approach. In addition, head, arm and upper body range of motion and velocity were observed. A general increase of axis irregularity that correlated to pain intensity was observed in the whiplash group. The rotation center was superiorly displaced in the non-specific neck pain group during side rotation, with the same tendency for the whiplash group. During ball catching, an anterior displacement (and a tendency to an inferior displacement) of the center of rotation and slower and more restricted upper body movements implied a changed movement strategy in neck pain patients, possibly as an attempt to stabilize the cervical spine during head movement.