Erratum to: Dependency of human neck reflex responses on the bandwidth of pseudorandom anterior-posterior torso perturbations

The vestibulocollic (VCR) and cervicocollic (CCR) reflexes are essential to stabilize the head-neck system and to deal with unexpected disturbances. This study investigates how neck reflexes contribute to stabilization and modulate with perturbation properties. We hypothesized that VCR and CCR modulate with the bandwidth of the perturbation and that this modulation is maintained across amplitudes and influenced by the eyes being open or closed. Seated subjects were perturbed in an anterior-posterior direction. The perturbations varied in bandwidth from 0.3 Hz to a maximum of 1.2, 2.0, 4.0, and 8.0 Hz, at three amplitudes, and with eyes open and closed. Frequency response functions of head kinematics and neck muscle EMG demonstrated substantial changes with bandwidth and vision and minor changes with amplitude, which through closed-loop identification were attributed to neural (reflexive) modulation. Results suggest that both reflexes were attenuated when perturbations exceeded the system’s natural frequency, thereby shifting from a head-in-space to a head-on-trunk stabilization tendency. Additionally, results indicate that reflexive and mechanical stiffness marginally exceed the negative stiffness due to gravity; a stabilization strategy which minimizes effort. With eyes closed, reflexes were attenuated further, presumably due to a reduced ability to discriminate self-motion, driving the system to a head-on-trunk stabilization strategy at the highest bandwidth. We conclude that VCR and CCR modulate with perturbation bandwidth and visual feedback conditions to maintain head-upright posture, but are invariant across amplitude changes.

[1]  Frans C T van der Helm,et al.  Comparison of different methods to identify and quantify balance control. , 2005, Journal of neuroscience methods.

[2]  E. Keshner Head-trunk coordination during linear anterior-posterior translations. , 2003, Journal of neurophysiology.

[3]  田中 啓治 Analysis of Local and Wide-Field Movements in the Superior Temporal Visual Areas of the Macaque Monkey , 1987 .

[4]  R. Fitzpatrick,et al.  Acceleration patterns of the head and pelvis when walking on level and irregular surfaces. , 2003, Gait & posture.

[5]  R. Peterka Sensorimotor integration in human postural control. , 2002, Journal of neurophysiology.

[6]  Norman M. Wereley,et al.  Visual, vestibular and voluntary contributions to human head stabilization , 2004, Experimental Brain Research.

[7]  R. Kearney,et al.  Intrinsic and reflex contributions to human ankle stiffness: variation with activation level and position , 2000, Experimental Brain Research.

[8]  E. Keshner Modulating active stiffness affects head stabilizing strategies in young and elderly adults during trunk rotations in the vertical plane. , 2000, Gait & posture.

[9]  Rik Pintelon,et al.  System Identification: A Frequency Domain Approach , 2012 .

[10]  V. J. Wilson,et al.  The neural substrate of the vestibulocollic reflex , 1999, Experimental Brain Research.

[11]  G.C.Y. Peng,et al.  How is the head held up? Modeling mechanisms for head stability in the sagittal plane , 1996, Proceedings of 18th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[12]  B W Peterson,et al.  Reflex and mechanical contributions to head stabilization in alert cats. , 1986, Journal of neurophysiology.

[13]  Leonard A. Rozendaal,et al.  Stability of bipedal stance: the contribution of cocontraction and spindle feedback , 2003, Biological Cybernetics.

[14]  Ian David Loram,et al.  Direct measurement of human ankle stiffness during quiet standing: the intrinsic mechanical stiffness is insufficient for stability , 2002, The Journal of physiology.

[15]  Frans C. T. van der Helm,et al.  Quantifying Proprioceptive Reflexes During Position Control of the Human Arm , 2008, IEEE Transactions on Biomedical Engineering.

[16]  Jay M. Goldberg,et al.  Vestibular control of the head: possible functions of the vestibulocollic reflex , 2011, Experimental Brain Research.

[17]  Frans C. T. van der Helm,et al.  Identification of intrinsic and reflexive components of human arm dynamics during postural control , 2002, Journal of Neuroscience Methods.

[18]  B. Peterson,et al.  Spatial and temporal response properties of the vestibulocollic reflex in decerebrate cats. , 1985, Journal of neurophysiology.

[19]  B. Cohen,et al.  Effects of walking velocity on vertical head and body movements during locomotion , 1999, Experimental Brain Research.

[20]  G.C.Y. Peng,et al.  Predicting vestibular, proprioceptive, and biomechanical control strategies in normal and pathological head movements , 1999, IEEE Transactions on Biomedical Engineering.

[21]  D E Angelaki,et al.  Three-dimensional organization of otolith-ocular reflexes in rhesus monkeys. III. Responses To translation. , 1998, Journal of neurophysiology.

[22]  M. Lacour,et al.  Functional coupling of the stabilizing eye and head reflexes during horizontal and vertical linear motion in the cat , 2004, Experimental Brain Research.

[23]  P. Altevogt,et al.  Vesiclepedia: A Compendium for Extracellular Vesicles with Continuous Community Annotation , 2012, PLoS biology.

[24]  J. J. Collins,et al.  The effects of visual input on open-loop and closed-loop postural control mechanisms , 2004, Experimental Brain Research.

[25]  George Adelman,et al.  Encyclopedia of neuroscience , 2004 .

[26]  T. Kiemel,et al.  Identification of the plant for upright stance in humans: multiple movement patterns from a single neural strategy. , 2008, Journal of neurophysiology.

[27]  J S Reynolds,et al.  Reweighting sensory signals to maintain head stability: adaptive properties of the cervicocollic reflex. , 2008, Journal of neurophysiology.

[28]  P. Morasso,et al.  Direct measurement of ankle stiffness during quiet standing: implications for control modelling and clinical application. , 2005, Gait & posture.

[29]  B J Hess,et al.  Computation of Inertial Motion: Neural Strategies to Resolve Ambiguous Otolith Information , 1999, The Journal of Neuroscience.

[30]  J. Goldberg,et al.  Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. , 1976, Journal of neurophysiology.

[31]  François Klam,et al.  ã Federation of European Neuroscience Societies Visual±vestibular interactive responses in the macaque ventral intraparietal area (VIP) , 2022 .

[32]  R H Schor,et al.  The neural substrate of the vestibulocollic reflex. What needs to be learned. , 1999, Experimental brain research.

[33]  B. W. Peterson,et al.  A dynamical model for reflex activated head movements in the horizontal plane , 1996, Biological Cybernetics.

[34]  Frans C. T. van der Helm,et al.  Comparison of different methods to identify and quantify balance control , 2005, Journal of Neuroscience Methods.

[35]  R. Peterka,et al.  Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt. , 2000, Journal of neurophysiology.

[36]  S C Gandevia,et al.  Loop gain of reflexes controlling human standing measured with the use of postural and vestibular disturbances. , 1996, Journal of neurophysiology.

[37]  F. Richmond,et al.  Morphology and distribution of muscle spindles in dorsal muscles of the cat neck. , 1975, Journal of neurophysiology.

[38]  R. Stein,et al.  Identification of intrinsic and reflex contributions to human ankle stiffness dynamics , 1997, IEEE Transactions on Biomedical Engineering.

[39]  Adam D. Schneider,et al.  The Vestibular System Implements a Linear–Nonlinear Transformation In Order to Encode Self-Motion , 2012, PLoS biology.

[40]  D. G. Watts,et al.  Spectral analysis and its applications , 1968 .

[41]  B W Peterson,et al.  Mechanisms controlling human head stabilization. II. Head-neck characteristics during random rotations in the vertical plane. , 1995, Journal of neurophysiology.

[42]  R. J. Leigh,et al.  Frequency and velocity of rotational head perturbations during locomotion , 2004, Experimental Brain Research.

[43]  David A. Abbink,et al.  A rigorous model of reflex function indicates that position and force feedback are flexibly tuned to position and force tasks , 2009, Experimental Brain Research.

[44]  G. Gdowski,et al.  Head movements produced during whole body rotations and their sensitivity to changes in head inertia in squirrel monkeys. , 2008, Journal of neurophysiology.

[45]  A. Berthoz,et al.  Dynamics of the head-neck system in response to small perturbations: Analysis and modeling in the frequency domain , 1975, Biological Cybernetics.

[46]  G. DeAngelis,et al.  Visual and vestibular cue integration for heading perception in extrastriate visual cortex , 2011, The Journal of physiology.

[47]  M B Dutia,et al.  The sagittal vestibulocollic reflex and its interaction with neck proprioceptive afferents in the decerebrate cat. , 1985, The Journal of physiology.

[48]  Duane T. McRuer,et al.  A Review of Quasi-Linear Pilot Models , 1967 .

[49]  B. Peterson,et al.  Mechanisms controlling human head stabilization. I. Head-neck dynamics during random rotations in the horizontal plane. , 1995, Journal of neurophysiology.

[50]  A. Berthoz,et al.  Head stabilization during various locomotor tasks in humans , 2004, Experimental Brain Research.

[51]  B W Peterson,et al.  Cervicocollic reflex: its dynamic properties and interaction with vestibular reflexes. , 1985, Journal of neurophysiology.

[52]  Frank A. Pintar,et al.  Physical properties of the human head: mass, center of gravity and moment of inertia. , 2009, Journal of biomechanics.

[53]  T C Hain,et al.  Predicting control mechanisms for human head stabilization by altering the passive mechanics. , 1999, Journal of vestibular research : equilibrium & orientation.

[54]  Frank Bremmer,et al.  ã Federation of European Neuroscience Societies Heading encoding in the macaque ventral intraparietal area (VIP) , 2022 .

[55]  D M Merfeld,et al.  Humans use internal models to estimate gravity and linear acceleration , 1999, Nature.