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01-05-2011 | REVIEW

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

Authors: Jay M. Goldberg, Kathleen E. Cullen

Published in: Experimental Brain Research | Issue 3-4/2011

Abstract

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.

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Angelaki DE, Cullen KE (2008) Vestibular system: the many facets of a multimodal sense. Annu Rev Neurosci 31:125–150PubMedCrossRef

Baker J, Goldberg J, Peterson B, Schor R (1982) Oculomotor reflexes after semicircular canal plugging in cats. Brain Res 252:151–155PubMedCrossRef

Berthoz A, Anderson JH (1971) Frequency analysis of vestibular influence on extensor motoneurons. II. Relationship between neck and forelimb extensors. Brain Res 34:376–380PubMedCrossRef

Bilotto G, Goldberg J, Peterson BW, Wilson VJ (1982) Dynamic properties of vestibular reflexes in the decerebrate cat. Exp Brain Res 47:343–352PubMedCrossRef

Bizzi E (1981) Eye-head coordination. In: Brooks VB (ed) Handbook of physiology the nervous system section 1 volume 2 part 2. American Physiological Society, Bethesda, pp 1321–1336

Boyle R (1993) Activity of medial vestibulospinal tract cells during rotation and ocular movement in the alert squirrel monkey. J Neurophysiol 70:2176–2180PubMed

Boyle R, Belton T, McCrea RA (1996) Responses of identified vestibulospinal neurons to voluntary eye and head movements in the squirrel monkey. Ann N Y Acad Sci 781:244–263PubMedCrossRef

Bronstein AM, Hood JD (1986) The cervico-ocular reflex in normal subjects and patients with absent vestibular function. Brain Res 373:399–408PubMedCrossRef

Carey JP, Della Santina CC (2005) Principles of applied vestibular physiology. In: Cummings CC (ed) Otolaryngology—head & neck surgery, vol 4, 4th edn. Elsevier Mosby, Philadelphia, pp 3115–3159

Colebatch JG, Halmagyi GM, Skuse NF (1994) Myogenic potentials generated by a click-evoked vestibulocollic reflex. J Neurol Neurosurg Psychiatry 57:190–197PubMedCrossRef

Cullen KE, Minor LB (2002) Semicircular canal afferents similarly encode active and passive head-on-body rotations: implications for the role of vestibular efference. J Neurosci 22:RC226

Cullen KE (2004) Sensory signals during active versus passive movement. Curr Opin Neurobiol 14:698–706PubMedCrossRef

Cullen KE, Huterer M, Braidwood DA, Sylvestre PA (2004) Time course of vestibuloocular reflex suppression during gaze shifts. J Neurophysiol 92:3408–3422PubMedCrossRef

Decety J (1996) Neural representations for action. Rev Neurosci 7:285–297PubMed

Dutia MB, Hunter MJ (1985) The sagittal vestibulocollic reflex and its interaction with neck proprioceptive afferents in the decerebrate cat. J Physiol 359:17–29PubMed

Ewald JR (1892) Physiologische Untersuchungen über das Endorgan des Nervus octavus. Wiesbaden, Bergmann

Ezure K, Sasaki S (1978) Frequency-response analysis of vestibular-induced neck reflex in cat. I. Characteristics of neural ransmission from horizontal semicircular canal to neck motoneurons. J Neurophysiol 41:445–458PubMed

Ezure K, Sasaki S, Uchino Y, Wilson VJ (1978) Frequency-response analysis of vestibular-induced neck reflex in cat. II. Functional significance of cervical afferents and polysynaptic descending pathways. J Neurophysiol 41:459–471PubMed

Farrer C, Franck N, Paillard J, Jeannerod M (2003) The role of proprioception in action recognition. Conscious Cogn 12:609–619PubMedCrossRef

Flourens M (1824) Recherches expérimentales sur les propriétés du système nerveux dans les animaux vertébrés.. Paris

Freedman EG (2001) Interactions between eye and head control signals can account for movement kinematics. Biol Cybern 84:453–462PubMedCrossRef

Freedman EG (2008) Coordination of the eyes and head during visual orienting. Exp Brain Res 190:369–387PubMedCrossRef

Freedman EG, Sparks DL (2000) Coordination of the eyes and head: movement kinematics. Exp Brain Res 131:22–32PubMedCrossRef

Fukushima K, Ohashi T, Fukushima J (1994) Effects of chemical deactivation of the interstitial nucleus of Cajal on the vertical vestibulo-collic reflex induced by pitch rotation in alert cats. Neurosci Res 20:281–286PubMedCrossRef

Galiana HL, Guitton D (1992) Central organization and modeling of eye-head coordination during orienting gaze shifts. Ann N Y Acad Sci 656:452–471

Gdowski GT, McCrea RA (1999) Integration of vestibular and head movement signals in the vestibular nuclei during whole-body rotation. J Neurophysiol 82:436–449PubMed

Ghez C, Martin JH (1982) The control of rapid limb movement in the cat. III. Agonist—antagonist coupling. Exp Brain Res 45:115–125PubMedCrossRef

Gioanni H (1988) Stabilizing gaze reflexes in the pigeon (Columba livia). I. Horizontal and vertical optokinetic eye (OKN) and head (OCR) reflexes. Exp Brain Res 69:567–582PubMedCrossRef

Goldberg JM, Fernandez C (1975) Responses of peripheral vestibular neurons to angular and linear accelerations in the squirrel monkey. Acta Otolaryngol 80:101–110PubMedCrossRef

Goldberg J, Peterson BW (1986) Reflex and mechanical contributions to head stabilization in alert cats. J Neurophysiol 1986 56:857–875

Graf W, de Waele C, Vidal PP (1995a) Functional anatomy of the head-neck movement system of quadrupedal and bipedal mammals. J Anat 186(1):55–74PubMed

Graf W, de Waele C, Vidal PP, Wang DH, Evinger C (1995b) The orientation of the cervical vertebral column in unrestrained awake animals. II. Movement strategies. Brain Behav Evol 45:209–231PubMedCrossRef

Grantyn A, Berthoz A (1987) Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I. Behavioral properties. Exp Brain Res 66:339–354PubMedCrossRef

Grantyn A, Ong-Meang Jacques V, Berthoz A (1987) Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. II. Morphological properties as revealed by intra-axonal injections of horseradish peroxidase. Exp Brain Res 66:355–377PubMedCrossRef

Guitton D (1992) Control of eye-head coordination during orienting gaze shifts. Trends Neurosci 15:174–179

Guitton D, Volle M (1987) Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J Neurophysiol 58:427–459PubMed

Guitton D, Kearney RE, Wereley N, Peterson BW (1986) Visual, vestibular and voluntary contributions to human head stabilization. Exp Brain Res 64:59–69PubMedCrossRef

Guitton D, Bergeron A, Choi WY, Matsuo S (2003) On the feedback control of orienting gaze shifts made with eye and head movements. Prog Brain Res 142:55–68PubMedCrossRef

Hallett M, Shahani BT, Young RR (1975) EMG analysis of stereotyped voluntary movements in man. J Neurol Neurosurg Psychiatry 38:1154–1162PubMedCrossRef

Hannaford B, Won SK, Lee SH, Stark L (1986) Neurological control of head movements: inverse modeling and electromyography. Math Biosci 78:159–178CrossRef

Harada Y, Taniguchi M, Namatame H, Iida A (2001) Magnetic materials in otoliths of bird and fish lagena and their function. Acta Otolaryngol 121:590–595PubMedCrossRef

Highstein SM, Ito M, Tsuchiya T (1971) Synaptic linkage in the vestibulo-ocular reflex pathway of rabbit. Exp Brain Res 113:306–326PubMed

Horak FB, MacPherson JM (1996) Postural orientation and equilibrium. In: Rowell LB, Shepherd JT (eds) Handbook of physiology. Section 12. Exercise, regulation and integration of multiple systems. Oxford University Press, New York, pp 255–292

Huterer M, Cullen KE (2002) Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in rhesus monkey. J Neurophysiol 88:13–28PubMed

Ito M, Nisimaru N, Yamamoto M (1976a) Pathways for the vestibulo-ocular reflex excitation arising from semicircular canals of rabbits. Exp Brain Res 24:257–271PubMed

Ito M, Nisimaru N, Yamamoto M (1976b) Postsynaptic inhibition of oculomotor neurons involved in vestibulo-ocular reflexes arising from semicircular canals of rabbits. Exp Brain Res 24:273–283PubMed

Ito Y, Corna S, von Brevern M, Bronstein A, Gresty M (1997) The functional effectiveness of neck muscle reflexes for head-righting in response to sudden fall. Exp Brain Res 117(2):266–272PubMedCrossRef

Jex HR, Magdaleno RE (1978) Biomechanical models for vibration feedthrough to hands and head for a semisupine pilot. Aviat Space Environ Med 49:304–316PubMed

Kawato M (1999) Internal models for motor control and trajectory planning. Curr Opin Neurobiol 9:718–727PubMedCrossRef

Keshner EA (2000) Modulating active stiffness affects head stabilizing strategies in young and elderly adults during trunk rotations in the vertical plane. Gait Posture 11:1–11PubMedCrossRef

Keshner EA, Peterson BW (1995) Mechanisms controlling human head stabilization. I. Head-neck characteristics during random rotations in the horizontal plane. J Neurophysiol 73:2293–2301PubMed

Keshner EA, Cromwell RL, Peterson BW (1995) Mechanisms controlling human head stabilization. II. Head-neck characteristics during random rotations in the vertical plane. J Neurophysiol 73:2302–2312PubMed

Kitama T, Grantyn A, Berthoz A (1995) Orienting-related eye-neck neurons of the medial ponto-bulbar reticular formation do not participate in horizontal canal-dependent vestibular reflexes of alert cats. Brain Res Bull 38:337–347PubMedCrossRef

Korte GE (1979) The brainstem projection of the vestibular nerve in the cat. J Comp Neurol 184:279–292PubMedCrossRef

Laurutis VP, Robinson DA (1986) The vestibulo-ocular reflex during human saccadic eye movements. J Physiol 373:209–233PubMed

Leigh RJ, Zee DS (2006) Eye-head movements. In the neurology of eye movements. Oxford, New York, pp 315–342

Lorente de Nó R (1933) Vestibulo-ocular reflex arc. Arch Neurol Psychiat 30:245–291

McCrea RA, Gdowski GT, Boyle R, Belton T (1999) Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. J Neurophysiol 82:416–428PubMed

McGill SM, Jones K, Bennett G, Bishop PJ (1994) Passive stiffness of the human neck in flexion, extension, and lateral bending. Clin Biomech 9:193–198CrossRef

Melvill Jones G (2000) Chapter 41: Posture. In: Kandel ER, Schwartz JH, Jessell TM (eds) Principles of neural science, 4th edn. McGraw-Hill: New York, p 816–831

Money KE, Correia KE (1972) The vestibular system of the owl. Comp Biochem Physiol 42A:353–358CrossRef

Money KE, Scott JW (1962) Functions of separate sensory receptors of nonauditory labyrinth of the cat. Am J Physiol 202:1211–1220PubMed

Moore ST, Hirasaki E, Cohen B, Raphan T (1999) Effect of viewing distance on the generation of vertical eye movements during locomotion. Exp Brain Res 129:347–361PubMedCrossRef

Moser EI, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain’s spatial representation system. Annu Rev Neurosci 31:69–89PubMedCrossRef

Paige GD (1983) Vestibuloocular reflex and its interactions with visual following mechanisms in the squirrel monkey. II. Response characteristics and plasticity following unilateral inactivation of horizontal canal. J Neurophysiol 49:152–168PubMed

Peng GC, Hain TC, Peterson BW (1996) A dynamical model for reflex activated head movements in the horizontal plane. Biol Cybern 75:309–319PubMedCrossRef

Peng GC, Hain TC, Peterson BW (1999) Predicting vestibular, proprioceptive, and biomechanical control strategies in normal and pathological head movements. IEEE Trans Biomed Eng 46:1269–1280PubMedCrossRef

Peng GC, Minor LB, Zee DS (2004) Coupled asymmetries of the vestibulo-ocular (VOR) and vestibulocollic (VCR) reflexes in patients with unilateral vestibular loss (UVL). Soc Neurosci Abstr 23:1294

Perlmutter SI, Iwamoto Y, Barke LF, Baker JF, Peterson BW (1998) Relation between axon morphology in C1 spinal cord and spatial properties of medial vestibulospinal tract neurons in the cat. J Neurophysiol 79:285–303PubMed

Peterson BW, Boyle R (2004) Vestibulocollic reflexes. In: Highstein SM, Fay RR, Popper AN (eds) The vestibular system. Springer, New York, pp 343–374CrossRef

Peterson BW, Fukushima K, Hirai N, Schor RH, Wilson VJ (1980) Responses of vestibulospinal and reticulospinal neurons to sinusoidal vestibular stimulation. J Neurophysiol 43:1236–1250PubMed

Peterson BW, Choi H, Hain T, Keshner E, Peng GC (2001) Dynamic and kinematic strategies for head movement control. Ann N Y Acad Sci 942:381–393PubMedCrossRef

Pozzo T, Berthoz A, Lefort L (1990) Head stabilization during various locomotor tasks in humans. I. Normal subjects. Exp Brain Res 82:97–106PubMedCrossRef

Pozzo T, Berthoz A, Lefort L, Vitte E (1991) Head stabilization during various locomotor tasks in humans. II. Patients with bilateral peripheral vestibular deficits. Exp Brain Res 85:208–217PubMedCrossRef

Rabbitt RD, Boyle R, Highstein SM (1999) Influence of surgical plugging on horizontal semicircular canal mechanics and afferent response dynamics. J Neurophysiol 82:1033–1053PubMed

Reynolds JS, Gdowski GT (2008) Head movements produced during whole body rotations and their sensitivity to changes in head inertia in squirrel monkeys. J Neurophysiol 95:2369–2382CrossRef

Robinson DA (1982) The use of matrices in analyzing the three-dimensional behavior of the vestibulo-ocular reflex. Biol Cybern 46:53–66PubMedCrossRef

Robinson FR, Phillips JO, Fuchs AF (1994) Coordination of gaze shifts in primates: brainstem inputs to neck and extraocular motoneuron pools. J Comp Neurol 346:43–62PubMedCrossRef

Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131–2142PubMed

Roy JE, Cullen KE (2004) Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci 24:2102–2111PubMedCrossRef

Sadeghi SG, Goldberg JM, Minor LB, Cullen KE (2009) Effects of canal plugging on the vestibuloocular reflex and vestibular nerve discharge during passive and active head rotations. J Neurophysiol 102:2693–2703PubMedCrossRef

Sadeghi SG, Minor LB, Cullen KE. (in press) Multimodal integration after unilateral labyrinthine lesion: single vestibular nuclei neuron responses and implications for postural compensation. J Neurophysiol. (Epub. 2010 Dec 8)

Schor RH (1974) Responses of cat vestibular neurons to sinusoidal roll tilt. Exp Brain Res 20:347–362PubMedCrossRef

Scott SH, Norman KE (2003) Computational approaches to motor control and their potential role for interpreting motor dysfunction. Curr Opin Neurol 16:693–698

Shinoda Y, Ohgaki T, Sugiuchi Y, Futami T (1992) Morphology of single medial vestibulospinal tract axons in the upper cervical spinal cord of the cat. J Comp Neurol 316:151–172PubMedCrossRef

Shinoda Y, Sugiuchi Y, Izawa Y, Hata Y (2006) Long descending motor tract axons and their control of neck and axial muscles. Prog Brain Res 151:527–563PubMedCrossRef

Shupert CL, Horak FB (1996) Effects of vestibular loss on head stabilization in response to head and body perturbations. J Vestib Res 6:423–437PubMedCrossRef

Sparks DL (2002) The brainstem control of saccadic eye movements. Nat Rev Neurosci 3:952–964PubMedCrossRef

Sugiuchi Y, Kakei S, Izawa Y, Shinoda Y (2004) Functional synergies among neck muscles revealed by branching patterns of single long descending motor-tract axons. Prog Brain Res 143:411–421PubMedCrossRef

Suzuki JI, Cohen B (1964) Head, eye, body and limb movements from semicircular canal nerves. Exp Neurol 10:393–405PubMedCrossRef

Sylvestre PA, Cullen KE (2006) Premotor correlates of integrated feedback control for eye-head gaze shifts. J Neurosci 26:4922–4929PubMedCrossRef

Szentagothai J (1950) The elementary vestibulo-ocular reflex arc. J Neurophysiol 395–407

Tabak S, Smeets JB, Collewijn H (1996) Modulation of the human vestibuloocular reflex during saccades: probing by high-frequency oscillation and torque pulses of the head. J Neurophysiol 76:3249–3263PubMed

Taube JS (2007) The head direction signal: origins and sensory-motor integration. Annu Rev Neurosci 30:181–207PubMedCrossRef

Terzuolo CA, Soechting JF, Viviani P (1973) Studies on the control of some simple motor tasks. I. Relations between parameters of movements and EMG activities. Brain Res 58:212–216PubMedCrossRef

Thomson DB, Ikegami H, Wilson VJ (1995) Effect of MLF transection on the vertical vestibulocollic reflex in decerebrate cats. J Neurophysiol 74:1815–1818PubMed

Tomko DL, Peterka RJ, Schor RH, O’Leary DP (1981) Response dynamics of horizontal canal afferents in barbiturate-anesthetized cats. J Neurophysiol 45:376–396PubMed

Tomlinson RD, Bahra PS (1986) Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibuloocular reflex. J Neurophysiol 56:1558–1570PubMed

Uchino YSM, Sato H, Bai R, Kawamoto E (2005) Otolith and canal integration on single vestibular neurons in cats. Brain Res 271–285

von Holst E, Mittelstaedt H (1950) Das reafferenzprinzip. Naturwissenschaften 37:464–476CrossRef

Welgampola MS, Colebatch JG (2005) Characteristics and clinical applications of vestibular-evoked myogenic potentials. Neurology 64:1682–1688PubMedCrossRef

Wilson VJ, Maeda M (1974) Connections between semicircular canals and neck motoneurons in the cat. J Neurophysiol 37:346–357PubMed

Wilson VJ, Schor RH (1999) The neural substrate of the vestibulocollic reflex. What needs to be learned. Exp Brain Res 129:483–493PubMedCrossRef

Wilson VJ, Yoshida M (1969) Monosynaptic inhibition of neck motoneurons by the medial vestibular nucleus. Brain Res 11:365–380

Winklhofer M, Kirschvink JL (2010) A quantitative assessment of torque-transducer models for magnetoreception. J R Soc Interface 7(2):S273–S289

Winters JM, Stark L (1985) Analysis of fundamental human movement patterns through the use of in-depth antagonistic muscle models. IEEE Trans Biomed Eng 32:826–839PubMedCrossRef

Wolpert DM, Ghahramani Z, Jordan MI (1995) Are arm trajectories planned in kinematic or dynamic coordinates? An adaptation study. Exp Brain Res 103:460–470PubMedCrossRef

Zangemeister WH, Stark L (1981) Active head rotations and eye-head coordination. Ann N Y Acad Sci 374:540–559PubMedCrossRef

Title: Vestibular control of the head: possible functions of the vestibulocollic reflex
Authors: Jay M. Goldberg
Kathleen E. Cullen
Publication date: 01-05-2011
Publisher: Springer-Verlag
Published in: Experimental Brain Research / Issue 3-4/2011
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI: https://doi.org/10.1007/s00221-011-2611-5

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

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