Skip to main content
SpringerLink
Log in

Vestibulocollic Reflexes

  • Chapter
The Vestibular System

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 19))

4. Summary

This chapter examined the functional properties and neural substrates of a key vestibulospinal reflex—the vestibular-neck or vestibulocollic reflex (VCR). Functionally, the VCR is a dynamic stabilizing system that shapes head movements, particularly in the critical 1–3 Hz range where the head-neck system exhibits resonant instability. VCR circuits are designed to suppress reflex responses to active, intended head motions, leaving the reflex free to oppose unwanted oscillations or motions induced by external perturbations. A great deal is known about the anatomy and physiology of neurons that comprise the central leg of the important three-neuron VCR reflex arcs. These include both lateral and medial vestibulospinal tract neurons. The latter can be functionally divided into two classes. One carries unmodified signals from semicircular canals to a wide array of motoneurons. Included in this class are the branching vestibulooculocollic neurons. The second class selectively targets small groups of motoneurons and carries a processed canal signal that is presumably designed to control a small synergistic group of muscles. During active gaze shifts, many vestibulooculocollic neurons cease discharging. Vestibulocollic neurons, on the other hand, continue discharging and responding to externally applied head motions while ignoring the canal activation produced by the active head movements. The mechanisms responsible for this behavior are under active investigation. It also remains to be seen how these neurons participate in reflexes generated by activation of otolith receptors.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Akaike T (1983) Neuronal organization of the vestibulospinal system in the cat. Brain Res 259:217–227.

    Article  CAS  PubMed  Google Scholar 

  • Akaike T, Fanardjian VV, Ito M, Kumada M, Nakajima H (1973) Electrophysiological analysis of the vestibulospinal reflex pathway of rabbit. I. Classification of tract cells. Exp Brain Res 17:477–496.

    CAS  PubMed  Google Scholar 

  • Baker J, Goldberg J, Peterson B (1985) Spatial and temporal response properties of the vestibulocollic reflex in decerebrate cats. J Neurophysiol 54:735–756.

    CAS  PubMed  Google Scholar 

  • Banovetz JM, Peterson BW, Baker JF (1995) Spatial coordination by descending vestibular signals. 1. Reflex excitation of neck muscles in alert and decerebrate cats. Exp Brain Res 105:345–362.

    CAS  PubMed  Google Scholar 

  • Batton RR III, Jayaraman A, Ruggiero D, Carpenter MB (1977) Fastigial efferent projections in the monkey, an autoradiographic study. J Comp Neurol 174: 281–305.

    Article  PubMed  Google Scholar 

  • Bilotto G, Goldberg J, Peterson BW, Wilson VJ (1982) Dynamic properties of vestibular reflexes in the decerebrate cat. Exp Brain Res 47(3):343–352.

    Article  CAS  PubMed  Google Scholar 

  • Bolton PS, Endo K, Goto T, Imagawa M, Sasaki M, Uchino Y, Wilson VJ (1992) Connections between utricular nerve and dorsal neck motoneurons of the decerebrate cat. J Neurophysiol 67(6): 1695–1697.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Boyle R (1997) Activity of lateral vestibulospinal neurons during applied linear and angular head acceleration in the alert squirrel monkey. Soc Neurosci Abstr 23:753.

    Google Scholar 

  • Boyle R (2000) Morphology of lumbar-projecting lateral vestibulospinal neurons in the brainstem and cervical spinal cord in the squirrel monkey. Arch Ital Biol 138:107–122.

    CAS  PubMed  Google Scholar 

  • Boyle R, Pompeiano O (1979) Frequency response characteristics of vestibulospinal neurons during sinusoidal neck rotation. Brain Res 173:344–349.

    Article  CAS  PubMed  Google Scholar 

  • Boyle R, Pompeiano O (1981) Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons. J Neurophysiol 45:852–868.

    CAS  PubMed  Google Scholar 

  • Boyle R, Moschovakis AK (1993) Vestibular control of head movement in squirrel monkey: morphology of individual vestibulospinal axons. Soc Neurosci Abstr 19:138.

    Google Scholar 

  • Boyle R, Goldberg JM, Highstein SM (1992) Inputs from regularly and irregularly discharging vestibular nerve afferents to secondary neurons in the vestibular nuclei of the squirrel monkey. III. Correlation with vestibulospinal and vestibuloocular output pathways. J Neurophysiol 68:471–484.

    CAS  PubMed  Google Scholar 

  • Boyle R, Belton T, McCrea RA (1996) Responses of identified vestibulospinal neurons to voluntary and reflex eye and head movements in the alert squirrel monkey. Am NY Acad Sci 781:244–263.

    CAS  Google Scholar 

  • Dutia MB (1988) Interaction between vestibulocollic and cervicocollic reflexes: automatic compensation of reflex gain by muscle afferents. Prog Brain Res 76:173–180.

    CAS  PubMed  Google Scholar 

  • Fukushima K (1987) The intersitial nucleus of Cajal and its role in the control of movements of head and eyes. Prog Neurobiol 29:107–192.

    Article  CAS  PubMed  Google Scholar 

  • Fukushima K, Peterson BW, Wilson VJ (1978) Vestibulospinal, reticulospinal and interstitiospinal pathways in the cat. Prog Brain Res 50:121–136.

    Google Scholar 

  • Fukushima K, Ohno M, Kato M (1981) Responses of cat mesencephalic reticulospinal neurons to stimulation of superior colliculus, pericruciate cortex, and neck muscle afferents. Exp Brain Res 44:441–444.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gdowski G, Boyle R, McCrea RA (2000) Sensory processing in the vestibular nuclei during active head movements. Arch Ital Biol 138:15–28.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Hongo T, Kitami T, Yoshida K (1988) Integration of vestibular and neck signals in the central cervical nucleus. Prog Brain Res 76:155–162.

    CAS  PubMed  Google Scholar 

  • Ikegami H, Sasaki M, Uchino Y (1994) Connections between utricular nerve and neck flexor motoneurons of decerebrate cats. Exp Brain Res 98:373–378.

    Article  CAS  PubMed  Google Scholar 

  • Imai T, Moore ST, Raphan T, Cohen B (2001) Interaction of the body, head, and eyes during walking and turning. Exp Brain Res 136(1):1–18.

    Article  CAS  PubMed  Google Scholar 

  • Isu N, Yokota J (1983) Morphophysiological study on the divergent projection of axon collaterals of medial vestibular neurons in the cat. Exp Brain Res 53:151–162.

    Article  CAS  PubMed  Google Scholar 

  • Isu N, Uchino Y, Nakashima H, Satoh S, Ichikawa T, Watanabe S (1988) Axonal trajectories of posterior canal-activated secondary vestibular neurons and their coactivation of extraocular and neck flexor motoneurons in the cat. Exp Brain Res 70:181–191.

    CAS  PubMed  Google Scholar 

  • Isu N, Sakuma A, Hiranuma K, Uchino H, Sasaki S-I, Imagawa M, Uchino Y (1991) The neuronal organization of horizontal semicircular canal-activated inhibitory vestibulocollic neurons in the cat. Exp Brain Res 86:9–17.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Keshner EA, Baker JF, Banovetz J, Peterson BW (1992) Patterns of neck muscle activation in cats during reflex and voluntary head movements. Exp Brain Res 88:361–374.

    Article  CAS  PubMed  Google Scholar 

  • 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 73:2302–2312.

    CAS  PubMed  Google Scholar 

  • Keshner EA, Statler KD, Delp S (1997) Kinematics of the freely moving head and neck in the alert cat. Exp Brain Res 115:257–266.

    Article  CAS  PubMed  Google Scholar 

  • 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 38:337–347.

    Article  CAS  PubMed  Google Scholar 

  • Kokkoroyannis T, Scudder CA, Balaban CD, Highstein SM, Moschovakis AK (1996) Anatomy and physiology of the primate intersitial nucleus of Cajal. I. Efferent projections. J Neurophysiol 75:725–739.

    CAS  PubMed  Google Scholar 

  • Lacour M, Borel L (1989) Functional coupling of the stabilizing gaze reflexes during vertical linear motion in the alert cat. Prog Brain Res 80:385–394.

    CAS  PubMed  Google Scholar 

  • Lacour M, Borel L, Barthelemy J, Harlay F, Xerri C (1987) Dynamic properties of the vertical otolith neck reflexes in the alert cat. Exp Brain Res 65:559–568.

    Article  CAS  PubMed  Google Scholar 

  • McCrea RA, Strassman A, May E, Highstein SM (1987a) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflexes of the squirrel monkey. J Comp Neurol 264:547–570.

    CAS  PubMed  Google Scholar 

  • McCrea RA, Strassman A, Highstein SM (1987b) Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflexes of the squirrel monkey. J Comp Neurol 264:571–592.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Minor LB, McCrea RA, Goldberg JM (1990) Dual projections of secondary vestibular axons in the medial longitudinal fasciculus to extraocular motor nuclei and the spinal cord of the squirrel monkey. Exp Brain Res 83:9–21.

    Article  CAS  PubMed  Google Scholar 

  • Newlands SD, Ling L, Phillips JO, Siebold C, Duckert L, Fuchs AF (1999) Short-and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization. J Neurophysiol 81:2119–2130.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Perlmutter SI, Iwamoto Y, Baker JF, Peterson BW (1998a) Interdependence of spatial properties and projection patterns of medial vestibulospinal tract neurons in the cat. J Neurophysiol 79:270–284.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Perlmutter SI, Iwamoto Y, Baker JF, Peterson BW (1999) Spatial alignment of rotational and static tilt responses of vestibulospinal neurons in the cat. J Neurophysiol 82:855–862.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Peterson BW, Goldberg J, Bilotto G, Fuller JH (1985) Cervicocollic reflex: its dynamic properties and interaction with vestibular reflexes. J Neurophysiol 54: 90–109.

    CAS  PubMed  Google Scholar 

  • Peterson BW, Pitts NG, Fukushima K, Mackel R (1978) Reticulospinal excitation and inhibition of neck motoneurons. Exp Brain Res 32:471–489.

    CAS  PubMed  Google Scholar 

  • Rapoport S, Susswein A, Uchino Y, Wilson VJ (1977a) Properties of vestibular neurones projecting to neck segments of the cat spinal cord. J Physiol (Lond) 268:493–510.

    CAS  Google Scholar 

  • Rapoport S, Susswein A, Uchino Y, Wilson VJ (1977b) Synaptic actions of individual vestibular neurones on cat neck motoneurones. J Physiol (Lond) 272:367–382.

    CAS  Google Scholar 

  • Richmond FJR, Scott DA, Abrahams VC (1978) Distribution of motoneurones to the neck muscles, biventer cervicis, splenius and complexus in the cat. J Comp Neurol 181:451–464.

    Article  CAS  PubMed  Google Scholar 

  • Schor RH, Miller AD (1981) Vestibular reflexes in neck and forelimb muscles evoked by roll tilt. J Neurophysiol 46:167–178.

    CAS  PubMed  Google Scholar 

  • Schor RH, Miller AD, Tomko DL (1984) Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. J Neurophysiol 51: 136–146.

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Ohgaki T, Futami T, Sugiuchi Y (1988a) Vestibular projections to the spinal cord: the morphology of single vestibulospinal axons. Prog Brain Res 76:17–27.

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Ohgaki T, Sugiuchi Y, Futami T (1988b) Structural basis for three-dimensional coding in the vestibulospinal reflex: morphology of single vestibulospinal axons in the cervical cord. Ann N Y Acad Sci 545:216–227.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Shinoda Y, Ohgaki T, Sugiuchi Y, Futami T, Kakei S (1992b) Functional synergies of neck muscles innervated by single medial vestibulospinal axons. Ann N Y Acad Sci 656:507–518.

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Sugiuchi Y, Futami T, Ando N, Kawasaki T (1994) Input patterns and pathways from six semicircular canals to motoneurons of neck muscles. I. The multifidus muscle group. J Neurophysiol 72:2691–2702.

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Sugiuchi Y, Futami T, Kakei S, Izawa Y, Na J (1996) Four convergent patterns of input from the six semicircular canals to motoneurons of different neck muscles in the upper cervical cord. Ann N Y Acad Sci 781:264–275.

    CAS  PubMed  Google Scholar 

  • Shinoda Y, Sugiuchi Y, Futami T, Ando N, Yagi J (1997) Input patterns and path-ways from six semicircular canals to motoneurons of neck muscles. II. The longissimus and semispinalis muscle groups. J Neurophysiol 77:1234–1258.

    CAS  PubMed  Google Scholar 

  • Strassman A, Highstein SM, McCrea RA (1986) Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. II. Inhibitory burst neurons. J Comp Neurol 249:358–380.

    CAS  PubMed  Google Scholar 

  • Suzuki JI, Cohen B (1966) Integration of semicircular canal activity. J Neurophysiol 29(6):981–995.

    CAS  PubMed  Google Scholar 

  • Szentágothai J (1951) Short propriospinal neurons and intrinsic connections of the spinal grey matter. Acta Morphol Acad Sci Hung 1:81–94.

    Google Scholar 

  • Uchino Y (2001) Otolith and semicircular canal inputs to single vestibular neurons in cat. Jpn Biol Sci Space 15:375–381.

    CAS  Google Scholar 

  • Uchino Y, Hirai N (1984) Axon collaterals of anterior semicircular canal-activated vestibular neurons and their coactivation of extraocular and neck motoneurons in the cat. Neurosci Res 1:309–325.

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Wickland CR, Baker JF, Peterson BW (1991) Torque vectors of neck muscles in the cat. Exp Brain Res 84:649–659.

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wilson VJ, Peterson BW (1988) Vestibular and reticular projections to the neck. In: Peterson BW, Richmond FJ (eds) Control of Head Movement. New York: Oxford University Press, pp. 129–140.

    Google Scholar 

  • Wilson VJ, Kato M, Peterson BW, Wylie RM (1967) A single-unit analysis of the organization of Deiters’ nucleus. J Neurophysiol 30:603–619.

    CAS  PubMed  Google Scholar 

  • Wilson VJ, Uchino Y, Maunz RA, Susswein A, Fukushima K (1978) Properties and connections of cat fastigiospinal neurons. Exp Brain Res 32:1–17.

    Article  CAS  PubMed  Google Scholar 

  • Wilson VJ, Peterson BW, Fukushima K, Hirai N, Uchino Y (1979) Analysis of vestibulocollic reflexes by sinusoidal polarization of vestibular afferent fibers. J Neurophysiol 42:331–346.

    CAS  PubMed  Google Scholar 

  • Wilson VJ, Yamagata Y, Yates BJ, Schor RH, Nonaka S (1990) Response of vestibular neurons to head rotations in vertical planes. III. Response of vestibulocollic neurons to vestibular and neck stimulation. J Neurophysiol 64:1695–1703.

    CAS  PubMed  Google Scholar 

  • Wilson VJ, Boyle R, Fukushima K, Rose PK, Shinoda Y, Sugiuchi Y (1995) The vestibulocollic reflex. J Vestib Res 5:147–170.

    Article  CAS  PubMed  Google Scholar 

Download references

Authors
  1. Barry W. Peterson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard D. Boyle
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Otolaryngology, Washington University School of Medicine, St. Louis, MO, 63110, USA

    Stephen M. Highstein

  2. Department of Psychology and Parmly Hearing Institute, Loyola University of Chicago, Chicago, IL, 60626, USA

    Richard R. Fay

  3. Department of Biology and Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD, 20742-4415, USA

    Arthur N. Popper

Rights and permissions

Reprints and permissions

Copyright information

© 2004 Springer-Verlag New York, Inc.

About this chapter

Cite this chapter

Peterson, B.W., Boyle, R.D. (2004). Vestibulocollic Reflexes. In: Highstein, S.M., Fay, R.R., Popper, A.N. (eds) The Vestibular System. Springer Handbook of Auditory Research, vol 19. Springer, New York, NY. https://doi.org/10.1007/0-387-21567-0_8

Download citation

  • DOI: https://doi.org/10.1007/0-387-21567-0_8

  • Publisher Name: Springer, New York, NY

  • Print ISBN: 978-0-387-98314-1

  • Online ISBN: 978-0-387-21567-9

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation