Skip to main content
SpringerLink
Log in

Internal models of self-motion: computations that suppress vestibular reafference in early vestibular processing

  • Review
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

In everyday life, vestibular sensors are activated by both self-generated and externally applied head movements. The ability to distinguish inputs that are a consequence of our own actions (i.e., active motion) from those that result from changes in the external world (i.e., passive or unexpected motion) is essential for perceptual stability and accurate motor control. Recent work has made progress toward understanding how the brain distinguishes between these two kinds of sensory inputs. We have performed a series of experiments in which single-unit recordings were made from vestibular afferents and central neurons in alert macaque monkeys during rotation and translation. Vestibular afferents showed no differences in firing variability or sensitivity during active movements when compared to passive movements. In contrast, the analyses of neuronal firing rates revealed that neurons at the first central stage of vestibular processing (i.e., in the vestibular nuclei) were effectively less sensitive to active motion. Notably, however, this ability to distinguish between active and passive motion was not a general feature of early central processing, but rather was a characteristic of a distinct group of neurons known to contribute to postural control and spatial orientation. Our most recent studies have addressed how vestibular and proprioceptive inputs are integrated in the vestibular cerebellum, a region likely to be involved in generating an internal model of self-motion. We propose that this multimodal integration within the vestibular cerebellum is required for eliminating self-generated vestibular information from the subsequent computation of orientation and posture control at the first central stage of processing.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alstermark B, Pinter MJ, Sasaki S (1992a) Descending pathways mediating disynaptic excitation of dorsal neck motoneurones in the cat: facilitatory interactions. Neurosci Res 15:32–41

    Article  PubMed  CAS  Google Scholar 

  • Alstermark B, Pinter MJ, Sasaki S (1992b) Descending pathways mediating disynaptic excitation of dorsal neck motoneurones in the cat: brain stem relay. Neurosci Res 15:42–57

    Article  PubMed  CAS  Google Scholar 

  • Anastasopoulos D, Mergner T (1982) Canal-neck interaction in vestibular nuclear neurons of the cat. Exp Brain Res 46:269–280

    Article  PubMed  CAS  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 

  • Bell CC, Han VZ, Sugawara Y, Grant K (1999) Synaptic plasticity in the mormyrid electrosensory lobe. J Exp Biol 202:1339–1347

    PubMed  CAS  Google Scholar 

  • Blakemore SJ, Wolpert DM, Frith CD (1998) Central cancellation of self-produced tickle sensation. Nat Neurosci 1:635–640

    Article  PubMed  CAS  Google Scholar 

  • Blakemore SJ, Wolpert DM, Frith CD (1999a) The cerebellum contributes to somatosensory cortical activity during self-produced tactile stimulation. Neuroimage 10:448–459

    Article  PubMed  CAS  Google Scholar 

  • Blakemore SJ, Frith CD, Wolpert DM (1999b) Spatio-temporal prediction modulates the perception of self-produced stimuli. J Cogn Neurosci 11:551–559

    Article  PubMed  CAS  Google Scholar 

  • Boyle R, Highstein SM (1990a) Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10:1570–1582

    PubMed  CAS  Google Scholar 

  • Boyle R, Highstein SM (1990b) Resting discharge and response dynamics of horizontal semicircular canal afferents of the toadfish, Opsanus tau. J Neurosci 10:1557–1569

    PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • 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 781:244–263

    Article  PubMed  CAS  Google Scholar 

  • Brooks JX, Cullen KE (2009) Multimodal integration in rostral fastigial nucleus provides an estimate of body movement. J Neurosci 29:10499–10511

    Article  PubMed  CAS  Google Scholar 

  • Caston J, Bricout-Berthout A (1984) Responses to somatosensory input by afferent and efferent neurons in the vestibular nerve of the frog. Brain Behav Evol 24:135–143

    Article  PubMed  CAS  Google Scholar 

  • Chubb MC, Fuchs AF, Scudder CA (1984) Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements. J Neurophysiol 52:724–742

    PubMed  CAS  Google Scholar 

  • Cullen KE, McCrea RA (1993) Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. I. Secondary vestibular neurons. J Neurophysiol 70:828–843

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Cullen KE, Roy JE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933

    Article  PubMed  Google Scholar 

  • Dickman JD, Correia MJ (1993) Bilateral communication between vestibular labyrinths in pigeons. Neuroscience 57:1097–1108

    Article  PubMed  CAS  Google Scholar 

  • Fuchs AF, Kimm J (1975) Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol 38:1140–1161

    PubMed  CAS  Google Scholar 

  • Fukushima K (1997) Corticovestibular interactions: anatomy, electrophysiology, and functional considerations. Exp Brain Res 117:1–16

    Article  PubMed  CAS  Google Scholar 

  • Gacek RR, Lyon M (1974) The localization of vestibular efferent neurons in the kitten with horseradish peroxidase. Acta Otolaryngol 77:92–101

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Goldberg JM, Fernandez C (1980) Efferent vestibular system in the squirrel monkey: anatomical location and influence on afferent activity. J Neurophysiol 43:986–1025

    PubMed  CAS  Google Scholar 

  • Hartmann R, Klinke R (1980) Efferent activity in the goldfish vestibular nerve and its influence on afferent activity. Pflugers Arch 388:123–128

    Article  PubMed  CAS  Google Scholar 

  • Highstein SM (1991) The central nervous system efferent control of the organs of balance and equilibrium. Neurosci Res 12:13–30

    Article  PubMed  CAS  Google Scholar 

  • Highstein SM (1992) The efferent control of the organs of balance and equilibrium in the toadfish, Opsanus tau. Ann N Y Acad Sci 656:108–123

    Article  PubMed  CAS  Google Scholar 

  • Highstein SM, Baker R (1985) Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau. J Neurophysiol 54:370–384

    PubMed  CAS  Google Scholar 

  • Jamali M, Sadeghi SG, Cullen KE (2009) Response of vestibular nerve afferents innervating utricle and saccule during passive and active translations. J Neurophysiol 101:141–149

    Article  PubMed  Google Scholar 

  • Kalluri R, Xue J, Eatock RA (2010) Ion channels set spike timing regularity of Mammalian vestibular afferent neurons. J Neurophysiol 104:2034–2051

    Article  PubMed  Google Scholar 

  • Keller EL, Daniels PD (1975) Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey. Exp Neurol 46:187–198

    Article  PubMed  CAS  Google Scholar 

  • Kleine JF, Guan Y, Kipiani E, Glonti L, Hoshi M, Buttner U (2004) Trunk position influences vestibular responses of fastigial nucleus neurons in the alert monkey. J Neurophysiol 91:2090–2100

    Article  PubMed  CAS  Google Scholar 

  • Klinke R (1970) Efferent influence on the vestibular organ during active movements of the body. Pflugers Arch 318:325–332

    Article  PubMed  CAS  Google Scholar 

  • Kurzan R, Straube A, Buttner U (1993) The effect of muscimol micro-injections into the fastigial nucleus on the optokinetic response and the vestibulo-ocular reflex in the alert monkey. Exp Brain Res 94:252–260

    Article  PubMed  CAS  Google Scholar 

  • Lisberger SG, Miles FA (1980) Role of primate medial vestibular nucleus in long-term adaptive plasticity of vestibuloocular reflex. J Neurophysiol 43:1725–1745

    PubMed  CAS  Google Scholar 

  • Marlinski V, Plotnik M, Goldberg JM (2004) Efferent actions in the chinchilla vestibular labyrinth. J Assoc Res Otolaryngol 5:126–143

    PubMed  Google Scholar 

  • 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 82:416–428

    PubMed  CAS  Google Scholar 

  • Mergner T, Anastasopoulos D, Becker W, Deecke L (1981) Discrimination between trunk and head rotation; a study comparing neuronal data from the cat with human psychophysics. Acta Psychol (Amst) 48:291–301

    Article  CAS  Google Scholar 

  • Mergner T, Nardi GL, Becker W, Deecke L (1983) The role of canal-neck interaction for the perception of horizontal trunk and head rotation. Exp Brain Res 49:198–208

    Article  PubMed  CAS  Google Scholar 

  • Mergner T, Siebold C, Schweigart G, Becker W (1991) Human perception of horizontal trunk and head rotation in space during vestibular and neck stimulation. Exp Brain Res 85:389–404

    Article  PubMed  CAS  Google Scholar 

  • Mohr C, Roberts PD, Bell CC (2003) The mormyromast region of the mormyrid electrosensory lobe. I. Responses to corollary discharge and electrosensory stimuli. J Neurophysiol 90:1193–1210

    Article  PubMed  Google Scholar 

  • Myers SF, Salem HH, Kaltenbach JA (1997) Efferent neurons and vestibular cross talk in the frog. J Neurophysiol 77:2061–2070

    PubMed  CAS  Google Scholar 

  • Pélisson D, Goffart L, Guillaume A (1998) Contribution of the rostral fastigial nucleus to the control of orienting gaze shifts in the head-unrestrained cat. J Neurophysiol 80:1180–1196

    PubMed  Google Scholar 

  • Perachio AA, Kevetter GA (1989) Identification of vestibular efferent neurons in the gerbil: histochemical and retrograde labelling. Exp Brain Res 78:315–326

    Article  PubMed  CAS  Google Scholar 

  • Plotnik M, Marlinski V, Goldberg JM (2002) Reflections of efferent activity in rotational responses of chinchilla vestibular afferents. J Neurophysiol 88:1234–1244

    PubMed  Google Scholar 

  • Plotnik M, Marlinski V, Goldberg JM (2005) Efferent-mediated fluctuations in vestibular nerve discharge: a novel, positive-feedback mechanism of efferent control. J Assoc Res Otolaryngol 6:311–323

    PubMed  Google Scholar 

  • Roy JE, Cullen KE (1998) A neural correlate for vestibulo-ocular reflex suppression during voluntary eye-head gaze shifts. Nat Neurosci 1:404–410

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Roy JE, Cullen KE (2002) Vestibuloocular reflex signal modulation during voluntary and passive head movements. J Neurophysiol 87:2337–2357

    PubMed  Google Scholar 

  • Roy JE, Cullen KE (2003) Brain stem pursuit pathways: dissociating visual, vestibular, and proprioceptive inputs during combined eye-head gaze tracking. J Neurophysiol 90:271–290

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sadeghi SG, Minor LB, Cullen KE (2007a) Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. J Neurophysiol 97:1503–1514

    Article  PubMed  Google Scholar 

  • Sadeghi SG, Chacron MJ, Taylor MC, Cullen KE (2007b) Neural variability, detection thresholds, and information transmission in the vestibular system. J Neurosci 27:771–781

    Article  PubMed  CAS  Google Scholar 

  • Sadeghi SG, Goldberg JM, Minor LB, Cullen KE (2009) Efferent-mediated responses in vestibular nerve afferents of the alert macaque. J Neurophysiol 101:988–1001

    Article  PubMed  Google Scholar 

  • Sato H, Ohkawa T, Uchino Y, Wilson VJ (1997) Excitatory connections between neurons of the central cervical nucleus and vestibular neurons in the cat. Exp Brain Res 115:381–386

    Article  PubMed  CAS  Google Scholar 

  • Sawtell NB, Williams A, Bell CC (2007) Central control of dendritic spikes shapes the responses of Purkinje-like cells through spike timing-dependent synaptic plasticity. J Neurosci 27:1552–1565

    Article  PubMed  CAS  Google Scholar 

  • Scudder CA, Fuchs AF (1992) Physiological and behavioral identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J Neurophysiol 68:244–264

    PubMed  CAS  Google Scholar 

  • Shaikh AG, Meng H, Angelaki DE (2004) Multiple reference frames for motion in the primate cerebellum. J Neurosci 24:4491–4497

    Article  PubMed  CAS  Google Scholar 

  • Thach WT, Goodkin HP, Keating JG (1992) The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci 15:403–442

    Article  PubMed  CAS  Google Scholar 

  • Tomlinson RD, Robinson DA (1984) Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 51:1121–1136

    PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Voogd J, Gerrits NM, Ruigrok TJ (1996) Organization of the vestibulocerebellum. Ann N Y Acad Sci 781:553–579

    Article  PubMed  CAS  Google Scholar 

  • Wilson VJ (1991) Vestibulospinal and neck reflexes: interaction in the vestibular nuclei. Arch Ital Biol 129:43–52

    PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Yamada J, Noda H (1987) Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. J Comp Neurol 265:224–241

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Steve Nuara for assistance with animal care, and Walter Kucharski for excellent technical assistance, and D.E. Mitchell for critically reading this manuscript. This work was funded by Canadian Institutes of Health Research, Le Fonds québécois de la recherche sur la nature et les technologies, and the National Institute of Health (R01DC2390).

Author information

Authors and Affiliations

  1. Aerospace Medical Research Unit, Department of Physiology, McGill University, Montreal, PQ, H3G 1Y6, Canada

    Kathleen E. Cullen, Jessica X. Brooks, Mohsen Jamali, Jerome Carriot & Corentin Massot

Authors
  1. Kathleen E. Cullen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jessica X. Brooks
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mohsen Jamali
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jerome Carriot
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Corentin Massot
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kathleen E. Cullen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cullen, K.E., Brooks, J.X., Jamali, M. et al. Internal models of self-motion: computations that suppress vestibular reafference in early vestibular processing. Exp Brain Res 210, 377–388 (2011). https://doi.org/10.1007/s00221-011-2555-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-011-2555-9

Keywords

Search

Navigation