Advertisement

Experimental Brain Research

, Volume 210, Issue 3–4, pp 377–388 | Cite as

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

  • Kathleen E. Cullen
  • Jessica X. Brooks
  • Mohsen Jamali
  • Jerome Carriot
  • Corentin Massot
Review

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.

Keywords

Vestibular nucleus Cerebellum Internal model Active/passive Reafference Afferent Self-motion Vestibular reflexes 

Notes

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).

References

  1. Alstermark B, Pinter MJ, Sasaki S (1992a) Descending pathways mediating disynaptic excitation of dorsal neck motoneurones in the cat: facilitatory interactions. Neurosci Res 15:32–41PubMedCrossRefGoogle Scholar
  2. Alstermark B, Pinter MJ, Sasaki S (1992b) Descending pathways mediating disynaptic excitation of dorsal neck motoneurones in the cat: brain stem relay. Neurosci Res 15:42–57PubMedCrossRefGoogle Scholar
  3. Anastasopoulos D, Mergner T (1982) Canal-neck interaction in vestibular nuclear neurons of the cat. Exp Brain Res 46:269–280PubMedCrossRefGoogle Scholar
  4. Batton RR III, Jayaraman A, Ruggiero D, Carpenter MB (1977) Fastigial efferent projections in the monkey: an autoradiographic study. J Comp Neurol 174:281–305PubMedCrossRefGoogle Scholar
  5. Bell CC, Han VZ, Sugawara Y, Grant K (1999) Synaptic plasticity in the mormyrid electrosensory lobe. J Exp Biol 202:1339–1347PubMedGoogle Scholar
  6. Blakemore SJ, Wolpert DM, Frith CD (1998) Central cancellation of self-produced tickle sensation. Nat Neurosci 1:635–640PubMedCrossRefGoogle Scholar
  7. Blakemore SJ, Wolpert DM, Frith CD (1999a) The cerebellum contributes to somatosensory cortical activity during self-produced tactile stimulation. Neuroimage 10:448–459PubMedCrossRefGoogle Scholar
  8. Blakemore SJ, Frith CD, Wolpert DM (1999b) Spatio-temporal prediction modulates the perception of self-produced stimuli. J Cogn Neurosci 11:551–559PubMedCrossRefGoogle Scholar
  9. Boyle R, Highstein SM (1990a) Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents. J Neurosci 10:1570–1582PubMedGoogle Scholar
  10. Boyle R, Highstein SM (1990b) Resting discharge and response dynamics of horizontal semicircular canal afferents of the toadfish, Opsanus tau. J Neurosci 10:1557–1569PubMedGoogle Scholar
  11. Boyle R, Pompeiano O (1981) Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons. J Neurophysiol 45:852–868PubMedGoogle Scholar
  12. 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 781:244–263PubMedCrossRefGoogle Scholar
  13. Brooks JX, Cullen KE (2009) Multimodal integration in rostral fastigial nucleus provides an estimate of body movement. J Neurosci 29:10499–10511PubMedCrossRefGoogle Scholar
  14. 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 24:135–143PubMedCrossRefGoogle Scholar
  15. Chubb MC, Fuchs AF, Scudder CA (1984) Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements. J Neurophysiol 52:724–742PubMedGoogle Scholar
  16. 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 70:828–843PubMedGoogle Scholar
  17. 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:RC226PubMedGoogle Scholar
  18. Cullen KE, Roy JE (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91:1919–1933PubMedCrossRefGoogle Scholar
  19. Dickman JD, Correia MJ (1993) Bilateral communication between vestibular labyrinths in pigeons. Neuroscience 57:1097–1108PubMedCrossRefGoogle Scholar
  20. Fuchs AF, Kimm J (1975) Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol 38:1140–1161PubMedGoogle Scholar
  21. Fukushima K (1997) Corticovestibular interactions: anatomy, electrophysiology, and functional considerations. Exp Brain Res 117:1–16PubMedCrossRefGoogle Scholar
  22. Gacek RR, Lyon M (1974) The localization of vestibular efferent neurons in the kitten with horseradish peroxidase. Acta Otolaryngol 77:92–101PubMedCrossRefGoogle Scholar
  23. Gdowski GT, McCrea RA (1999) Integration of vestibular and head movement signals in the vestibular nuclei during whole-body rotation. J Neurophysiol 82:436–449PubMedGoogle Scholar
  24. Goldberg JM, Fernandez C (1980) Efferent vestibular system in the squirrel monkey: anatomical location and influence on afferent activity. J Neurophysiol 43:986–1025PubMedGoogle Scholar
  25. Hartmann R, Klinke R (1980) Efferent activity in the goldfish vestibular nerve and its influence on afferent activity. Pflugers Arch 388:123–128PubMedCrossRefGoogle Scholar
  26. Highstein SM (1991) The central nervous system efferent control of the organs of balance and equilibrium. Neurosci Res 12:13–30PubMedCrossRefGoogle Scholar
  27. Highstein SM (1992) The efferent control of the organs of balance and equilibrium in the toadfish, Opsanus tau. Ann N Y Acad Sci 656:108–123PubMedCrossRefGoogle Scholar
  28. Highstein SM, Baker R (1985) Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau. J Neurophysiol 54:370–384PubMedGoogle Scholar
  29. Jamali M, Sadeghi SG, Cullen KE (2009) Response of vestibular nerve afferents innervating utricle and saccule during passive and active translations. J Neurophysiol 101:141–149PubMedCrossRefGoogle Scholar
  30. Kalluri R, Xue J, Eatock RA (2010) Ion channels set spike timing regularity of Mammalian vestibular afferent neurons. J Neurophysiol 104:2034–2051PubMedCrossRefGoogle Scholar
  31. Keller EL, Daniels PD (1975) Oculomotor related interaction of vestibular and visual stimulation in vestibular nucleus cells in alert monkey. Exp Neurol 46:187–198PubMedCrossRefGoogle Scholar
  32. 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 91:2090–2100PubMedCrossRefGoogle Scholar
  33. Klinke R (1970) Efferent influence on the vestibular organ during active movements of the body. Pflugers Arch 318:325–332PubMedCrossRefGoogle Scholar
  34. 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 94:252–260PubMedCrossRefGoogle Scholar
  35. Lisberger SG, Miles FA (1980) Role of primate medial vestibular nucleus in long-term adaptive plasticity of vestibuloocular reflex. J Neurophysiol 43:1725–1745PubMedGoogle Scholar
  36. Marlinski V, Plotnik M, Goldberg JM (2004) Efferent actions in the chinchilla vestibular labyrinth. J Assoc Res Otolaryngol 5:126–143PubMedGoogle Scholar
  37. 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 82:416–428PubMedGoogle Scholar
  38. 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) 48:291–301CrossRefGoogle Scholar
  39. 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 49:198–208PubMedCrossRefGoogle Scholar
  40. 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 85:389–404PubMedCrossRefGoogle Scholar
  41. 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 90:1193–1210PubMedCrossRefGoogle Scholar
  42. Myers SF, Salem HH, Kaltenbach JA (1997) Efferent neurons and vestibular cross talk in the frog. J Neurophysiol 77:2061–2070PubMedGoogle Scholar
  43. 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 80:1180–1196PubMedGoogle Scholar
  44. Perachio AA, Kevetter GA (1989) Identification of vestibular efferent neurons in the gerbil: histochemical and retrograde labelling. Exp Brain Res 78:315–326PubMedCrossRefGoogle Scholar
  45. Plotnik M, Marlinski V, Goldberg JM (2002) Reflections of efferent activity in rotational responses of chinchilla vestibular afferents. J Neurophysiol 88:1234–1244PubMedGoogle Scholar
  46. 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 6:311–323PubMedGoogle Scholar
  47. Roy JE, Cullen KE (1998) A neural correlate for vestibulo-ocular reflex suppression during voluntary eye-head gaze shifts. Nat Neurosci 1:404–410PubMedCrossRefGoogle Scholar
  48. Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131–2142PubMedGoogle Scholar
  49. Roy JE, Cullen KE (2002) Vestibuloocular reflex signal modulation during voluntary and passive head movements. J Neurophysiol 87:2337–2357PubMedGoogle Scholar
  50. Roy JE, Cullen KE (2003) Brain stem pursuit pathways: dissociating visual, vestibular, and proprioceptive inputs during combined eye-head gaze tracking. J Neurophysiol 90:271–290PubMedCrossRefGoogle Scholar
  51. Roy JE, Cullen KE (2004) Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci 24:2102–2111PubMedCrossRefGoogle Scholar
  52. 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 97:1503–1514PubMedCrossRefGoogle Scholar
  53. Sadeghi SG, Chacron MJ, Taylor MC, Cullen KE (2007b) Neural variability, detection thresholds, and information transmission in the vestibular system. J Neurosci 27:771–781PubMedCrossRefGoogle Scholar
  54. Sadeghi SG, Goldberg JM, Minor LB, Cullen KE (2009) Efferent-mediated responses in vestibular nerve afferents of the alert macaque. J Neurophysiol 101:988–1001PubMedCrossRefGoogle Scholar
  55. 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 115:381–386PubMedCrossRefGoogle Scholar
  56. 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 27:1552–1565PubMedCrossRefGoogle Scholar
  57. Scudder CA, Fuchs AF (1992) Physiological and behavioral identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J Neurophysiol 68:244–264PubMedGoogle Scholar
  58. Shaikh AG, Meng H, Angelaki DE (2004) Multiple reference frames for motion in the primate cerebellum. J Neurosci 24:4491–4497PubMedCrossRefGoogle Scholar
  59. Thach WT, Goodkin HP, Keating JG (1992) The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci 15:403–442PubMedCrossRefGoogle Scholar
  60. Tomlinson RD, Robinson DA (1984) Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 51:1121–1136PubMedGoogle Scholar
  61. von Holst E, Mittelstaedt H (1950) Das reafferenzprinzip. Naturwissenschaften 37:464–476CrossRefGoogle Scholar
  62. Voogd J, Gerrits NM, Ruigrok TJ (1996) Organization of the vestibulocerebellum. Ann N Y Acad Sci 781:553–579PubMedCrossRefGoogle Scholar
  63. Wilson VJ (1991) Vestibulospinal and neck reflexes: interaction in the vestibular nuclei. Arch Ital Biol 129:43–52PubMedGoogle Scholar
  64. 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 64:1695–1703PubMedGoogle Scholar
  65. Yamada J, Noda H (1987) Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. J Comp Neurol 265:224–241PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Kathleen E. Cullen
    • 1
  • Jessica X. Brooks
    • 1
  • Mohsen Jamali
    • 1
  • Jerome Carriot
    • 1
  • Corentin Massot
    • 1
  1. 1.Aerospace Medical Research Unit, Department of PhysiologyMcGill UniversityMontrealCanada

Personalised recommendations