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Vestibular processing during natural self-motion: implications for perception and action

Nature Reviews Neuroscience volume 20, pages 346–363 (2019)Cite this article

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Abstract

How the brain computes accurate estimates of our self-motion relative to the world and our orientation relative to gravity in order to ensure accurate perception and motor control is a fundamental neuroscientific question. Recent experiments have revealed that the vestibular system encodes this information during everyday activities using pathway-specific neural representations. Furthermore, new findings have established that vestibular signals are selectively combined with extravestibular information at the earliest stages of central vestibular processing in a manner that depends on the current behavioural goal. These findings have important implications for our understanding of the brain mechanisms that ensure accurate perception and behaviour during everyday activities and for our understanding of disorders of vestibular processing.

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Fig. 1: Overview of the vestibular labyrinth and central pathways.
Fig. 2: Motor and multisensory integration in the vestibular nuclei.
Fig. 3: Internal models of self-motion in the vestibular cerebellum.
Fig. 4: Vestibular processing for self-motion perception.

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References

  1. Curthoys, I. S. & Halmagyi, G. M. Vestibular compensation: a review of the oculomotor, neural, and clinical consequences of unilateral vestibular loss. J. Vestib. Res. 5, 67–107 (1995).

    Article  CAS  PubMed  Google Scholar 

  2. Carriot, J., Jamali, M. & Cullen, K. E. Rapid adaptation of multisensory integration in vestibular pathways. Front. Syst. Neurosci. 9, 59 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  3. Peterka, R. J., Wall, C. & Kentala, E. Determining the effectiveness of a vibrotactile balance prosthesis. J. Vestib. Res. 16, 45–56 (2006).

    PubMed  Google Scholar 

  4. Cullen, K. E. The vestibular system: multimodal integration and encoding of self-motion for motor control. Trends Neurosci. 35, 185–196 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Massot, C., Chacron, M. J. & Cullen, K. E. Information transmission and detection thresholds in the vestibular nuclei: single neurons versus population encoding. J. Neurophysiol. 105, 1798–1814 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  6. Schneider, A. D., Jamali, M., Carriot, J., Chacron, M. J. & Cullen, K. E. The increased sensitivity of irregular peripheral canal and otolith vestibular afferents optimizes their encoding of natural stimuli. J. Neurosci. 35, 5522–5536 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Jamali, M., Chacron, M. J. & Cullen, K. E. Self-motion evokes precise spike timing in the primate vestibular system. Nat. Commun. 7, 13229 (2016). This paper demonstrates that two distinct sensory channels represent vestibular information from the semicircular canals: one using rate coding and the other using precise spike timing.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Jamali, M., Carriot, J., Chacron, M. J. & Cullen, K. E. Parallel channels with different timescales encode self-motion information in the vestibular system [235.08]. Presented at Neuroscience 2015 (Society for Neuroscience).

  9. Metzen, M. G. et al. Coding of envelopes by correlated but not single-neuron activity requires neural variability. Proc. Natl. Acad. Sci. USA 112, 4791–4796 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Roy, J. E. & Cullen, K. E. Selective processing of vestibular reafference during self-generated head motion. J. Neurosci. 21, 2131–2142 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Carriot, J., Brooks, J. X. & Cullen, K. E. Multimodal integration of self-motion cues in the vestibular system: active versus passive translations. J. Neurosci. 33, 19555–19566 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dale, A. & Cullen, K. E. The ventral posterior lateral thalamus preferentially encodes externally applied versus active movement: implications for self-motion perception. Cereb. Cortex 29, 305–318 (2019). This study demonstrates that the posterior thalamocortical vestibular pathway selectively encodes unexpected motion, thereby ensuring perceptual stability during active versus externally generated motion.

    Article  PubMed  Google Scholar 

  13. Cullen, K. E. & Roy, J. E. Signal processing in the vestibular system during active versus passive head movements. J. Neurophysiol. 91, 1919–1933 (2004).

    Article  PubMed  Google Scholar 

  14. Roy, J. E. & Cullen, K. E. A neural correlate for vestibulo-ocular reflex suppression during voluntary eye-head gaze shifts. Nat. Neurosci. 1, 404–410 (1998).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Brooks, J. X. & Cullen, K. E. Early vestibular processing does not discriminate active from passive self-motion if there is a discrepancy between predicted and actual proprioceptive feedback. J. Neurophysiol. 111, 2465–2478 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Brooks, J. X., Carriot, J. & Cullen, K. E. Learning to expect the unexpected: rapid updating in primate cerebellum during voluntary self-motion. Nat. Neurosci. 18, 1310–1317 (2015). This study demonstrates rapid updating in the primate cerebellum that is consistent with the dynamic comparison between expected and actual sensory feedback. Neuronal responses are consistent with the computation of sensory prediction, which enables the distinction between self-generated and externally applied vestibular sensory inputs.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cullen, K. E. The neural encoding of self-motion. Curr. Opin. Neurobiol. 21, 587–595 (2011).

    Article  CAS  PubMed  Google Scholar 

  19. Goldberg, J. M. Afferent diversity and the organization of central vestibular pathways. Exp. Brain Res. 130, 277–297 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Ramachandran, R. & Lisberger, S. G. Neural substrate of modified and unmodified pathways for learning in monkey vestibuloocular reflex. J. Neurophysiol. 100, 1868–1878 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Sadeghi, S. G., Minor, L. B. & Cullen, K. E. Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. J. Neurophysiol. 97, 1503–1514 (2007).

    Article  PubMed  Google Scholar 

  22. Jamali, M., Carriot, J., Chacron, M. J. & Cullen, K. E. Strong correlations between sensitivity and variability give rise to constant discrimination thresholds across the otolith afferent population. J. Neurosci. 33, 11302–11313 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Carriot, J., Jamali, M., Chacron, M. J. & Cullen, K. E. Statistics of the vestibular input experienced during natural self-motion: implications for neural processing. J. Neurosci. 34, 8347–8357 (2014). This study quantifies, for the first time, the statistics of natural vestibular inputs experienced by freely moving human subjects during typical everyday activities.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Carriot, J., Jamali, M., Chacron, M. J. & Cullen, K. E. The statistics of the vestibular input experienced during natural self-motion differ between rodents and primates. J. Physiol. 595, 2751–2766 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Dugué, G. P., Tihy, M., Gourévitch, B. & Léna, C. Cerebellar re-encoding of self-generated head movements. eLife 6, e26179 (2017). This study shows that a subpopulation of Purkinje cells in the caudal vermis of freely moving rats responds to head rotations about an axis that is defined relative to gravity.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Simoncelli, E. P. & Olshausen, B. A. Natural image statistics and neural representation. Annu. Rev. Neurosci. 24, 1193–1216 (2001).

    Article  CAS  PubMed  Google Scholar 

  27. Eatock, R. A. & Songer, J. E. Vestibular hair cells and afferents: two channels for head motion signals. Annu. Rev. Neurosci. 34, 501–534 (2011).

    Article  CAS  PubMed  Google Scholar 

  28. Goldberg, J. M. & Fernández, C. Conduction times and background discharge of vestibular afferents. Brain Res. 122, 545–550 (1977). This study shows that vestibular afferents can be grouped, on the basis of the regularity of their background firing rates and conduction rates, as regular versus irregular afferents.

    Article  CAS  PubMed  Google Scholar 

  29. Eatock, R. A. Specializations for fast signaling in the amniote vestibular inner ear. Integr. Comp. Biol. 58, 341–350 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  30. Songer, J. E. & Eatock, R. A. Tuning and timing in mammalian type I hair cells and calyceal synapses. J. Neurosci. 33, 3706–3724 (2013). This study investigates the tuning and fast dynamics of signalling by type I hair cells and concludes that transducer adaptation, membrane charging time and the dynamics of both quantal and nonquantal transmission make significant contributions.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Sadeghi, S. G., Chacron, M. J., Taylor, M. C. & Cullen, K. E. Neural variability, detection thresholds, and information transmission in the vestibular system. J. Neurosci. 27, 771–781 (2007). This study provides the first description of neuronal detection thresholds and information transmission during self-motion by single vestibular afferents.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lewis, E. R. & Parnas, B. R. Theoretical bases of short-latency spike volleys in the peripheral vestibular system. J. Vestib. Res. 4, 189–202 (1994).

    CAS  PubMed  Google Scholar 

  33. Jones, T. A. et al. The adequate stimulus for mammalian linear vestibular evoked potentials (VsEPs). Hear. Res 280, 133–140 (2011).

    Article  PubMed  Google Scholar 

  34. Brown, D. J., Pastras, C. J. & Curthoys, I. S. Electrophysiological measurements of peripheral vestibular function-a review of electrovestibulography. Front. Syst. Neurosci. 11, 34 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  36. Ramachandran, R. & Lisberger, S. G. Transformation of vestibular signals into motor commands in the vestibuloocular reflex pathways of monkeys. J. Neurophysiol. 96, 1061–1074 (2006).

    Article  PubMed  Google Scholar 

  37. Marlinski, V. & McCrea, R. A. Self-motion signals in vestibular nuclei neurons projecting to the thalamus in the alert squirrel monkey. J. Neurophysiol. 101, 1730–1741 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Meng, H., May, P. J., Dickman, J. D. & Angelaki, D. E. Vestibular signals in primate thalamus: properties and origins. J. Neurosci. 27, 13590–13602 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Abzug, C., Maeda, M., Peterson, B. W. & Wilson, V. J. Cervical branching of lumbar vestibulospinal axons. J. Physiol. 243, 499–522 (1974).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Gdowski, G. T. & McCrea, R. A. Integration of vestibular and head movement signals in the vestibular nuclei during whole-body rotation. J. Neurophysiol. 82, 436–449 (1999).

    Article  CAS  PubMed  Google Scholar 

  41. Shinoda, Y., Futami, T., Mitoma, H. & Yokota, J. Morphology of single neurones in the cerebello-rubrospinal system. Behav. Brain Res. 28, 59–64 (1988).

    Article  CAS  PubMed  Google Scholar 

  42. Massot, C., Schneider, A. D., Chacron, M. J. & Cullen, K. E. The vestibular system implements a linear-nonlinear transformation in order to encode self-motion. PLoS Biol. 10, e1001365 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Fechner, G.H. Elements of Psychophysics (eds Howes, D. H. & Boring, E. G.) Vol. 1 (Holt, Rinehart and Winston, 1966).

  44. Tolhurst, D. J., Tadmor, Y. & Chao, T. Amplitude spectra of natural images. Ophthalmic Physiol. Opt. 12, 229–232 (1992).

    Article  CAS  PubMed  Google Scholar 

  45. Ruderman, D. L. & Bialek, W. Statistics of natural images: scaling in the woods. Phys. Rev. Lett. 73, 814–817 (1994).

    Article  CAS  PubMed  Google Scholar 

  46. Mallery, R. M., Olomu, O. U., Uchanski, R. M., Militchin, V. A. & Hullar, T. E. Human discrimination of rotational velocities. Exp. Brain Res. 204, 11–20 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Naseri, A. R. & Grant, P. R. Human discrimination of translational accelerations. Exp. Brain Res. 218, 455–464 (2012).

    Article  PubMed  Google Scholar 

  48. Carriot, J., Jamali, M., Cullen, K. E. & Chacron, M. J. Envelope statistics of self-motion signals experienced by human subjects during everyday activities: implications for vestibular processing. PLoS ONE 12, e0178664 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lewis, R. F., Priesol, A. J., Nicoucar, K., Lim, K. & Merfeld, D. M. Dynamic tilt thresholds are reduced in vestibular migraine. J. Vestib. Res. 21, 323–330 (2011).

    PubMed  PubMed Central  Google Scholar 

  50. Kim, C. H., Shin, J. E., Song, C. I., Yoo, M. H. & Park, H. J. Vertical components of head-shaking nystagmus in vestibular neuritis, Meniere’s disease and migrainous vertigo. Clin. Otolaryngol. 39, 261–265 (2014).

    Article  CAS  PubMed  Google Scholar 

  51. US National Library of Medicine. ClinicalTrials.gov https://www.clinicaltrials.gov/ct2/show/NCT02725463 (2018).

  52. Lackner, J. R. & DiZio, P. Vestibular, proprioceptive, and haptic contributions to spatial orientation. Annu. Rev. Psychol. 56, 115–147 (2005).

    Article  PubMed  Google Scholar 

  53. Carriot, J., Cian, C., Paillard, A., Denise, P. & Lackner, J. R. Influence of multisensory graviceptive information on the apparent zenith. Exp. Brain Res. 208, 569–579 (2011).

    Article  CAS  PubMed  Google Scholar 

  54. Goldberg, J. M. et al. The Vestibular System: A Sixth Sense (Oxford Univ. Press, 2012).

  55. Boyle, R., Büttner, U. & Markert, G. Vestibular nuclei activity and eye movements in the alert monkey during sinusoidal optokinetic stimulation. Exp. Brain Res. 57, 362–369 (1985).

    Article  CAS  PubMed  Google Scholar 

  56. Buettner, U. W. & Büttner, U. Vestibular nuclei activity in the alert monkey during suppression of vestibular and optokinetic nystagmus. Exp. Brain Res. 37, 581–593 (1979).

    Article  CAS  PubMed  Google Scholar 

  57. Waespe, W. & Henn, V. Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp. Brain Res. 27, 523–538 (1977).

    Article  CAS  PubMed  Google Scholar 

  58. Waespe, W. & Henn, V. Vestibular nuclei activity during optokinetic after-nystagmus (OKAN) in the alert monkey. Exp. Brain Res. 30, 323–330 (1977).

    CAS  PubMed  Google Scholar 

  59. Reisine, H. & Raphan, T. Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation. Exp. Brain Res. 92, 209–226 (1992).

    Article  CAS  PubMed  Google Scholar 

  60. Beraneck, M. & Cullen, K. E. Activity of vestibular nuclei neurons during vestibular & optokinetic stimulation in the alert mouse. J. Neurophysiol. 98, 1549–1565 (2007).

    Article  CAS  PubMed  Google Scholar 

  61. Bryan, A. S. & Angelaki, D. E. Optokinetic and vestibular responsiveness in the macaque rostral vestibular and fastigial nuclei. J. Neurophysiol. 101, 714–720 (2009).

    Article  PubMed  Google Scholar 

  62. Tokita, T., Ito, Y. & Takagi, K. Modulation by head and trunk positions of the vestibulo-spinal reflexes evoked by galvanic stimulation of the labyrinth. Observations by labyrinthine evoked EMG. Acta Otolaryngol. 107, 327–332 (1989).

    Article  CAS  PubMed  Google Scholar 

  63. Kennedy, P. M. & Inglis, J. T. Interaction effects of galvanic vestibular stimulation and head position on the soleus H reflex in humans. Clin. Neurophysiol. 113, 1709–1714 (2002).

    Article  PubMed  Google Scholar 

  64. Medrea, I. & Cullen, K. E. Multisensory integration in early vestibular processing in mice: the encoding of passive versus active motion. J. Neurophysiol. 110, 2704–2717 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  65. McCall, A. A., Miller, D. M., DeMayo, W. M., Bourdages, G. H. & Yates, B. J. Vestibular nucleus neurons respond to hindlimb movement in the conscious cat. J. Neurophysiol. 116, 1785–1794 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Gdowski, G. T. & McCrea, R. A. Neck proprioceptive inputs to primate vestibular nucleus neurons. Exp. Brain Res. 135, 511–526 (2000).

    Article  CAS  PubMed  Google Scholar 

  67. Sadeghi, S. G., Mitchell, D. E. & Cullen, K. E. Different neural strategies for multimodal integration: comparison of two macaque monkey species. Exp. Brain Res. 195, 45–57 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  68. Carriot, J., Jamali, M., Brooks, J. X. & Cullen, K. E. Integration of canal and otolith inputs by central vestibular neurons is subadditive for both active and passive self-motion: implication for perception. J. Neurosci. 35, 3555–3565 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. MacNeilage, P. R., Turner, A. H. & Angelaki, D. E. Canal-otolith interactions and detection thresholds of linear and angular components during curved-path self-motion. J. Neurophysiol. 104, 765–773 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Krakauer, J. W. & Mazzoni, P. Human sensorimotor learning: adaptation, skill, and beyond. Curr. Opin. Neurobiol. 21, 636–644 (2011).

    Article  CAS  PubMed  Google Scholar 

  71. Oman, C. M. A heuristic mathematical model for the dynamics of sensory conflict and motion sickness. Acta Otolaryngol. Suppl. 392, 1–44 (1982).

    CAS  PubMed  Google Scholar 

  72. Borah, J., Young, L. R. & Curry, R. E. Optimal estimator model for human spatial orientation. Ann. NY Acad. Sci. 545, 51–73 (1987).

    Article  Google Scholar 

  73. Merfeld, D. M. Modeling human vestibular responses during eccentric rotation and off vertical axis rotation. Acta Otolaryngol. Suppl. 520 Pt 2, 354–359 (1994).

    Google Scholar 

  74. Zupan, L. H., Merfeld, D. M. & Darlot, C. Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements. Biol. Cybern. 86, 209–230 (2002).

    Article  CAS  PubMed  Google Scholar 

  75. Lim, K., Karmali, F., Nicoucar, K. & Merfeld, D. M. Perceptual precision of passive body tilt is consistent with statistically optimal cue integration. J. Neurophysiol. 117, 2037–2052 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  76. Laurens, J. & Angelaki, D. E. A unified internal model theory to resolve the paradox of active versus passive self-motion sensation. eLife 6, e28074 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  77. Karmali, F., Whitman, G. T. & Lewis, R. F. Bayesian optimal adaptation explains age-related human sensorimotor changes. J. Neurophysiol. 119, 509–520 (2018).

    Article  PubMed  Google Scholar 

  78. Porrill, J., Dean, P. & Anderson, S. R. Adaptive filters and internal models: multilevel description of cerebellar function. Neural Netw. 47, 134–149 (2013).

    Article  PubMed  Google Scholar 

  79. Dean, P. & Porrill, J. Decorrelation learning in the cerebellum: computational analysis and experimental questions. Prog. Brain Res. 210, 157–192 (2014).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  81. Cullen, K. E., Brooks, J. X., Jamali, M., Carriot, J. & Massot, C. Internal models of self-motion: computations that suppress vestibular reafference in early vestibular processing. Exp. Brain Res. 210, 377–388 (2011).

    Article  PubMed  Google Scholar 

  82. Kleine, J. F. et al. Trunk position influences vestibular responses of fastigial nucleus neurons in the alert monkey. J. Neurophysiol. 91, 2090–2100 (2004).

    Article  CAS  PubMed  Google Scholar 

  83. Shaikh, A. G., Meng, H. & Angelaki, D. E. Multiple reference frames for motion in the primate cerebellum. J. Neurosci. 24, 4491–4497 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Martin, C. Z., Brooks, J. X. & Green, A. M. Role of rostral fastigial neurons in encoding a body-centered representation of translation in three dimensions. J. Neurosci. 38, 3584–3602 (2018). This study describes recordings from deep cerebellar neurons in the rFN that provide evidence for the 3D transformation of vestibular signals from a head-centred to a body-centred reference frame.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Tokita, T., Miyata, H., Takagi, K. & Ito, Y. Studies on vestibulo-spinal reflexes by examination of labyrinthine-evoked EMGs of lower limbs. Acta Otolaryngol. Suppl. 481, 328–332 (1991).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  87. Brooks, J. X. & Cullen, K. E. Multimodal integration in rostral fastigial nucleus provides an estimate of body movement. J. Neurosci. 29, 10499–10511 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Cullen, K. E. Physiology of central pathways. Handb. Clin. Neurol. 137, 17–40 (2016).

    Article  CAS  PubMed  Google Scholar 

  89. McCall, A. A., Miller, D. M. & Yates, B. J. Descending influences on vestibulospinal and vestibulosympathetic reflexes. Front. Neurol. 8, 112 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Helmholtz, V. H. Handbuch der Physiologischen Optik [German] (Leopold Voss, 1867).

  91. Oman, C. & Cullen, K. Brainstem processing of vestibular sensory exafference: implications for motion sickness etiology. Exp. Brain Res. 232, 2483–2492 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  92. Bell, C. C., Han, V. & Sawtell, N. B. Cerebellum-like structures and their implications for cerebellar function. Annu. Rev. Neurosci. 31, 1–24 (2008).

    Article  CAS  PubMed  Google Scholar 

  93. Blakemore, S. J., Frith, C. D. & Wolpert, D. M. The cerebellum is involved in predicting the sensory consequences of action. Neuroreport 12, 1879–1884 (2001).

    Article  CAS  PubMed  Google Scholar 

  94. Einstein, A. The Meaning of Relativity (Routledge, 2003).

  95. Angelaki, D. E. & Cullen, K. E. Vestibular system: the many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125–150 (2008).

    Article  CAS  PubMed  Google Scholar 

  96. Merfeld, D. M., Park, S., Gianna-Poulin, C., Black, F. O. & Wood, S. Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt&Translation. J. Neurophysiol. 94, 199–205 (2005).

    Article  PubMed  Google Scholar 

  97. Green, A. M. & Angelaki, D. E. Coordinate transformations and sensory integration in the detection of spatial orientation and self-motion: from models to experiments. Prog. Brain Res. 165, 155–180 (2007).

    Article  PubMed  Google Scholar 

  98. Laurens, J. & Angelaki, D. E. The functional significance of velocity storage and its dependence on gravity. Exp. Brain Res. 210, 407–422 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  99. Laurens, J. et al. Transformation of spatiotemporal dynamics in the macaque vestibular system from otolith afferents to cortex. eLife 6, e20787 (2017). This study compares the dynamic and directional tuning of otolith afferents with that of neurons in the vestibular and cerebellar nuclei and five cortical areas.

    Article  PubMed  PubMed Central  Google Scholar 

  100. Yakusheva, T. A. et al. Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron 54, 973–985 (2007).

    Article  CAS  PubMed  Google Scholar 

  101. Yakusheva, T., Blazquez, P. M. & Angelaki, D. E. Frequency-selective coding of translation and tilt in macaque cerebellar nodulus and uvula. J. Neurosci. 28, 9997–10009 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Yakusheva, T., Blazquez, P. M. & Angelaki, D. E. Relationship between complex and simple spike activity in macaque caudal vermis during three-dimensional vestibular stimulation. J. Neurosci. 30, 8111–8126 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Laurens, J., Meng, H. & Angelaki, D. E. Neural representation of orientation relative to gravity in the macaque cerebellum. Neuron 80, 1508–1518 (2013).

    Article  CAS  PubMed  Google Scholar 

  104. Angelaki, D. E. & Hess, B. J. Lesion of the nodulus and ventral uvula abolish steady-state off-vertical axis otolith response. J. Neurophysiol. 73, 1716–1720 (1995).

    Article  CAS  PubMed  Google Scholar 

  105. Wearne, S., Raphan, T. & Cohen, B. Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J. Neurophysiol. 79, 2690–2715 (1998).

    Article  CAS  PubMed  Google Scholar 

  106. Mackrous, I., Carriot, J., Jamali, M., Brook, J. & Cullen, K. E. The neural encoding of active self-motion by the primate cerebellum: evidence for an internal model that accounts for gravity [404.19]. Presented at Neuroscience 2017 (Society for Neuroscience).

  107. Seemungal, B. M., Gunaratne, I. A., Fleming, I. O., Gresty, M. A. & Bronstein, A. M. Perceptual and nystagmic thresholds of vestibular function in yaw. J. Vestib Res. 14, 461–466 (2004).

    CAS  PubMed  Google Scholar 

  108. Grabherr, L., Nicoucar, K., Mast, F. W. & Merfeld, D. M. Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency. Exp. Brain Res. 186, 677–681 (2008).

    Article  PubMed  Google Scholar 

  109. Valko, Y., Lewis, R. F., Priesol, A. J. & Merfeld, D. M. Vestibular labyrinth contributions to human whole-body motion discrimination. J. Neurosci. 32, 13537–13542 (2012). This study provides the first description of the vestibular contributions to perceptual motion thresholds by testing patients with total bilateral vestibular loss.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Gu, Y., DeAngelis, G. C. & Angelaki, D. E. A functional link between area MSTd and heading perception based on vestibular signals. Nat. Neurosci. 10, 1038–1047 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Yu, X., Dickman, D. & Angelaki, D. Detection thresholds of macaque otolith afferents. J. Neurosci. 32, 8306–8316 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Yu, X. J., Dickman, J. D., DeAngelis, G. C. & Angelaki, D. E. Neuronal thresholds and choice-related activity of otolith afferent fibers during heading perception. Proc. Natl Acad. Sci. USA 112, 6467–6472 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Liu, S., Yakusheva, T., Deangelis, G. C. & Angelaki, D. E. Direction discrimination thresholds of vestibular and cerebellar nuclei neurons. J. Neurosci. 30, 439–448 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Liu, S., Dickman, D., Newlands, S., DeAngelis, G. & Angelaki, D. Reduced choice-related activity and correlated noise accompany perceptual deficits following unilateral vestibular lesion. Proc. Natl Acad. Sci. USA 110, 17999–18004 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  115. Yu, X.-J., Thomassen, J., Dickman, D., Newlands, S. & Angelaki, D. Long-term deficits in motion detection thresholds and spike count variability after unilateral vestibular lesion. J. Neurophysiol. 112, 870–889 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  116. Taube, J. S. The head direction signal: origins and sensory-motor integration. Annu. Rev. Neurosci. 30, 181–207 (2007).

    Article  CAS  PubMed  Google Scholar 

  117. Moser, E. I., Kropff, E. & Moser, M.-B. B. Place cells, grid cells, and the brain’s spatial representation system. Annu. Rev. Neurosci. 31, 69–89 (2008).

    Article  CAS  PubMed  Google Scholar 

  118. Dumont, J. R. & Taube, J. S. The neural correlates of navigation beyond the hippocampus. Prog. Brain Res. 219, 83–102 (2015).

    Article  PubMed  Google Scholar 

  119. Clark, B. J. & Harvey, R. E. Do the anterior and lateral thalamic nuclei make distinct contributions to spatial representation and memory? Neurobiol. Learn. Mem. 133, 69–78 (2016).

    Article  PubMed  Google Scholar 

  120. Lopez, C. & Blanke, O. The thalamocortical vestibular system in animals and humans. Brain Res. Rev. 67, 119–146 (2011).

    Article  PubMed  Google Scholar 

  121. Marlinski, V. & McCrea, R. A. Activity of ventroposterior thalamus neurons during rotation and translation in the horizontal plane in the alert squirrel monkey. J. Neurophysiol. 99, 2533–2545 (2008).

    Article  PubMed  Google Scholar 

  122. Marlinski, V. & McCrea, R. A. Coding of self-motion signals in ventro-posterior thalamus neurons in the alert squirrel monkey. Exp. Brain Res. 189, 463–472 (2008).

    Article  PubMed  Google Scholar 

  123. Meng, H. & Angelaki, D. E. Responses of ventral posterior thalamus neurons to three-dimensional vestibular and optic flow stimulation. J. Neurophysiol. 103, 817–826 (2010).

    Article  PubMed  Google Scholar 

  124. Guldin, W. O., Akbarian, S. & Grüsser, O. J. Cortico-cortical connections and cytoarchitectonics of the primate vestibular cortex: a study in squirrel monkeys (Saimiri sciureus). J. Comp. Neurol. 326, 375–401 (1992).

    Article  CAS  PubMed  Google Scholar 

  125. Penfield, W. Some observations on the functional organization of the human brain. Ideggyogy. Sz. 10, 138–141 (1957).

    CAS  PubMed  Google Scholar 

  126. Brandt, T., Dieterich, M. & Danek, A. Vestibular cortex lesions affect the perception of verticality. Ann. Neurol. 35, 403–412 (1994).

    Article  CAS  PubMed  Google Scholar 

  127. Grüsser, O. J., Pause, M. & Schreiter, U. Localization and responses of neurones in the parieto-insular vestibular cortex of awake monkeys (Macaca fascicularis). J. Physiol. 430, 537–557 (1990).

    Article  PubMed  PubMed Central  Google Scholar 

  128. Grüsser, O. J., Pause, M. & Schreiter, U. Vestibular neurones in the parieto-insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses. J. Physiol. 430, 559–583 (1990).

    Article  PubMed  PubMed Central  Google Scholar 

  129. Akbarian, S., Grüsser, O. J. & Guldin, W. O. Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey. J. Comp. Neurol. 339, 421–437 (1994).

    Article  CAS  PubMed  Google Scholar 

  130. Chen, A., Gu, Y., Liu, S., DeAngelis, G. C. & Angelaki, D. E. Evidence for a causal contribution of macaque vestibular, but not intraparietal, cortex to heading perception. J. Neurosci. 36, 3789–3798 (2016). This study reports the surprising result that, whereas inactivation of area PIVC yields deficits during heading discrimination for both visual and vestibular cues, inactivation of area VIP does not result in behavioural deficits.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Akbarian, S., Grüsser, O. J. & Guldin, W. O. Thalamic connections of the vestibular cortical fields in the squirrel monkey (Saimiri sciureus). J. Comp. Neurol. 326, 423–441 (1992).

    Article  CAS  PubMed  Google Scholar 

  132. Shinder, M. E. & Newlands, S. D. Sensory convergence in the parieto-insular vestibular cortex. J. Neurophysiol. 111, 2445–2464 (2014). This study describes the convergence of vestibular, visual and proprioceptive self-motion cues with external visual object motion information in area PIVC and concludes that neurons may encode the relative movement of head and body relative to external visual objects in space.

    Article  PubMed  PubMed Central  Google Scholar 

  133. Bremmer, F. Navigation in space — the role of the macaque ventral intraparietal area. J. Physiol. 566, 29–35 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Klam, F. & Graf, W. Vestibular response kinematics in posterior parietal cortex neurons of macaque monkeys. Eur. J. Neurosci. 18, 995–1010 (2003).

    Article  PubMed  Google Scholar 

  135. Schlack, A., Hoffmann, K. P. & Bremmer, F. Interaction of linear vestibular and visual stimulation in the macaque ventral intraparietal area (VIP). Eur. J. Neurosci. 16, 1877–1886 (2002).

    Article  PubMed  Google Scholar 

  136. Avillac, M., Denève, S., Olivier, E., Pouget, A. & Duhamel, J.-R. R. Reference frames for representing visual and tactile locations in parietal cortex. Nat. Neurosci. 8, 941–949 (2005).

    Article  CAS  PubMed  Google Scholar 

  137. Duhamel, J. R., Colby, C. L. & Goldberg, M. E. Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J. Neurophysiol. 79, 126–136 (1998).

    Article  CAS  PubMed  Google Scholar 

  138. Bremmer, F., Klam, F., Duhamel, J. R., Ben Hamed, S. & Graf, W. Visual-vestibular interactive responses in the macaque ventral intraparietal area (VIP). Eur. J. Neurosci. 16, 1569–1586 (2002).

    Article  PubMed  Google Scholar 

  139. Chen, A., DeAngelis, G. C. & Angelaki, D. E. Representation of vestibular and visual cues to self-motion in ventral intraparietal cortex. J. Neurosci. 31, 12036–12052 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Chen, A., DeAngelis, G. C. & Angelaki, D. E. Functional specializations of the ventral intraparietal area for multisensory heading discrimination. J. Neurosci. 33, 3567–3581 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Chen, X., DeAngelis, G. C. & Angelaki, D. E. Diverse spatial reference frames of vestibular signals in parietal cortex. Neuron 80, 1310–1321 (2013).

    Article  CAS  PubMed  Google Scholar 

  142. Bremmer, F., Kubischik, M., Pekel, M., Lappe, M. & Hoffmann, K. P. Linear vestibular self-motion signals in monkey medial superior temporal area. Ann. NY Acad. Sci. 871, 272–281 (1999).

    Article  CAS  PubMed  Google Scholar 

  143. Duffy, C. J. MST neurons respond to optic flow and translational movement. J. Neurophysiol. 80, 1816–1827 (1998).

    Article  CAS  PubMed  Google Scholar 

  144. Page, W. K. & Duffy, C. J. Heading representation in MST: sensory interactions and population encoding. J. Neurophysiol. 89, 1994–2013 (2003).

    Article  PubMed  Google Scholar 

  145. Thier, P. & Erickson, R. G. Responses of visual-tracking neurons from cortical area MST-I to visual, eye and head motion. Eur. J. Neurosci. 4, 539–553 (1992).

    Article  PubMed  Google Scholar 

  146. Takahashi, K. et al. Multimodal coding of three-dimensional rotation and translation in area MSTd: comparison of visual and vestibular selectivity. J. Neurosci. 27, 9742–9756 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Angelaki, D. E., Gu, Y. & Deangelis, G. C. Visual and vestibular cue integration for heading perception in extrastriate visual cortex. J. Physiol. 589, 825–833 (2011).

    Article  CAS  PubMed  Google Scholar 

  148. Fetsch, C. R., DeAngelis, G. C. & Angelaki, D. E. Bridging the gap between theories of sensory cue integration and the physiology of multisensory neurons. Nat. Rev. Neurosci. 14, 429–442 (2013).

    Article  CAS  PubMed  Google Scholar 

  149. Gu, Y., Deangelis, G. C. & Angelaki, D. E. Causal links between dorsal medial superior temporal area neurons and multisensory heading perception. J. Neurosci. 32, 2299–2313 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Gu, Y. Vestibular signals in primate cortex for self-motion perception. Curr. Opin. Neurobiol. 52, 10–17 (2018).

    Article  CAS  PubMed  Google Scholar 

  151. Jamali, M., Sadeghi, S. G. & Cullen, K. E. Response of vestibular nerve afferents innervating utricle and saccule during passive and active translations. J. Neurophysiol. 101, 141–149 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  152. Klam, F. & Graf, W. Discrimination between active and passive head movements by macaque ventral and medial intraparietal cortex neurons. J. Physiol. 574, 367–386 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Hitier, M., Besnard, S. & Smith, P. F. Vestibular pathways involved in cognition. Front. Integr. Neurosci. 8, 59 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  154. Taube, J. S., Muller, R. U. & Ranck, J. B. Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. I. Description and quantitative analysis. J. Neurosci. 10, 420–435 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Taube, J. S., Muller, R. U. & Ranck, J. B. Jr. Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J. Neurosci. 10, 436–447 (1990).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Shine, J. P., Valdés-Herrera, J. P., Hegarty, M. & Wolbers, T. The human retrosplenial cortex and thalamus code head direction in a global reference frame. J. Neurosci. 36, 6371–6381 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Knierim, J. J. & Zhang, K. Attractor dynamics of spatially correlated neural activity in the limbic system. Annu. Rev. Neurosci. 35, 267–285 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Yoder, R. M. & Taube, J. S. The vestibular contribution to the head direction signal and navigation. Front. Integr. Neurosci. 8, 32 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  159. Butler, W. N., Smith, K. S., Meer, M. A. & Taube, J. S. The head-direction signal plays a functional role as a neural compass during navigation. Curr. Biol. 27, 1259–1267 (2017). This study provides evidence that the HD network plays a causal role as a neural compass in navigation by establishing a link between the disruption of the HD signal and errors in directional homing behaviour in rats.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Taube, J. S. & Bassett, J. P. Persistent neural activity in head direction cells. Cereb. Cortex 13, 1162–1172 (2003).

    Article  PubMed  Google Scholar 

  161. Wiener, S. I., Berthoz, A. & Zugaro, M. B. B. Multisensory processing in the elaboration of place and head direction responses by limbic system neurons. Brain Res. Cogn. Brain Res. 14, 75–90 (2002).

    Article  PubMed  Google Scholar 

  162. Cullen, K. E. The neural encoding of self-generated and externally applied movement: implications for the perception of self-motion and spatial memory. Front. Integr. Neurosci. 7, 108 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  163. Cullen, K. E., Brooks, J. X. & Sadeghi, S. G. How actions alter sensory processing. Ann. NY Acad. Sci. 1164, 29–36 (2009).

    Article  PubMed  Google Scholar 

  164. Cullen, K. E. & Taube, J. S. Our sense of direction: progress, controversies and challenges. Nat. Neurosci. 20, 1465–1473 (2017).

    Article  CAS  PubMed  Google Scholar 

  165. Laurens, J. & Angelaki, D. E. The brain compass: a perspective on how self-motion updates the head direction cell attractor. Neuron 97, 275–289 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Babayan, B. M. et al. A hippocampo-cerebellar centred network for the learning and execution of sequence-based navigation. Sci. Rep. 7, 17812 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Page, W. K. & Duffy, C. J. Cortical neuronal responses to optic flow are shaped by visual strategies for steering. Cereb. Cortex 18, 727–739 (2008).

    Article  PubMed  Google Scholar 

  168. Jacob, M. S. & Duffy, C. J. Steering transforms the cortical representation of self-movement from direction to destination. J. Neurosci. 35, 16055–16063 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Roy, J. E. & Cullen, K. E. Vestibuloocular reflex signal modulation during voluntary and passive head movements. J. Neurophysiol. 87, 2337–2357 (2002).

    Article  PubMed  Google Scholar 

  170. McCollum, G. Sensory and motor interdependence in postural adjustments. J. Vestib Res. 9, 303–325 (1999).

    CAS  PubMed  Google Scholar 

  171. Mergner, T. & Rosemeier, T. Interaction of vestibular, somatosensory and visual signals for postural control and motion perception under terrestrial and microgravity conditions — a conceptual model. Brain Res. Brain Res. Rev. 28, 118–135 (1998).

    Article  CAS  PubMed  Google Scholar 

  172. Sadeghi, S. G., Minor, L. B. & Cullen, K. E. Dynamics of the horizontal vestibuloocular reflex after unilateral labyrinthectomy: response to high frequency, high acceleration, and high velocity rotations. Exp. Brain Res. 175, 471–484 (2006).

    Article  PubMed  Google Scholar 

  173. Beraneck, M. & Idoux, E. Reconsidering the role of neuronal intrinsic properties and neuromodulation in vestibular homeostasis. Front. Neurol. 3, 25 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  174. Dieringer, N. & Precht, W. Mechanisms of compensation for vestibular deficits in the frog. I. Modification of the excitatory commissural system. Exp. Brain Res. 36, 311–328 (1979).

    Article  CAS  PubMed  Google Scholar 

  175. Dieringer, N. & Precht, W. Mechanisms of compensation for vestibular deficits in the frog. II. Modification of the inhibitory pathways. Exp. Brain Res. 36, 329–357 (1979).

    Article  CAS  PubMed  Google Scholar 

  176. Mitchell, D. E., Della Santina, C. C. & Cullen, K. E. Plasticity within non-cerebellar pathways rapidly shapes motor performance in vivo. Nat. Commun. 7, 11238 (2016). This study investigates the VOR circuitry by applying temporally precise activation of vestibular afferents in awake-behaving monkeys using a neural prosthetic and then linking plasticity at different neural sites with changes in motor performance.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Mitchell, D. E., Della Santina, C. C. & Cullen, K. E. Plasticity within excitatory and inhibitory pathways of the vestibulo-spinal circuitry guides changes in motor performance. Sci. Rep. 7, 853 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Sadeghi, S. G., Minor, L. B. & Cullen, K. E. Neural correlates of motor learning in the vestibulo-ocular reflex: dynamic regulation of multimodal integration in the macaque vestibular system. J. Neurosci. 30, 10158–10168 (2010). This paper shows that following peripheral vestibular loss, compensation is mediated by the rapid and dynamic reweighting of extravestibular inputs (that is, proprioceptive inputs and motor signals) at the level of the vestibular nuclei.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Sadeghi, S. G., Minor, L. B. & Cullen, K. E. Multimodal integration after unilateral labyrinthine lesion: single vestibular nuclei neuron responses and implications for postural compensation. J. Neurophysiol. 105, 661–673 (2011).

    Article  PubMed  Google Scholar 

  180. Sadeghi, S. G., Minor, L. B. & Cullen, K. E. Neural correlates of sensory substitution in vestibular pathways following complete vestibular loss. J. Neurosci. 32, 14685–14695 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  181. Jamali, M. et al. Neuronal detection thresholds during vestibular compensation: contributions of response variability and sensory substitution. 592, 1565–1580 (2014).

  182. Lacour, M. Restoration of vestibular function: basic aspects and practical advances for rehabilitation. Curr. Med. Res. Opin. 22, 1651–1659 (2006).

    Article  PubMed  Google Scholar 

  183. Horak, F. B. Postural compensation for vestibular loss and implications for rehabilitation. Restor. Neurol. Neurosci. 28, 57–68 (2010).

    PubMed  PubMed Central  Google Scholar 

  184. Iaria, G., Petrides, M., Dagher, A., Pike, B. & Bohbot, V. D. D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. J. Neurosci. 23, 5945–5952 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Wolbers, T. & Büchel, C. Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. J. Neurosci. 25, 3333–3340 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Vitte, E. et al. Activation of the hippocampal formation by vestibular stimulation: a functional magnetic resonance imaging study. Exp. Brain Res. 112, 523–526 (1996).

    Article  CAS  PubMed  Google Scholar 

  187. Brandt, T. et al. Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128, 2732–2741 (2005). This article presents the first demonstration that human spatial navigation depends on the vestibular system, even when the subjects are stationary.

    Article  PubMed  Google Scholar 

  188. Maguire, E. A. et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc. Natl Acad. Sci. USA 97, 4398–4403 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  189. Biegler, R., McGregor, A., Krebs, J. R. & Healy, S. D. A larger hippocampus is associated with longer-lasting spatial memory. Proc. Natl Acad. Sci. USA 98, 6941–6944 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Cronin, T., Arshad, Q. & Seemungal, B. M. Vestibular deficits in neurodegenerative disorders: balance, dizziness, and spatial disorientation. Front. Neurol. 8, 538 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  191. Leandri, M. et al. Balance features in Alzheimer’s disease and amnestic mild cognitive impairment. J. Alzheimers Dis. 16, 113–120 (2009).

    Article  PubMed  Google Scholar 

  192. Nakamagoe, K. et al. Vestibular function impairment in Alzheimer’s disease. J. Alzheimers Dis. 47, 185–196 (2015).

    Article  PubMed  Google Scholar 

  193. Previc, F. H. Vestibular loss as a contributor to Alzheimer’s disease. Med. Hypotheses 80, 360–367 (2013).

    Article  PubMed  Google Scholar 

  194. Harun, A., Oh, E. S., Bigelow, R. T., Studenski, S. & Agrawal, Y. Vestibular impairment in dementia. Otol. Neurotol. 37, 1137–1142 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  195. Zhao, X. et al. Disrupted small-world brain networks in moderate Alzheimer’s disease: a resting-state FMRI study. PLoS ONE 7, e33540 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. Bigelow, R. T. & Agrawal, Y. Vestibular involvement in cognition: visuospatial ability, attention, executive function, and memory. J. Vestib Res. 25, 73–89 (2015).

    PubMed  Google Scholar 

  197. Bigelow, R. T. et al. Association between visuospatial ability and vestibular function in the baltimore longitudinal study of aging. J. Am. Geriatr. Soc. 63, 1837–1844 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  198. Yoshida, K., Berthoz, A., Vidal, P. P. & McCrea, R. A. Morphological and physiological characteristics of inhibitory burst neurons controlling rapid eye movements on the alert cat. J. Neurophysiol. 48, 761–784 (1982).

    Article  CAS  PubMed  Google Scholar 

  199. Strassman, A., Highstein, S. M. & McCrea, R. A. Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. J. Comp. Neurol. 249, 358–380 (1986).

    Article  CAS  PubMed  Google Scholar 

  200. Brooks, J. X. & Cullen, K. E. The primate cerebellum selectively encodes unexpected self-motion. Curr. Biol. 23, 947–955 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The author thanks V. Chang and O. Zobeiri for their helpful advice and contributions to figures in this paper and O. Stanley, K. P. Wiboonsaksakul, E. Gugig and L. Wang for their advice and comments. The author is funded by the Canadian Institutes of Health Research (CIHR) and the National Institutes of Health (NIH) DC2390.

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    Kathleen E. Cullen

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Glossary

Linear rate code

A neural code in which the frequency of action potentials fired by a neuron (that is, the firing rate) is linearly related to the intensity of the stimulus.

Vestibulo-ocular reflex

(VOR). A reflex that moves the eye in the opposite direction of the ongoing head motion to stabilize the visual axis of gaze relative to the environment.

Vestibulo-spinal reflex

A reflex that activates the neck and/or skeletal muscles to stabilize the body in order to maintain posture and balance.

Superposition principle

The principle that, for all linear systems, the net response to two or more stimuli is the sum of the responses to each stimulus individually (also known as the superposition property).

High-pass tuning

A neuronal property in which the neuronal response becomes increasingly more sensitive as the frequency of stimulation becomes higher.

Phase leads

Advances in the phase (position within a cycle) of responses relative to an input sinusoidal waveform.

Precise spike timing

A situation in which information is encoded by the precise timing of the action potential sequence generated by a neuron.

Jerk

The rate of change in acceleration, which mathematically is the first derivative of acceleration.

Saccades

Rapid movements of the eyes made to voluntarily shift the axis of gaze between fixation points.

Boosting nonlinearity

A nonlinearity characterized by lower sensitivities to lower-amplitude than to higher-amplitude head motion, which is observed when high-frequency and low-frequency head motion stimuli are simultaneously applied.

Reafferent cancellation signal

A signal computed by the brain to cancel the sensory consequences of actively generated vestibular stimulation produced during voluntary movements.

Adaptive filters

Filters with parameters that can be adjusted to learn, and in turn attenuate, the transmission of predictable features of the input.

Continuous ring attractor network

A recurrent network schematized as a ring of neurons around which moves a ‘bump’ of activity that indicates the current estimate of head direction.

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Cullen, K.E. Vestibular processing during natural self-motion: implications for perception and action. Nat Rev Neurosci 20, 346–363 (2019). https://doi.org/10.1038/s41583-019-0153-1

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