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Vestibular contributions to linear motion perception

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Abstract

Vestibular contributions to linear motion (i.e., translation) perception mediated by the otoliths have yet to be fully characterized. To quantify the maximal extent that non-vestibular cues can contribute to translation perception, we assessed vestibular perceptual thresholds in two patients with complete bilateral vestibular ablation to compare to our data in 12 young (< 40 years), healthy controls. Vestibular thresholds were assessed for naso-occipital (“x-translation”), inter-aural (“y-translation”), and superior-inferior (“z-translation”) translations in three body orientations (upright, supine, side-lying). Overall, in our patients with bilateral complete vestibular loss, thresholds were elevated ~ 2–45 times relative to healthy controls. No systematic differences in vestibular perceptual thresholds were noted between motions that differed only with respect to their orientation relative to the head (i.e., otoliths) in patients with bilateral vestibular loss. In addition, bilateral loss patients tended to show a larger impairment in the perception of earth-vertical translations (i.e., motion parallel to gravity) relative to earth-horizontal translations, which suggests increased contribution of the vestibular system for earth-vertical motions. However, differences were also noted between the two patients. Finally, with the exception of side-lying x-translations, no consistent effects of body orientation in our bilateral loss patients were seen independent from those resulting from changes in the plane of translation relative to gravity. Overall, our data confirm predominant vestibular contributions to whole-body direction-recognition translation tasks and provide fundamental insights into vestibular contributions to translation motion perception.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Agrawal Y, Bremova T, Kremmyda O, Strupp M, MacNeilage PR (2013) Clinical testing of otolith function: perceptual thresholds and myogenic potentials. JARO J Assoc Res Otolaryngol 14:905–915

    Article  PubMed  Google Scholar 

  • Angelaki DE, Hess BJ (1994) Inertial representation of angular motion in the vestibular system of rhesus monkeys. I. vestibuloocular reflex. J Neurophysiol 71:1222–1249

    Article  CAS  PubMed  Google Scholar 

  • Angelaki DE, McHenry MQ, Dickman JD, Newlands SD, Hess BJM (1999) Computation of Inertial Motion: Neural Strategies to Resolve Ambiguous Otolith Information. J Neurosci 19:316–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Angelaki DE, Shaikh AG, Green AM, Dickman JD (2004) Neurons compute internal models of the physical laws of motion. Nature 430:560–564

    Article  CAS  PubMed  Google Scholar 

  • Benson AJ, Spencer MB, Stott JRR (1986) Thresholds for the detection of the direction of whole-body, linear movement in the horizontal plane. Aviat Space Environ Med 57:1088–1096

    CAS  PubMed  Google Scholar 

  • Benson AJ, Hutt ECB, Brown SF, Hutt C, Brown SF, Hutt ECB, Brown SF (1989) Thresholds for the perception of whole body angular movement about a vertical axis. Aviat Space Environ Med 60:205–213

    CAS  PubMed  Google Scholar 

  • Bermúdez Rey MC, Clark TK, Wang W, Leeder T, Bian Y, Merfeld DM (2016) Vestibular perceptual thresholds increase above the age of 40. Front Neurol. https://doi.org/10.3389/fneur.2016.00162

    Article  PubMed  PubMed Central  Google Scholar 

  • Bremova T, Caushaj A, Ertl M, Strobl R, Böttcher N, Strupp M, MacNeilage PR (2016) Comparison of linear motion perception thresholds in vestibular migraine and Menière’s disease. Eur Arch Otorhinolaryngol 273:2931–2939

    Article  PubMed  PubMed Central  Google Scholar 

  • Catanzaro MF, Miller DJ, Cotter LA, McCall AA, Yates BJ (2014) Integration of vestibular and gastrointestinal inputs by cerebellar fastigial nucleus neurons: multisensory influences on motion sickness. Exp Brain Res 232:2581–2589

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaudhuri SE, Merfeld DM (2013) Signal detection theory and vestibular perception: III. Estimating unbiased fit parameters for psychometric functions. Exp Brain Res 225:133–146

    Article  PubMed  Google Scholar 

  • Chaudhuri SE, Karmali F, Merfeld DM (2013) Whole body motion-detection tasks can yield much lower thresholds than direction-recognition tasks: implications for the role of vibration. J Neurophysiol 110:2764–2772

    Article  PubMed  PubMed Central  Google Scholar 

  • Clark TK, Merfeld DM (2021) Statistical approaches to identifying lapses in psychometric response data. Psychon Bull Rev 28:1433–1457

    Article  PubMed  Google Scholar 

  • Crane BT (2012a) Fore-aft translation aftereffects. Exp Brain Res 219:477–487

    Article  PubMed  PubMed Central  Google Scholar 

  • Crane BT (2012b) Roll aftereffects: influence of tilt and inter-stimulus interval. Exp Brain Res 223:89–98

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandez C, Goldberg JM (1976) Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. II. Directional selectivity and force response relations. J Neurophysiol 39:985–995

    Article  CAS  PubMed  Google Scholar 

  • Goodman-Keiser MD, Qin C, Thompson AM, Foreman RD (2010) Upper thoracic postsynaptic dorsal column neurons conduct cardiac mechanoreceptive information, but not cardiac chemical nociception in rats. Brain Res 1366:71–84

    Article  CAS  PubMed  Google Scholar 

  • Grabherr L, Nicoucar K, Mast FW, Merfeld DM (2008) Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency. Exp Brain Res 186:677–681

    Article  PubMed  Google Scholar 

  • Graybiel A, Patterson JRJL (1955) Thresholds of stimulation of the otolith organs as indicated by the oculogravic illusion. J Appl Physiol 7:666–670

    Article  CAS  PubMed  Google Scholar 

  • Hummel N, Cuturi LF, MacNeilage PR, Flanagin VL (2016) The effect of supine body position on human heading perception. J vis 16:19–19

    Article  PubMed  Google Scholar 

  • Kaernbach C (2001) Slope bias of psychometric functions derived from adaptive data. Percept Psychophys 63:1389–1398

    Article  CAS  PubMed  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  PubMed Central  Google Scholar 

  • Karmali F, Chaudhuri SE, Yi Y, Merfeld DM (2016) Determining thresholds using adaptive procedures and psychometric fits: evaluating efficiency using theory, simulations, and human experiments. Exp Brain Res 234:773–789

    Article  PubMed  Google Scholar 

  • Karmali F, Rey MCB, Clark TK, Wang W, Merfeld DM (2017) Multivariate analyses of balance test performance, vestibular thresholds, and age. Front Neurol 8:1–16

    Article  Google Scholar 

  • Karmali F, Goodworth AD, Valko Y, Leeder T, Peterka RJ, Merfeld DM (2021) The role of vestibular cues in postural sway. J Neurophysiol 125:672–686

    Article  PubMed  PubMed Central  Google Scholar 

  • King S, Priesol AJ, Davidi SE, Merfeld DM, Ehtemam F, Lewis RF (2019) Self-motion perception is sensitized in vestibular migraine: pathophysiologic and clinical implications. Sci Rep 9:1–12

    Article  Google Scholar 

  • Kingma H (2005) Thresholds for perception of direction of linear acceleration as a possible evaluation of the otolith function. BMC Ear Nose Throat Disord 6:1–6

    Google Scholar 

  • Klein SA (2001) Measuring, estimating, and understanding the psychometric function: a commentary. Percept Psychophys 63:1421–1455

    Article  CAS  PubMed  Google Scholar 

  • Kobel MJ, Wagner AR, Merfeld DM (2021a) Impact of gravity on the perception of linear motion. J Neurophysiol 126:875–887

    Article  PubMed  PubMed Central  Google Scholar 

  • Kobel MJ, Wagner AR, Merfeld DM, Mattingly JK (2021b) Vestibular thresholds: a review of advances and challenges in clinical applications. Front Neurol 12:203

    Article  Google Scholar 

  • Kobel MJ, Wagner AR, Merfeld DM (2023) Evaluating vestibular contributions to rotation and tilt perception. Exp Brain Res 241:1873–1885

    Article  PubMed  Google Scholar 

  • Kostreva DR, Pontus SP (1993a) Hepatic vein, hepatic parenchymal, and inferior vena caval mechanoreceptors with phrenic afferents. Am J Physio Gastrointest Liver Physiol 265:G15–G20

    Article  CAS  Google Scholar 

  • Kostreva DR, Pontus SP (1993b) Pericardial mechanoreceptors with phrenic afferents. Am J Physiol Heart Circulatory Physiol 264:H1836–H1846

    Article  CAS  Google Scholar 

  • Laurens J, Meng H, Angelaki DE (2013a) Computation of linear acceleration through an internal model in the macaque cerebellum. Nat Neurosci 16:1701–1708

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laurens J, Meng H, Angelaki DE (2013b) Neural representation of orientation relative to gravity in the macaque cerebellum. Neuron 80:1508–1518

    Article  CAS  PubMed  Google Scholar 

  • Lewis RF, Priesol AJ, Nicoucar K, Lim K, Merfeld DM (2011a) Dynamic tilt thresholds are reduced in vestibular migraine. J Vestib Res Equilib Orient 21:323–330

    Article  Google Scholar 

  • Lewis RF, Priesol AJ, Nicoucar K, Lim K, Merfeld DM (2011b) Abnormal motion perception in vestibular migraine. Laryngoscope 121:1124–1125

    Article  PubMed  PubMed Central  Google Scholar 

  • Lim K, Merfeld DM (2012) Signal detection theory and vestibular perception: II. Fitting perceptual thresholds as a function of frequency. Exp Brain Res 222:303–320

    Article  PubMed  PubMed Central  Google Scholar 

  • MacNeilage PR, Banks MS, DeAngelis GC, Angelaki DE (2010) Vestibular heading discrimination and sensitivity to linear acceleration in head and world coordinates. J Neurosci 30:9084–9094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mallery RM, Olomu OU, Uchanski RM, Militchin VA, Hullar TE (2010) Human discrimination of rotational velocities. Exp Brain Res 204:11–20

    Article  PubMed  PubMed Central  Google Scholar 

  • Merchant SN, Tsuji K, Wall C, Velázquez-Villaseñor L, Glynn RJ, Rauch SD (2000) Temporal bone studies of the human peripheral vestibular system. Ann Otol Rhinol Laryngol 109:3–13

    Article  Google Scholar 

  • Merfeld DM, Young LR, Oman CM, Shelhamer MJ (1993) A multidimensional model of the effect of gravity on the spatial orientation of the monkey. J Vestib Res 3:141–161

    Article  CAS  PubMed  Google Scholar 

  • Merfeld DM, Zupan L, Peterka RJ (1999) Humans use internal models to estimate gravity and linear acceleration. Nat 398:615–618

    Article  CAS  Google Scholar 

  • Merfeld DM (2011) Signal detection theory and vestibular thresholds: I. Basic theory and practical considerations. Exp Brain Res 210:389–405

    Article  PubMed  PubMed Central  Google Scholar 

  • Mikellidou K, Cicchini GM, Thompson PG, Burr DC (2015) The oblique effect is both allocentric and egocentric. J vis 15:24–24

    Article  PubMed  Google Scholar 

  • Mittelstaedt H (1983) A new solution to the problem of the subjective vertical. Naturwissenschaften 70:272–281

    Article  CAS  PubMed  Google Scholar 

  • Mittelstaedt H (1995) Evidence of somatic graviception from new and classical investigations. Acta Otolaryngol 115:186–187

    Article  Google Scholar 

  • Mittelstaedt H (1996) Somatic graviception. Biol Psychol 42:53–74

    Article  CAS  PubMed  Google Scholar 

  • Mittelstaedt H, Fricke E (1988) The relative effect of saccular and somatosensory information on spatial perception and control. Clinical testing of the vestibular system. Karger Publishers, Basel, pp 24–30

    Google Scholar 

  • Mittelstaedt M-L, Mittelstaedt H (1996) The influence of otoliths and somatic graviceptors on angular velocity estimation. J Vestib Res 6:355–366

    Article  CAS  PubMed  Google Scholar 

  • Naganuma H, Tokumasu K, Hashimoto S, Okamoto M, Yamashina S (2001) Three-dimensional analysis of morphological aspects of the human saccular macula. Ann Otol Rhinol Laryngol 110:1017–1024

    Article  CAS  PubMed  Google Scholar 

  • Naganuma H, Tokumasu K, Hashimoto S, Okamoto M, Yamashina S (2003) Three-dimensional analysis of morphological aspects of the human utricular macula. Ann Otol Rhinol Laryngol 112:419–424

    Article  PubMed  Google Scholar 

  • Naseri AR, Grant PR (2012) Human discrimination of translational accelerations. Exp Brain Res 218:455–464

    Article  PubMed  Google Scholar 

  • Priesol AJ, Valko Y, Merfeld DM, Lewis RF (2014) Motion perception in patients with idiopathic bilateral vestibular hypofunction. Otolaryngol Head Neck Surg (united States) 150:1040–1042

    Article  Google Scholar 

  • Quenouille MH (1956) Notes on bias in estimation. Biometrika 43:353–360

    Article  Google Scholar 

  • Roditi RE, Crane BT (2012) Directional asymmetries and age effects in human self-motion perception. JARO J Assoc Res Otolaryngol 13:381–401

    Article  PubMed  Google Scholar 

  • Suri K, Clark TK (2020) Human vestibular perceptual thresholds for pitch tilt are slightly worse than for roll tilt across a range of frequencies. Exp Brain Res 238:1499–1509

    Article  PubMed  Google Scholar 

  • Suzuki T, Sugiyama Y, Yates BJ (2012) Integrative responses of neurons in parabrachial nuclei to a nauseogenic gastrointestinal stimulus and vestibular stimulation in vertical planes. Am J Physiol Regul Integr Comp Physiol 302:R965–R975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takagi A, Sando I, Takagi A, Sando I (1988) Computer-aided three-dimensional reconstruction and measurement of the vestibular end-organs. Otolaryngol Head Neck Surg 98:195–202

    Article  CAS  PubMed  Google Scholar 

  • Taylor M, Creelman CD (1967) PEST: Efficient estimates on probability functions. J Acoust Soc Am 41:782–787

    Article  Google Scholar 

  • Tukey J (1958) Bias and confidence in not quite large samples. Ann Math Stat 29:614

    Google Scholar 

  • Vaitl D, Mittelstaedt H, Baisch F (1997) Shifts in blood volume alter the perception of posture. Int J Psychophysiol 27:99–105

    Article  CAS  PubMed  Google Scholar 

  • Vaitl D, Mittelstaedt H, Saborowski R, Stark R, Baisch F (2002) Shifts in blood volume alter the perception of posture: further evidence for somatic graviception. Int J Psychophysiol 44:1–11

    Article  PubMed  Google Scholar 

  • Valko Y, Lewis RF, Priesol AJ, Merfeld DM (2012) Vestibular labyrinth contributions to human whole-body motion discrimination. J Neurosci 32:13537–13542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Stiphout L, Lucieer F, Pleshkov M, Van Rompaey V, Widdershoven J, Guinand N, Pérez Fornos A, Kingma H, van de Berg R (2021) Bilateral vestibulopathy decreases self-motion perception. J Neurol. https://doi.org/10.3389/fneur.2022.856472

    Article  PubMed  PubMed Central  Google Scholar 

  • Wichmann FA, Hill NJ (2001) The psychometric function: I. Fitting, sampling, and goodness of fit. Percept Psychophys 63:1293–1313

    Article  CAS  PubMed  Google Scholar 

  • Yu X, Dickman JD, Angelaki DE (2012) Detection thresholds of macaque otolith afferents. J Neurosci 32:8306–8316

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank our bilateral loss participants for their time, effort, and willingness to travel to participate in our research. We also thank Bob Grimes and Michael Hall for their technical assistance and Philippe deNeere for artistic assistance.

Funding

This research was supported by the National Institute on Deafness and Other Communication Disorders Grants (R01DC014924) and the National Institute on Aging (R01AG073113). Department of Defense Congressionally Directed Medical Research Programs (CDMRP) Award Number W81XWH192000. MK was supported in part by a The Ohio State University Graduate School’s Alumni Grants for Graduate Research and Scholarship (AGGRS) Program.

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All authors contributed to the study conception and design. Data collection was performed by MJK and ARW. Data analysis and the first draft of the manuscript was written by MJK. All authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Megan J. Kobel.

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The authors declare that they have no conflict of interest.

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Written informed consent was obtained from all participants included in the study.

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All study procedures were approved by the Ohio State University Institutional Review Board.

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Communicated by Bill J Yates.

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Kobel, M.J., Wagner, A.R. & Merfeld, D.M. Vestibular contributions to linear motion perception. Exp Brain Res 242, 385–402 (2024). https://doi.org/10.1007/s00221-023-06754-y

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