Abstract
Angular and linear accelerations of the head occur throughout everyday life, whether from external forces such as in a vehicle or from volitional head movements. The relative timing of the angular and linear components of motion differs depending on the movement. The inner ear detects the angular and linear components with its semicircular canals and otolith organs, respectively, and secondary neurons in the vestibular nuclei receive input from these vestibular organs. Many secondary neurons receive both angular and linear input. Linear information alone does not distinguish between translational linear acceleration and angular tilt, with its gravity-induced change in the linear acceleration vector. Instead, motions are thought to be distinguished by use of both angular and linear information. However, for combined motions, composed of angular tilt and linear translation, the infinite range of possible relative timing of the angular and linear components gives an infinite set of motions among which to distinguish the various types of movement. The present research focuses on motions consisting of angular tilt and horizontal translation, both sinusoidal, where the relative timing, i.e. phase, of the tilt and translation can take any value in the range −180° to 180°. The results show how hypothetical neurons receiving convergent input can distinguish tilt from translation, and that each of these neurons has a preferred combined motion, to which the neuron responds maximally. Also shown are the values of angular and linear response amplitudes and phases that can cause a neuron to be tilt-only or translation-only. Such neurons turn out to be sufficient for distinguishing between combined motions, with all of the possible relative angular–linear phases. Combinations of other neurons, as well, are shown to distinguish motions. Relative response phases and in-phase firing-rate modulation are the key to identifying specific motions from within this infinite set of combined motions.
Similar content being viewed by others
References
Angelaki DE (1991) Dynamic polarization vector of spatially tuned neurons. IEEE Trans Biomed Eng 38:1053–1060
Angelaki DE (1992) Spatio-temporal convergence (STC) in otolith neurons. Biol Cybern 67:83–96
Angelaki DE, Dickman JD (2000) Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J Neurophysiol 84:2113–2132
Angelaki DE, Dickman JD (2003) Gravity or translation: central processing of vestibular signals to detect motion or tilt. J Vestib Res 13:245–253
Angelaki DE, Bush GA, Perachio AA (1993) Two-dimensional spatiotemporal coding of linear acceleration in vestibular nuclei neurons. J Neurosci 13:1403–1417
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
Angelaki DE, Green AM, Dickman JD (2001a) Differential sensorimotor processing of vestibulo-ocular signals during rotation and translation. J Neurosci 21:3968–3985
Angelaki DE, Wei M, Merfeld DM (2001b) Vestibular discrimination of gravity and translational acceleration. Ann NY Acad Sci 942:114–127
Angelaki DE, Shaikh AG, Green AM, Dickman JD (2004) Neurons compute internal models of the physical laws of motion. Nature 430:560–564
Averbeck BB, Latham PE, Pouget A (2006) Neural correlations, population coding and computation. Nat Re Neurosci 7:358–366
Baker J, Goldberg J, Hermann G, Peterson B (1984) Spatial and temporal response properties of secondary neurons that receive convergent input in vestibular nuclei of alert cats. Brain Res 294:138–143
Boyle R (2001) Vestibulospinal control of reflex and voluntary head movement. Ann NY Acad Sci 942:364–380
Boyle R, Pompeiano O (1981) Convergence and interaction of neck and macular vestibular inputs on vestibulospinal neurons. J Neurophysiol 45:852–868
Boyle R, Belton T, McCrea RA (1996) Responses of identified vestibulospinal neurons to voluntary eye and head movements in the squirrel monkey. Ann NY Acad Sci 781:244–263
Boyle R, Bush G, Ehsanian R (2004) Input/output properties of the lateral vestibular nucleus. Archives Italiennes de Biologie 142:133–153
Curthoys IS, Markham CH (1971) Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. I. Natural stimulation. Brain Res 35:469–490
Daunton N, Melvill Jones G (1982) Distribution of sensitivity vectors in central vestibular units responding to linear acceleration. Soc Neurosci Abstr 8:42
Dickman JD, Angelaki DE (2002) Vestibular convergence patterns in vestibular nuclei neurons of alert primates. J Neurophysiol 88:3518–3533
Dickman JD, Angelaki DE (2004) Dynamics of vestibular neurons during rotational motion in alert rhesus monkeys. Exp Brain Res 155:91–101
Droulez J, Darlot C (1989) The geometric and dynamic implications of the coherence constraints in three-dimensional sensorimotor interactions. In: Jeannerod M (ed) Attention and Performance. Lawrence Erlbaum, Hillsdale, pp 495–526
Duensing F, Schaefer KP (1959) Über die Konvergenz verschiedener labyrinthärer Afferenzen auf einzelne Neurone des Vestibulariskerngebietes. Arch Psychiatr Z Gesamte Neurol 199:345–371
Fernandez C, Goldberg JM (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 34:661–675
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
Gdowski GT, McCrea RA (1999) Integration of vestibular and head movement signals in the vestibular nuclei during whole-body rotation. J Neurophysiol 81:436–449
Gdowski GT, Boyle R, McCrea RA (2000) Sensory processing in the vestibular nuclei during active head movements. Archives Italiennes de Biologie 138:15–28
Glasauer S (1993) Human spatial orientation during centrifuge experiments: non-linear interaction of semicircular canals and otoliths. In: Krejcova H, Jerabek J (eds) Proceeding of XVIIth Barany Society Meeting, Prague, pp 48–52
Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34:635–660
Green AM, Angelaki DE (2003) Resolution of sensory ambiguities for gaze stabilization requires a second neural integrator. J Neurosci 23:9265–9275
Green AM, Angelaki DE (2004) An integrative neural network for detecting inertial motion and head orientation. J Neurophysiol 92:905–925
Green AM, Galiana HL (1998) Hypothesis for shared central processing of canal and otolith signals. J Neurophysiol 80:2222–2228
Hess BJM, Angelaki DE (1999a) Inertial processing of vestibulo-ocular signals. Ann NY Acad Sci 871:148–161
Hess BJM, Angelaki DE (1999b) Oculomotor control of primary eye position discriminates between translation and tilt. J Neurophysiol 81:394–398
Holly JE (2000) Baselines for three-dimensional perception of combined linear and angular self-motion with changing rotational axis. J Vestib Res 10:163–178
Holly JE, McCollum G (1998) Timing of secondary vestibular neuron responses to a range of rotational head movements. Biol Cybern 79:39–48
Holly JE, McCollum G, Boyle R (1999) Identification of head motions by central vestibular neurons receiving linear and angular input. Biol Cybern 81:177–188
Keller EL (1976) Behavior of horizontal semicircular canal afferents in alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 24:459–471
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
Keller EL, Kamath BY (1975) Characteristics of head rotation and eye movement-related neurons in alert monkey vestibular nucleus. Brain Res 100:182–187
Keshner EA, Kenyon R, Langston J (2004) Postural responses exhibit multisensory dependencies with discordant visual and support surface motion. J Vestib Res 14:307–319
Kushiro K, Dai M, Kunin M, Yakushin SB, Cohen B, Raphan T (2002) Compensatory and orienting eye movements induced by off-vertical axis rotation (OVAR) in monkeys. J Neurophysiol 88:2445–2462
Louie AW, Kimm J (1976) The response of 8th nerve fibers to horizontal sinusoidal oscillation in the alert monkey. Exp Brain Res 24:447–457
McConville KMV, Tomlinson RD, Na E-Q (1996) Behavior of eye-movement-related cells in the vestibular nuclei during combined rotational and translational stimuli. J Neurophysiol 76:3136–3148
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
Melvill Jones G, Milsum JH (1969) Neural response of the vestibular system to translational acceleration. In: Conference on systems analysis approach to neurophysiological problems, Brainerd, Suppl pp 8–20
Merfeld DM, Zupan LH (2002) Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. J Neurophysiol 87:819–833
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
Mergner T, Glasauer S (1999) A simple model of vestibular canal-otolith signal fusion. Ann NY Acad Sci 871:430–434
Miles FA (1974) Single unit firing patterns in the vestibular nuclei related to voluntary eye movements and passive body rotation in conscious monkeys. Brain Res 71:215–224
Ormsby CC, Young LR (1977) Integration of semicircular canal and otolith information for multisensory orientation stimuli. Math Biosci 34:1–21
Perachio AA, Bush GA, Angelaki DE (1992) A model of responses of horizontal-canal-related vestibular nuclei neurons that respond to linear head acceleration. Ann NY Acad Sci 656:795–801
Perlmutter SI, Iwamoto Y, Baker JF, Peterson BW (1999) Spatial alignment of rotational and static tilt responses of vestibulospinal neurons in the cat. J Neurophysiol 82:855–862
Pouget A, Dayan P, Zemel RS (2003) Inference and computation with population codes. Annu Rev Neurosci 26:381–410
Raphan T, Cohen B (2002) The vestibulo-ocular reflex in three dimensions. Exp Brain Res 145:1–27
Roy JE, Cullen KE (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21:2131–2142
Roy JE, Cullen KE (2004) Dissociating self-generated from passively applied head motion: neural mechanisms in the vestibular nuclei. J Neurosci 24:2102–2111
Schor RH, Steinbacher BC Jr, Yates BJ (1998) Horizontal linear and angular responses of neurons in the medial vestibular nucleus of the decerebrate cat. J Vestib Res 8:107–116
Searles EJ, Barnes CD (1977) Ipsilateral utricular and semicircular canal interactions from electrical stimulation of individual vestibular nerve branches recorded in the descending medial longitudinal fasciculus. Brain Res 125:23–36
Tomlinson RD, Robinson DA (1984) Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 51:1121–1136
Tomlinson RD, McConville KMV, Na EQ (1996) Behavior of cells without eye movement sensitivity in the vestibular nuclei during combined rotational and translational stimuli. J Vestib Res 6:145–158
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Holly, J.E., Pierce, S.E. & McCollum, G. Head tilt–translation combinations distinguished at the level of neurons. Biol Cybern 95, 311–326 (2006). https://doi.org/10.1007/s00422-006-0099-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00422-006-0099-z