Key Points
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Short-latency eye movements, triggered by visual (ocular following reflex; OFR) and vestibular (translational vestibulo-ocular reflex; TVOR) mechanisms, compensate for the retinal image slip that is experienced during translational self-motion. These eye movements are predominantly conjugate during lateral motion when gaze and travel directions are approximately orthogonal to each other. Motion in a forward direction generates combinations of conjugate and vergence eye movements.
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Owing to the geometry of the translation-induced flow patterns, the OFR and the TVOR can reduce retinal image slip only locally to maintain foveal visual acuity. Foveal image stabilization is preferred at the cost of peripheral vision even when spatial attention is allocated to a peripheral target.
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A major challenge for the brain is estimation of target distance, which is necessary to adjust the amplitude of compensatory eye movements. For the OFR, this selection is driven by disparity- and motion parallax-sensitive mechanisms, whereas for the TVOR, target distance is solely computed on the basis of motor cues, primarily vergence angle and accommodation.
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The OFR is generated using visual motion signals in the medial superior temporal cortex, which projects to the paraflocculus of the cerebellum via the pontine nuclei. Purkinje cells in the ventral paraflocculus are thought to encode a motor command for the OFR. Neural processing underlying the generation of TVOR involves the vestibulo-cerebellum and the vestibular nuclei.
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Compensation of retinal image slip during translation involves eye movements that, in turn, modify the pattern of optic flow experienced by the moving observer. The mathematical analysis suggests that this interaction does not interfere with the use of optic flow information for visual navigation.
Abstract
Self-motion disturbs the stability of retinal images by inducing optic flow. Objects of interest need to be fixated or tracked, yet these eye movements can infringe on the experienced retinal flow that is important for visual navigation. Separating the components of optic flow caused by an eye movement from those due to self-motion, as well as using optic flow for visual navigation while simultaneously maintaining visual acuity on near targets, represent key challenges for the visual system. Here we summarize recent advances in our understanding of how the visuomotor and vestibulomotor systems function and interact, given the complex task of compensating for instabilities of retinal images, which typically vary as a function of retinal location and differ for each eye.
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References
Gibson, J. J. The visual perception of objective motion and subjective movement. Psychol. Rev. 61, 304–314 (1954).
Royden, C. S., Crowell, J. A. & Banks, M. S. Estimating heading during eye movements. Vision Res. 34, 3197–3214 (1994). One of the most comprehensive studies characterizing the role of retinal and extraretinal signals in perception of self-motion direction during pursuit eye movements.
Warren, W. H. Jr & Hannon, D. J. Direction of self-motion is perceived from optical flow. Nature 336, 162–163 (1988).
Warren, W. H. Jr, Morris, M. W. & Kalish, M. Perception of translational heading from optical flow. J. Exp. Psychol. Hum. Percept. Perform. 14, 646–660 (1988).
Warren, W. H. Jr & Hannon, D. J. Eye movements and optical flow. J. Opt. Soc. Am. A 7, 160–169 (1990).
Warren, W. H. Jr, Kay, B. A., Zosh, W. D., Duchon, A. P. & Sahuc, S. Optic flow is used to control human walking. Nature Neurosci. 4, 213–216 (2001).
Busettini, C., Masson, G. S. & Miles, F. A. Radial optic flow induces vergence eye movements with ultra-short latencies. Nature 390, 512–515 (1997).
Miles, F. A. Visual Motion and its Role in the Stabilization of Gaze (eds Miles, F. A. & Wallman, J.) 393–403 (Elsevier, Amsterdam, 1993).
Miles, F. A. The neural processing of 3-D visual information: evidence from eye movements. Eur. J. Neurosci. 10, 811–822 (1998).
Schwarz, U., Busettini, C. & Miles, F. A. Ocular responses to linear motion are inversely proportional to viewing distance. Science 245, 1394–1396 (1989). A pioneering study showing for the first time that compensatory eye movements are generated either during translation in darkness (TVOR) or during lamellar optic flow stimulation (OFR).
Yang, D., Fitzgibbon, E. J. & Miles, F. A. Short-latency vergence eye movements induced by radial optic flow in humans: dependence on ambient vergence level. J. Neurophysiol. 81, 945–949 (1999).
Busettini, C., Miles, F. A., Schwarz, U. & Carl, J. R. Human ocular responses to translation of the observer and of the scene: dependence on viewing distance. Exp. Brain Res. 100, 484–494 (1994).
Busettini, C., Masson, G. S. & Miles, F. A. A role for stereoscopic depth cues in the rapid visual stabilization of the eyes. Nature 380, 342–345 (1996).
Busettini, C., Miles, F. A. & Krauzlis, R. J. Short-latency disparity vergence responses and their dependence on a prior saccadic eye movement. J. Neurophysiol. 75, 1392–1410 (1996).
Angelaki, D. E. & McHenry, M. Q. Short-latency primate vestibuloocular responses during translation. J. Neurophysiol. 82, 1651–1654 (1999).
Hess, B. J. & Angelaki, D. E. Vestibular contributions to gaze stability during transient forward and backward motion. J. Neurophysiol. 90, 1996–2004 (2003).
Paige, G. D. & Tomko, D. L. Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics. J. Neurophysiol. 65, 1170–1182 (1991).
Paige, G. D. & Tomko, D. L. Eye movement responses to linear head motion in the squirrel monkey. II. Visual-vestibular interactions and kinematic considerations. J. Neurophysiol. 65, 1183–1196 (1991).
Schwarz, U. & Miles, F. A. Ocular responses to translation and their dependence on viewing distance. I. Motion of the observer. J. Neurophysiol. 66, 851–864 (1991).
Telford, L., Seidman, S. H. & Paige, G. D. Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance. J. Neurophysiol. 78, 1775–1790 (1997).
Banks, M. S., Ehrlich, S. M., Backus, B. T. & Crowell, J. A. Estimating heading during real and simulated eye movements. Vision Res. 36, 431–443 (1996).
Royden, C. S., Banks, M. S. & Crowell, J. A. The perception of heading during eye movements. Nature 360, 583–585 (1992).
Royden, C. S. Analysis of misperceived observer motion during simulated eye rotations. Vision Res. 34, 3215–3222 (1994).
Van den Berg, A. V. Perception of heading. Nature 365, 497–498 (1993).
Van den Berg, A. V. & Brenner, E. Humans combine the optic flow with static depth cues for robust perception of heading. Vision Res. 34, 2153–2167 (1994).
Wertheim, A. H. Motion perception during self-motion: the direct versus inferential controversy revisited. Behav. Brain Sci. 17, 293–311 (1994).
Haarmeier, T., Their, P., Repnow, M. & Petersen, D. False perception of motion in a patient who cannot compensate for eye movements. Nature 389, 849–852 (1997).
Haarmeier, T., Bunjes, F., Lindner, A., Berret, E. & Their, P. Optimizing visual motion perception during eye movements. Neuron 32, 527–535 (2001).
Angelaki, D. E. & Hess, B. J. Direction of heading and vestibular control of binocular eye movements. Vision Res. 41, 3215–3228 (2001).
Angelaki, D. E., McHenry, M. Q. & Hess, B. J. Primate translational vestibuloocular reflexes. I. High-frequency dynamics and three-dimensional properties during lateral motion. J. Neurophysiol. 83, 1637–1647 (2000).
McHenry, M. Q. & Angelaki, D. E. Primate translational vestibuloocular reflexes. II. Version and vergence responses to fore-aft motion. J. Neurophysiol. 83, 1648–1661 (2000).
Medendorp, W. P., Van Gisbergen, J. A. & Gielen, C. C. Human gaze stabilization during active head translations. J. Neurophysiol. 87, 295–304 (2002).
Paige, G. D., Telford, L., Seidman, S. H. & Barnes, G. R. Human vestibuloocular reflex and its interactions with vision and fixation distance during linear and angular head movement. J. Neurophysiol. 80, 2391–2404 (1998).
Ramat, S. & Zee, D. S. Ocular motor responses to abrupt interaural head translation in normal humans. J. Neurophysiol. 90, 887–902 (2003).
Seidman, S. H., Paige, G. D. & Tomko, D. L. Adaptive plasticity in the naso-occipital linear vestibulo-ocular reflex. Exp. Brain Res. 125, 485–494 (1999).
Busettini, C., Miles, F. A. & Schwarz, U. Ocular responses to translation and their dependence on viewing distance. II. Motion of the scene. J. Neurophysiol. 66, 865–878 (1991).
Miles, F. A., Kawano, K. & Optican, L. M. Short-latency ocular following responses of monkey. I. Dependence on temporospatial properties of visual input. J. Neurophysiol. 56, 1321–1354 (1986).
Gellman, R. S., Carl, J. R. & Miles, F. A. Short latency ocular-following responses in man. Vis. Neurosci. 5, 107–122 (1990).
Cohen, B., Matsuo, V. & Raphan, T. Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. J. Physiol. (Lond.) 270, 321–344 (1977).
Miles, F. A. Eye Movement Research: Mechanisms, Processes and Applications (eds Findlay, J. M., Kentridge, R. W. & Walker, R.) 47–57 (Elsevier, Amsterdam, 1995).
Busettini, C., Fitzgibbon, E. J. & Miles, F. A. Short-latency disparity vergence in humans. J. Neurophysiol. 85, 1129–1152 (2001).
Kawano, K. & Miles, F. A. Short-latency ocular following responses of monkey. II. Dependence on a prior saccadic eye movement. J. Neurophysiol. 56, 1355–1380 (1986).
Lappe, M., Pekel, M. & Hoffmann, K. P. Optokinetic eye movements elicited by radial optic flow in the macaque monkey. J. Neurophysiol. 79, 1461–1480 (1998).
Niemann, T., Lappe, M., Buscher, A. & Hoffmann, K. P. Ocular responses to radial optic flow and single accelerated targets in humans. Vision Res. 39, 1359–1371 (1999).
Wei, M. & Angelaki, D. E. Does head rotation contribute to gaze stability during passive translations? J. Neurophysiol. 91, 1913–1918 (2004).
Keller, E. L. & Khan, N. S. Smooth-pursuit initiation in the presence of a textured background in monkey. Vision Res. 26, 943–955 (1986).
Kimmig, H. G., Miles, F. A. & Schwarz, U. Effects of stationary textured backgrounds on the initiation of pursuit eye movements in monkeys. J. Neurophysiol. 68, 2147–2164 (1992).
Mestre, D. R. & Masson, G. S. Ocular responses to motion parallax stimuli: the role of perceptual and attentional factors. Vision Res. 37, 1627–1641 (1997).
Masson, G. S., Busettini, C., Yang, D. S. & Miles, F. A. Short-latency ocular following in humans: sensitivity to binocular disparity. Vision Res. 41, 3371–3387 (2001).
Yang, D. S. & Miles, F. A. Short-latency ocular following in humans is dependent on absolute (rather than relative) binocular disparity. Vision Res. 43, 1387–1396 (2003).
Masson, G. S., Busettini, C. & Miles, F. A. Vergence eye movements in response to binocular disparity without depth perception. Nature 389, 283–286 (1997). Shows that disparity-driven vergence responses of opposite direction can be elicited with dense anticorrelated patterns, in which each black dot in one eye is matched to a white dot in the other eye, despite the fact that humans fail to perceive depth in such stimuli. These results suggest that visual signals for these responses arise from an early, pre-perceptual, stage of cortical processing.
Treue, S., Husain, M. & Andersen, R. A. Human perception of structure from motion. Vision Res. 31, 59–75 (1991).
Mays, L. E. Neural control of vergence eye movements: convergence and divergence neurons in midbrain. J. Neurophysiol. 51, 1091–1108 (1984).
Mays, L. E. & Gamlin, P. D. Neuronal circuitry controlling the near response. Curr. Opin. Neurobiol. 5, 763–768 (1995).
Bishop, P. O. Vertical disparity, egocentric distance and stereoscopic depth constancy: a new interpretation. Proc. R. Soc. Lond. B 237, 445–469 (1989).
Cumming, B. G., Johnston, E. B. & Parker, A. J. Vertical disparities and perception of three-dimensional shape. Nature 349, 411–413 (1991).
Mayhew, J. E. & Longuet-Higgins, H. C. A computational model of binocular depth perception. Nature 297, 376–378 (1982).
Bradshaw, M. F., Glennerster, A. & Rogers, B. J. The effect of display size on disparity scaling from differential perspective and vergence cues. Vision Res. 36, 1255–1264 (1996).
Rogers, B. J. & Bradshaw, M. F. Vertical disparities, differential perspective and binocular stereopsis. Nature 361, 253–255 (1993).
Rogers, B. J. & Bradshaw, M. F. Disparity scaling and the perception of frontoparallel surfaces. Perception 24, 155–179 (1995).
Wei, M., DeAngelis, G. C. & Angelaki, D. E. Do visual cues contribute to the neural estimate of viewing distance used by the oculomotor system? J. Neurosci. 23, 8340–8350 (2003). Tests whether visual cues to viewing distance (for example, vertical disparities) can be used by the vestibulomotor system to scale the TVOR. The results show that only motor, but not visual, cues are important for the viewing distance-dependent scaling of the TVOR.
Snyder, L. H., Lawrence, D. M. & King, W. M. Changes in vestibulo-ocular reflex (VOR) anticipate changes in vergence angle in monkey. Vision Res. 32, 569–575 (1992).
Cumming, B. G. & Parker, A. J. Responses of primary visual cortical neurons to binocular disparity without depth perception. Nature 389, 280–283 (1997).
Masson, G. S., Yang, D. S. & Miles, F. A. Reversed short-latency ocular following. Vision Res. 42, 2081–2087 (2002).
Duffy, C. J. & Wurtz, R. H. Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. J. Neurophysiol. 65, 1329–1345 (1991).
Lappe, M., Bremmer, F., Pekel, M., Thiele, A. & Hoffmann, K. P. Optic flow processing in monkey STS: a theoretical and experimental approach. J. Neurosci. 16, 6265–6285 (1996).
Paige, W. K. & Duffy, C. J. Heading representation in MST: sensory interactions and population encoding. J. Neurophysiol. 89, 1994–2013 (2003).
Duffy, C. J. MST neurons respond to optic flow and translational movement. J. Neurophysiol. 80, 1816–1827 (1998).
Britten, K. H. Clustering of response selectivity in the medial superior temporal area of extrastriate cortex in the macaque monkey. Vis. Neurosci. 15, 553–558 (1998).
Tanaka, K. et al. Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. J. Neurosci. 6, 134–144 (1986).
Tanaka, K., Fukada, Y. & Saito, H. A. Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. J. Neurophysiol. 62, 642–656 (1989).
Gu, Y., Watkins, P. V., Angelaki, D. E. & DeAngelis, G. C. Visual and non-visual contributions to 3D heading selectivity in area MSTd. J. Neurosci. (in the press).
Glickstein, M. et al. Visual pontocerebellar projections in the macaque. J. Comp. Neurol. 349, 51–72 (1994).
Dursteler, M. R. & Wurtz, R. H. Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. J. Neurophysiol. 60, 940–965 (1988).
Inoue, Y., Takemura, A., Kawano, K. & Mustari, M. J. Role of the pretectal nucleus of the optic tract in short-latency ocular following responses in monkeys. Exp. Brain Res. 131, 269–281 (2000).
May, J. G., Keller, E. L. & Suzuki, D. A. Smooth-pursuit eye movement deficits with chemical lesions in the dorsolateral pontine nucleus of the monkey. J. Neurophysiol. 59, 952–977 (1988).
Zee, D. S., Yamazaki, A., Butler, P. H. & Gucer, G. Effects of ablation of flocculus and paraflocculus of eye movements in primate. J. Neurophysiol. 46, 878–899 (1981).
Kawano, K., Shidara, M. & Yamane, S. Neural activity in dorsolateral pontine nucleus of alert monkey during ocular following responses. J. Neurophysiol. 67, 680–703 (1992).
Kawano, K., Shidara, M., Watanabe, Y. & Yamane, S. Neural activity in cortical area MST of alert monkey during ocular following responses. J. Neurophysiol. 71, 2305–2324 (1994).
Shidara, M. & Kawano, K. Role of Purkinje cells in the ventral paraflocculus in short-latency ocular following responses. Exp. Brain Res. 93, 185–195 (1993).
Shidara, M., Kawano, K., Gomi, H. & Kawato, M. Inverse-dynamics model eye movement control by Purkinje cells in the cerebellum. Nature 365, 50–52 (1993).
Gomi, H. et al. Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys I. Simple spikes. J. Neurophysiol. 80, 818–831 (1998).
Takemura, A., Inoue, Y., Gomi, H., Kawato, M. & Kawano, K. Change in neuronal firing patterns in the process of motor command generation for the ocular following response. J. Neurophysiol. 86, 1750–1763 (2001).
Nagao, S., Kitamura, T., Nakamura, N., Hiramatsu, T. & Yamada, J. Differences of the primate flocculus and ventral paraflocculus in the mossy and climbing fiber input organization. J. Comp. Neurol. 382, 480–498 (1997).
Inoue, Y., Takemura, A., Kawano, K., Kitama, T. & Miles, F. A. Dependence of short-latency ocular following and associated activity in the medial superior temporal area (MST) on ocular vergence. Exp. Brain Res. 121, 135–144 (1998).
Keating, E. G., Pierre, A. & Chopra, S. Ablation of the pursuit area in the frontal cortex of the primate degrades foveal but not optokinetic smooth eye movements. J. Neurophysiol. 76, 637–641 (1996).
Buttner, U. & Waespe, W. Purkinje cell activity in the primate flocculus during optokinetic stimulation, smooth pursuit eye movements and VOR-suppression. Exp. Brain Res. 55, 97–104 (1984).
Zhou, H. H., Wei, M. & Angelaki, D. E. Motor scaling by viewing distance of early visual motion signals during smooth pursuit. J. Neurophysiol. 88, 2880–2885 (2002).
Takemura, A., Inoue, Y., Kawano, K., Quaia, C. & Miles, F. A. Single-unit activity in cortical area MST associated with disparity-vergence eye movements: evidence for population coding. J. Neurophysiol. 85, 2245–2266 (2001). Shows that the population activity of MST neurons might participate in the generation of the short-latency disparity-driven vergence component of the visuomotor responses.
Schaafsma, S. J. & Duysens, J. Neurons in the ventral intraparietal area of awake macaque monkey closely resemble neurons in the dorsal part of the medial superior temporal area in their responses to optic flow patterns. J. Neurophysiol. 76, 4056–4068 (1996).
Siegel, R. M. & Read, H. L. Analysis of optic flow in the monkey parietal area 7a. Cereb. Cortex 7, 327–346 (1997).
Anderson, K. C. & Siegel, R. M. Optic flow selectivity in the anterior superior temporal polysensory area, STPa, of the behaving monkey. J. Neurosci. 19, 2681–2692 (1999).
Bremmer, F., Duhamel, J. R., Ben Hamed, S. & Graf, W. Heading encoding in the macaque ventral intraparietal area (VIP). Eur. J. Neurosci. 16, 1554–1568 (2002).
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).
Angelaki, D. E., Green, A. M. & Dickman, J. D. Differential sensorimotor processing of vestibulo-ocular signals during rotation and translation. J. Neurosci. 21, 3968–3985 (2001).
Chen-Huang, C. & McCrea, R. A. Effects of viewing distance on the responses of vestibular neurons to combined angular and linear vestibular stimulation. J. Neurophysiol. 81, 2538–2557 (1999).
Crowell, J. A., Banks, M. S., Shenoy, K. V. & Andersen, R. A. Visual self-motion perception during head turns. Nature Neurosci. 1, 732–737 (1998).
Crowell, J. A. & Banks, M. S. Perceiving heading with different retinal regions and types of optic flow. Percept. Psychophys. 53, 325–337 (1993).
Land, M. F. & Lee, D. N. Where we look when we steer. Nature 369, 742–744 (1994).
Wann, J. P., Swapp, D. & Rushton, S. K. Heading perception and the allocation of attention. Vision Res. 40, 2533–2543 (2000).
Britten, K. H. & Van Wezel, R. J. Area MST and heading perception in macaque monkeys. Cereb. Cortex 12, 692–701 (2002). Using electrical microstimulation of the MST cortex to bias perception of movement direction from optic flow, this study provides behavioural evidence supporting the idea that optic flow-sensitive MST neurons might be involved in perception. Although the positive effects were weak, this study represents the only experiment so far to show a direct neural involvement in perception of movement direction from optic flow.
Heuer, H. W. & Britten, K. H. Optic flow signals in extrastriate area MST: comparison of perceptual and neuronal sensitivity. J. Neurophysiol. 91, 1314–1326 (2004).
Einstein, A. Über das Relativitätsprinzip und die aus demselben gezogenen Folgerungen. Jahrb. Radioakt. 4, 411–462 (1908).
Angelaki, D. E. & Dickman, J. D. Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J. Neurophysiol. 84, 2113–2132 (2000).
Fernandez, C. & Goldberg, J. M. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J. Neurophysiol. 39, 996–1008 (1976).
Angelaki, D. E., McHenry, M. Q., Dickman, J. D., Newlands, S. D. & Hess, B. J. Computation of inertial motion: neural strategies to resolve ambiguous otolith information. J. Neurosci. 19, 316–327 (1999). By characterizing the TVOR after inactivation of the semicircular canals, this study provides the first direct behavioural evidence that reflexive vestibulomotor responses during translation do not arise exclusively from the otolith organs of the vestibular system. Instead, the internal estimate of translation arises from a central processing of both otolith and semicircular canal information.
Green, A. M. & Angelaki, D. E. Resolution of sensory ambiguities for gaze stabilization requires a second neural integrator. J. Neurosci. 23, 9265–9275 (2003).
Green, A. M. & Angelaki, D. E. An integrative neural network for detecting inertial motion and head orientation. J. Neurophysiol. 92, 905–925 (2004).
Merfeld, D. M. Modeling the vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp. Brain Res. 106, 123–134 (1995).
Merfeld, D. M. & Zupan, L. H. Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. J. Neurophysiol. 87, 819–833 (2002).
Mergner, T. & Glasauer, S. A simple model of vestibular canal-otolith signal fusion. Ann. NY Acad. Sci. 871, 430–434 (1999).
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).
Angelaki, D. E., Shaikh, A. G., Green, A. M. & Dickman, J. D. Neurons compute internal models of the physical laws of motion. Nature 430, 560–564 (2004). Provides the first neural evidence for the existence of subcortical neural populations that use the two vestibular sensory signals to compute an internal model of self-motion.
Green, A. M., Shaikh, A. G. & Angelaki, D. E. Sensory vestibular contributions to constructing internal models of self-motion. J. Neural Eng. 2, S164–S179 (2005).
Merfeld, D. M., Zupan, L. & Peterka, R. J. Humans use internal models to estimate gravity and linear acceleration. Nature 398, 615–618 (1999).
Shaikh, A. G. et al. Sensory convergence solves a motion ambiguity problem. Curr. Biol. 15, 1657–1662 (2005).
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The authors' work is supported by grants from the National Institutes of Health (NIH) and the Swiss National Science Foundation.
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Glossary
- OCULAR FOLLOWING REFLEX
-
(OFR). Short-latency reflexive eye movements in response to the optic flow experienced during self-motion. These responses, which can be either conjugate or disjunctive, are typically studied during the first ∼100 ms of brief presentations of visual motion (open-loop conditions).
- BINOCULAR DISPARITY
-
Differences in the position of similar images in the two eyes. Side-to-side differences are called horizontal disparities and can produce a compelling sensation of three-dimensionality. Differences in the up–down position are known as vertical disparities.
- VESTIBULAR END ORGANS
-
A set of balance receptors in the inner ear, consisting of the otolith organs (utricle and sacculus) that encode linear acceleration and the semicircular canals (lateral, anterior and posterior) that measure angular acceleration.
- RETINAL IMAGE SLIP
-
The difference between the velocity of the movement of a retinal image and the eye, which is picked up by motion detectors in the visual system.
- CONJUGATE EYE MOVEMENTS
-
Eye movements of similar amplitude and direction in the two eyes.
- DISJUNCTIVE EYE MOVEMENTS
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Eye movements that differ in amplitude between the two eyes. The disjunctive components are typically quantified by measuring the vergence angle, which is defined as the difference between the right and left eye positions.
- IMAGE SHEAR
-
Deformation of retinal image due to translation of the subject.
- SEMICIRCULAR CANALS
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One of the two sets of vestibular end organs that measure angular acceleration of the head. In each ear, there are three semicircular canals, the lateral, anterior and posterior, each of which senses angular motion in each of three orthogonal planes.
- OTOLITH ORGANS
-
Linear acceleration sensors that are located in the inner ear and consist of receptor hair cells with different polarization vectors distributed over the utricular (approximately horizontal) and the saccular (approximately in the sagittal plane) maculae.
- ACCOMMODATION
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The automatic adjustment of the eye to allow it to see at different distances, which is chiefly brought about by changes in the convexity of the lens. Horizontal vergence and accommodation normally occur together. The two responses are accompanied by an appropriate change in pupil diameter. The three concomitant changes are known as the near-triad response.
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Angelaki, D., Hess, B. Self-motion-induced eye movements: effects on visual acuity and navigation. Nat Rev Neurosci 6, 966–976 (2005). https://doi.org/10.1038/nrn1804
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DOI: https://doi.org/10.1038/nrn1804
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