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Self-motion-induced eye movements: effects on visual acuity and navigation

Key Points

  • 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.

  • 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.

  • 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.

  • 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.

  • 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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Figure 1: Optic flow experienced when looking out the window of a moving train or when walking forward.
Figure 2: The translational vestibulo-ocular reflex depends on viewing distance, movement direction and gaze direction.
Figure 3: The ocular following reflex depends on viewing distance.
Figure 4: Summary of sensorimotor circuitry for the generation of visuomotor and vestibulomotor eye movements during translational self-motion.
Figure 5: Optic flow experienced when moving forward while looking away from the direction of movement.

References

  1. Gibson, J. J. The visual perception of objective motion and subjective movement. Psychol. Rev. 61, 304–314 (1954).

    CAS  PubMed  Article  Google Scholar 

  2. 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.

    CAS  PubMed  Article  Google Scholar 

  3. Warren, W. H. Jr & Hannon, D. J. Direction of self-motion is perceived from optical flow. Nature 336, 162–163 (1988).

    Article  Google Scholar 

  4. 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).

    PubMed  Article  Google Scholar 

  5. Warren, W. H. Jr & Hannon, D. J. Eye movements and optical flow. J. Opt. Soc. Am. A 7, 160–169 (1990).

    PubMed  Article  Google Scholar 

  6. 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).

    CAS  PubMed  Article  Google Scholar 

  7. Busettini, C., Masson, G. S. & Miles, F. A. Radial optic flow induces vergence eye movements with ultra-short latencies. Nature 390, 512–515 (1997).

    CAS  PubMed  Article  Google Scholar 

  8. Miles, F. A. Visual Motion and its Role in the Stabilization of Gaze (eds Miles, F. A. & Wallman, J.) 393–403 (Elsevier, Amsterdam, 1993).

    Google Scholar 

  9. Miles, F. A. The neural processing of 3-D visual information: evidence from eye movements. Eur. J. Neurosci. 10, 811–822 (1998).

    CAS  PubMed  Article  Google Scholar 

  10. 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).

    CAS  PubMed  Article  Google Scholar 

  11. 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).

    CAS  PubMed  Article  Google Scholar 

  12. 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).

    CAS  Article  PubMed  Google Scholar 

  13. 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).

    CAS  Article  PubMed  Google Scholar 

  14. 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).

    CAS  Article  PubMed  Google Scholar 

  15. Angelaki, D. E. & McHenry, M. Q. Short-latency primate vestibuloocular responses during translation. J. Neurophysiol. 82, 1651–1654 (1999).

    CAS  PubMed  Article  Google Scholar 

  16. Hess, B. J. & Angelaki, D. E. Vestibular contributions to gaze stability during transient forward and backward motion. J. Neurophysiol. 90, 1996–2004 (2003).

    PubMed  Article  Google Scholar 

  17. 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).

    CAS  PubMed  Article  Google Scholar 

  18. 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).

    CAS  PubMed  Article  Google Scholar 

  19. 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).

    CAS  PubMed  Article  Google Scholar 

  20. 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).

    CAS  PubMed  Article  Google Scholar 

  21. 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).

    CAS  PubMed  Article  Google Scholar 

  22. Royden, C. S., Banks, M. S. & Crowell, J. A. The perception of heading during eye movements. Nature 360, 583–585 (1992).

    CAS  PubMed  Article  Google Scholar 

  23. Royden, C. S. Analysis of misperceived observer motion during simulated eye rotations. Vision Res. 34, 3215–3222 (1994).

    CAS  PubMed  Article  Google Scholar 

  24. Van den Berg, A. V. Perception of heading. Nature 365, 497–498 (1993).

    CAS  PubMed  Article  Google Scholar 

  25. 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).

    CAS  PubMed  Article  Google Scholar 

  26. Wertheim, A. H. Motion perception during self-motion: the direct versus inferential controversy revisited. Behav. Brain Sci. 17, 293–311 (1994).

    Article  Google Scholar 

  27. 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).

    CAS  PubMed  Article  Google Scholar 

  28. Haarmeier, T., Bunjes, F., Lindner, A., Berret, E. & Their, P. Optimizing visual motion perception during eye movements. Neuron 32, 527–535 (2001).

    CAS  PubMed  Article  Google Scholar 

  29. Angelaki, D. E. & Hess, B. J. Direction of heading and vestibular control of binocular eye movements. Vision Res. 41, 3215–3228 (2001).

    CAS  PubMed  Article  Google Scholar 

  30. 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).

    CAS  PubMed  Article  Google Scholar 

  31. 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).

    CAS  PubMed  Article  Google Scholar 

  32. Medendorp, W. P., Van Gisbergen, J. A. & Gielen, C. C. Human gaze stabilization during active head translations. J. Neurophysiol. 87, 295–304 (2002).

    CAS  PubMed  Article  Google Scholar 

  33. 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).

    CAS  PubMed  Article  Google Scholar 

  34. Ramat, S. & Zee, D. S. Ocular motor responses to abrupt interaural head translation in normal humans. J. Neurophysiol. 90, 887–902 (2003).

    PubMed  Article  Google Scholar 

  35. 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).

    CAS  PubMed  Article  Google Scholar 

  36. 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).

    CAS  PubMed  Article  Google Scholar 

  37. 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).

    CAS  Article  PubMed  Google Scholar 

  38. Gellman, R. S., Carl, J. R. & Miles, F. A. Short latency ocular-following responses in man. Vis. Neurosci. 5, 107–122 (1990).

    CAS  Article  PubMed  Google Scholar 

  39. 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).

    CAS  Article  Google Scholar 

  40. Miles, F. A. Eye Movement Research: Mechanisms, Processes and Applications (eds Findlay, J. M., Kentridge, R. W. & Walker, R.) 47–57 (Elsevier, Amsterdam, 1995).

    Book  Google Scholar 

  41. Busettini, C., Fitzgibbon, E. J. & Miles, F. A. Short-latency disparity vergence in humans. J. Neurophysiol. 85, 1129–1152 (2001).

    CAS  PubMed  Article  Google Scholar 

  42. 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).

    CAS  PubMed  Article  Google Scholar 

  43. 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).

    CAS  PubMed  Article  Google Scholar 

  44. 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).

    CAS  PubMed  Article  Google Scholar 

  45. Wei, M. & Angelaki, D. E. Does head rotation contribute to gaze stability during passive translations? J. Neurophysiol. 91, 1913–1918 (2004).

    PubMed  Article  Google Scholar 

  46. Keller, E. L. & Khan, N. S. Smooth-pursuit initiation in the presence of a textured background in monkey. Vision Res. 26, 943–955 (1986).

    CAS  PubMed  Article  Google Scholar 

  47. 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).

    CAS  PubMed  Article  Google Scholar 

  48. 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).

    CAS  PubMed  Article  Google Scholar 

  49. 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).

    CAS  PubMed  Article  Google Scholar 

  50. 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).

    PubMed  PubMed Central  Article  Google Scholar 

  51. 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.

    CAS  PubMed  Article  Google Scholar 

  52. Treue, S., Husain, M. & Andersen, R. A. Human perception of structure from motion. Vision Res. 31, 59–75 (1991).

    CAS  PubMed  Article  Google Scholar 

  53. Mays, L. E. Neural control of vergence eye movements: convergence and divergence neurons in midbrain. J. Neurophysiol. 51, 1091–1108 (1984).

    CAS  PubMed  Article  Google Scholar 

  54. Mays, L. E. & Gamlin, P. D. Neuronal circuitry controlling the near response. Curr. Opin. Neurobiol. 5, 763–768 (1995).

    CAS  PubMed  Article  Google Scholar 

  55. Bishop, P. O. Vertical disparity, egocentric distance and stereoscopic depth constancy: a new interpretation. Proc. R. Soc. Lond. B 237, 445–469 (1989).

    CAS  PubMed  Article  Google Scholar 

  56. Cumming, B. G., Johnston, E. B. & Parker, A. J. Vertical disparities and perception of three-dimensional shape. Nature 349, 411–413 (1991).

    CAS  PubMed  Article  Google Scholar 

  57. Mayhew, J. E. & Longuet-Higgins, H. C. A computational model of binocular depth perception. Nature 297, 376–378 (1982).

    CAS  PubMed  Article  Google Scholar 

  58. 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).

    CAS  PubMed  Article  Google Scholar 

  59. Rogers, B. J. & Bradshaw, M. F. Vertical disparities, differential perspective and binocular stereopsis. Nature 361, 253–255 (1993).

    CAS  PubMed  Article  Google Scholar 

  60. Rogers, B. J. & Bradshaw, M. F. Disparity scaling and the perception of frontoparallel surfaces. Perception 24, 155–179 (1995).

    CAS  PubMed  Article  Google Scholar 

  61. 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.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  62. 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).

    CAS  PubMed  Article  Google Scholar 

  63. Cumming, B. G. & Parker, A. J. Responses of primary visual cortical neurons to binocular disparity without depth perception. Nature 389, 280–283 (1997).

    CAS  PubMed  Article  Google Scholar 

  64. Masson, G. S., Yang, D. S. & Miles, F. A. Reversed short-latency ocular following. Vision Res. 42, 2081–2087 (2002).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. 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).

    CAS  Article  PubMed  Google Scholar 

  66. 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).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  69. 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).

    CAS  PubMed  Article  Google Scholar 

  70. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  71. 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).

    CAS  Article  PubMed  Google Scholar 

  72. 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).

  73. Glickstein, M. et al. Visual pontocerebellar projections in the macaque. J. Comp. Neurol. 349, 51–72 (1994).

    CAS  PubMed  Article  Google Scholar 

  74. 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).

    CAS  PubMed  Article  Google Scholar 

  75. 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).

    CAS  PubMed  Article  Google Scholar 

  76. 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).

    CAS  PubMed  Article  Google Scholar 

  77. 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).

    CAS  PubMed  Article  Google Scholar 

  78. 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).

    CAS  PubMed  Article  Google Scholar 

  79. 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).

    CAS  Article  PubMed  Google Scholar 

  80. 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).

    CAS  PubMed  Article  Google Scholar 

  81. 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).

    CAS  PubMed  Article  Google Scholar 

  82. 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).

    CAS  PubMed  Article  Google Scholar 

  83. 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).

    CAS  PubMed  Article  Google Scholar 

  84. 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).

    CAS  PubMed  Article  Google Scholar 

  85. 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).

    CAS  PubMed  Article  Google Scholar 

  86. 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).

    CAS  PubMed  Article  Google Scholar 

  87. 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).

    CAS  PubMed  Article  Google Scholar 

  88. 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).

    PubMed  Article  Google Scholar 

  89. 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.

    CAS  PubMed  Article  Google Scholar 

  90. 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).

    CAS  PubMed  Article  Google Scholar 

  91. Siegel, R. M. & Read, H. L. Analysis of optic flow in the monkey parietal area 7a. Cereb. Cortex 7, 327–346 (1997).

    CAS  PubMed  Article  Google Scholar 

  92. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  93. 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).

    PubMed  Article  Google Scholar 

  94. 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).

    PubMed  Article  Google Scholar 

  95. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  96. 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).

    CAS  PubMed  Article  Google Scholar 

  97. 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).

    CAS  PubMed  Article  Google Scholar 

  98. Crowell, J. A. & Banks, M. S. Perceiving heading with different retinal regions and types of optic flow. Percept. Psychophys. 53, 325–337 (1993).

    CAS  PubMed  Article  Google Scholar 

  99. Land, M. F. & Lee, D. N. Where we look when we steer. Nature 369, 742–744 (1994).

    CAS  PubMed  Article  Google Scholar 

  100. Wann, J. P., Swapp, D. & Rushton, S. K. Heading perception and the allocation of attention. Vision Res. 40, 2533–2543 (2000).

    CAS  PubMed  Article  Google Scholar 

  101. 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.

    PubMed  Article  Google Scholar 

  102. 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).

    PubMed  Article  Google Scholar 

  103. Einstein, A. Über das Relativitätsprinzip und die aus demselben gezogenen Folgerungen. Jahrb. Radioakt. 4, 411–462 (1908).

    Google Scholar 

  104. Angelaki, D. E. & Dickman, J. D. Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J. Neurophysiol. 84, 2113–2132 (2000).

    CAS  PubMed  Article  Google Scholar 

  105. 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).

    CAS  PubMed  Article  Google Scholar 

  106. 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.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  107. Green, A. M. & Angelaki, D. E. Resolution of sensory ambiguities for gaze stabilization requires a second neural integrator. J. Neurosci. 23, 9265–9275 (2003).

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  108. Green, A. M. & Angelaki, D. E. An integrative neural network for detecting inertial motion and head orientation. J. Neurophysiol. 92, 905–925 (2004).

    PubMed  Article  Google Scholar 

  109. 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).

    CAS  PubMed  Article  Google Scholar 

  110. 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).

    CAS  PubMed  Article  Google Scholar 

  111. Mergner, T. & Glasauer, S. A simple model of vestibular canal-otolith signal fusion. Ann. NY Acad. Sci. 871, 430–434 (1999).

    CAS  PubMed  Article  Google Scholar 

  112. 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).

    CAS  PubMed  Article  Google Scholar 

  113. 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.

    CAS  PubMed  Article  Google Scholar 

  114. 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).

    PubMed  Article  Google Scholar 

  115. Merfeld, D. M., Zupan, L. & Peterka, R. J. Humans use internal models to estimate gravity and linear acceleration. Nature 398, 615–618 (1999).

    CAS  PubMed  Article  Google Scholar 

  116. Shaikh, A. G. et al. Sensory convergence solves a motion ambiguity problem. Curr. Biol. 15, 1657–1662 (2005).

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

The authors' work is supported by grants from the National Institutes of Health (NIH) and the Swiss National Science Foundation.

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Correspondence to Dora E. Angelaki.

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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

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

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

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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