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Annual Review of Vision Science

Volume 2, 2016

Corollary Discharge and Oculomotor Proprioception: Cortical Mechanisms for Spatially Accurate Vision

Abstract

A classic problem in psychology is understanding how the brain creates a stable and accurate representation of space for perception and action despite a constantly moving eye. Two mechanisms have been proposed to solve this problem: Herman von Helmholtz's idea that the brain uses a corollary discharge of the motor command that moves the eye to adjust the visual representation, and Sir Charles Sherrington's idea that the brain measures eye position to calculate a spatial representation. Here, we discuss the cognitive, neuropsychological, and physiological mechanisms that support each of these ideas. We propose that both are correct: A rapid corollary discharge signal remaps the visual representation before an impending saccade, computing accurate movement vectors; and an oculomotor proprioceptive signal enables the brain to construct a more accurate craniotopic representation of space that develops slowly after the saccade.

Keyword(s): corollary discharge, craniotopic representation, oculomotor proprioception, predictive, remapping, retinotopic representation, saccade, spatial accuracy
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2016-10-14
2024-04-19
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Literature Cited

  1. Andersen RA, Essick GK, Siegel RM. 1985. Encoding of spatial location by posterior parietal neurons. Science 230:456–58 [Google Scholar]
  2. Andersen RA, Mountcastle VB. 1983. The influence of the angle of gaze upon the excitability of the light-sensitive neurons of the posterior parietal cortex. J. Neurosci. 3:532–48 [Google Scholar]
  3. Balslev D, Miall RC. 2008. Eye position representation in human anterior parietal cortex. J. Neurosci. 28:8968–72 [Google Scholar]
  4. Barash S, Bracewell RM, Fogassi L, Gnadt JW, Andersen RA. 1991. Saccade-related activity in the lateral intraparietal area. II. Spatial properties. J. Neurophysiol. 66:1109–24 [Google Scholar]
  5. Batista AP, Buneo CA, Snyder LH, Andersen RA. 1999. Reach plans in eye-centered coordinates. Science 285:257–60 [Google Scholar]
  6. Ben Hamed S, Duhamel J-R, Bremmer F, Graf W. 2001. Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis. Exp. Brain Res. 140:127–44 [Google Scholar]
  7. Bisley JW, Goldberg ME. 2003. Neuronal activity in the lateral intraparietal area and spatial attention. Science 299:81–86 [Google Scholar]
  8. Bisley JW, Goldberg ME. 2010. Attention, intention, and priority in the parietal lobe. Annu. Rev. Neurosci. 33:1–21 [Google Scholar]
  9. Blakemore SJ, Goodbody SJ, Wolpert DM. 1998. Predicting the consequences of our own actions: the role of sensorimotor context estimation. J. Neurosci. 18:7511–18 [Google Scholar]
  10. Bridgeman B, Stark L. 1991. Ocular proprioception and efference copy in registering visual direction. Vis. Res. 31:1903–13 [Google Scholar]
  11. Cannon SC, Robinson DA. 1987. Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J. Neurophysiol. 57:1383–409 [Google Scholar]
  12. Colby CL, Goldberg ME. 1999. Space and attention in parietal cortex. Annu. Rev. Neurosci. 23:319–49 [Google Scholar]
  13. Cooper S, Daniel PM. 1949. Muscle spindles in human extrinsic eye muscles. Brain 72:1–24 [Google Scholar]
  14. Dassonville P, Schlag J, Schlag-Rey M. 1992. Oculomotor localization relies on a damped representation of saccadic eye displacement in human and nonhuman primates. Vis. Neurosci. 9:261–69 [Google Scholar]
  15. Dayan P, Abbott LF. 2001. Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems Cambridge, MA: MIT Press
  16. Donaldson IM. 2000. The functions of the proprioceptors of the eye muscles. Philos. Trans. R. Soc. B 355:1685–754 [Google Scholar]
  17. Duhamel J-R, Bremmer F, Ben Hamed S, Graf W. 1997. Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389:845–48 [Google Scholar]
  18. Duhamel J-R, Colby CL, Goldberg ME. 1992a. The updating of the representation of visual space in parietal cortex by intended eye movements. Science 255:90–92 [Google Scholar]
  19. Duhamel J-R, Goldberg ME, FitzGibbon EJ, Sirigu A, Grafman J. 1992b. Saccadic dysmetria in a patient with a right frontoparietal lesion: the importance of corollary discharge for accurate spatial behavior. Brain 115:1387–402 [Google Scholar]
  20. Fogassi L, Gallese V, di Pellegrino G, Fadiga L, Gentilucci M. et al. 1992. Space coding by premotor cortex. Exp. Brain Res. 89:686–90 [Google Scholar]
  21. Galletti C, Battaglini PP, Fattori P. 1995. Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur. J. Neurosci. 7:2486–501 [Google Scholar]
  22. Gauthier GM, Nommay D, Vercher JL. 1990. Ocular muscle proprioception and visual localization of targets in man. Brain 113:1857–71 [Google Scholar]
  23. Goldberg ME, Bruce CJ. 1990. Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. J. Neurophysiol. 64:489–508 [Google Scholar]
  24. Goldberg ME, Colby CL, Duhamel J-R. 1990. Representation of visuomotor space in the parietal lobe of the monkey. Cold Spring Harb. Symp. Quant. Biol. 55:729–39 [Google Scholar]
  25. Goldberg ME, Wurtz RH. 1972. Activity of superior colliculus in behaving monkey: I. Visual receptive fields of single neurons. J. Neurophysiol. 35:542–59 [Google Scholar]
  26. Gottlieb JP, Kusunoki M, Goldberg ME. 1998. The representation of visual salience in monkey parietal cortex. Nature 391:481–84 [Google Scholar]
  27. Graf AB, Andersen RA. 2014. Inferring eye position from populations of lateral intraparietal neurons. eLife 3e02813
  28. Guthrie BL, Porter JD, Sparks DL. 1983. Corollary discharge provides accurate eye position information to the oculomotor system. Science 221:1193–95 [Google Scholar]
  29. Hallett PE, Lightstone AD. 1976. Saccadic eye movements to flashed targets. Vis. Res. 16:107–14 [Google Scholar]
  30. Heide W, Blankenburg M, Zimmermann E, Kömpf D. 1995. Cortical control of double-step saccades: implications for spatial orientation. Ann. Neurol. 38:739–48 [Google Scholar]
  31. Jeffries SM, Kusunoki M, Bisley JW, Cohen IS, Goldberg ME. 2007. Rhesus monkeys mislocalize saccade targets flashed for 100 ms around the time of a saccade. Vis. Res. 47:1924–34 [Google Scholar]
  32. Joiner W, Cavanaugh J, Wurtz R. 2011. Modulation of shifting receptive field activity in frontal eye field by visual salience. J. Neurophysiol. 106:1179–269 [Google Scholar]
  33. Karn KS, Møller P, Hayhoe MM. 1997. Reference frames in saccadic targeting. Exp. Brain Res. 115:267–82 [Google Scholar]
  34. Kusunoki M, Goldberg ME. 2003. The time course of perisaccadic receptive field shifts in the lateral intraparietal area of the monkey. J. Neurophysiol. 89:1519–27 [Google Scholar]
  35. Lewis RF, Gaymard BM, Tamargo RJ. 1998. Efference copy provides the eye position information required for visually guided reaching. J. Neurophysiol. 80:1605–8 [Google Scholar]
  36. Lewis RF, Zee DS. 1993. Abnormal spatial localization with trigeminal-oculomotor synkinesis. Evidence for a proprioceptive effect. Brain 116:1105–18 [Google Scholar]
  37. Lewis RF, Zee DS, Gaymard BM, Guthrie BL. 1994. Extraocular muscle proprioception functions in the control of ocular alignment and eye movement conjugacy. J. Neurophysiol. 72:1028–31 [Google Scholar]
  38. Lienbacher K, Horn AK. 2012. Palisade endings and proprioception in extraocular muscles: a comparison with skeletal muscles. Biol. Cybern. 106:643–55 [Google Scholar]
  39. Lienbacher K, Mustari M, Hess B, Büttner-Ennever J, Horn AK. 2011. Is there any sense in the Palisade endings of eye muscles?. Ann. N.Y. Acad. Sci. 1233:1–7 [Google Scholar]
  40. Mathôt S, Theeuwes J. 2013. A reinvestigation of the reference frame of the tilt-adaptation aftereffect. Sci. Rep. 3:1152 [Google Scholar]
  41. Mays LE, Sparks DL. 1980a. Dissociation of visual and saccade-related responses in superior colliculus neurons. J. Neurophysiol. 43:207–32 [Google Scholar]
  42. Mays LE, Sparks DL. 1980b. Saccades are spatially, not retinocentrically, coded. Science 208:1163–65 [Google Scholar]
  43. Melcher D. 2007. Predictive remapping of visual features precedes saccadic eye movements. Nat. Neurosci. 10:903–7 [Google Scholar]
  44. Merriam EP, Genovese CR, Colby CL. 2003. Spatial updating in human parietal cortex. Neuron 39:361–73 [Google Scholar]
  45. Nakamura K, Colby CL. 2002. Updating of the visual representation in monkey striate and extrastriate cortex during saccades. PNAS 99:4026–31 [Google Scholar]
  46. Neupane S, Guitton D, Pack CC. 2016. Two distinct types of remapping in primate cortical area V4. Nat. Commun. 7:10402 [Google Scholar]
  47. Phillips AN, Segraves MA. 2010. Predictive activity in macaque frontal eye field neurons during natural scene searching. J. Neurophysiol. 103:1238–52 [Google Scholar]
  48. Poletti M, Burr DC, Rucci M. 2013. Optimal multimodal integration in spatial localization. J. Neurosci. 33:14259–68 [Google Scholar]
  49. Pouget A, Sejnowski TJ. 2001. Simulating a lesion in a basis function model of spatial representations: comparison with hemineglect. Psychol. Rev. 108:653–73 [Google Scholar]
  50. Rath-Wilson K, Guitton D. 2015. Refuting the hypothesis that a unilateral human parietal lesion abolishes saccade corollary discharge. Brain 138:3760–75 [Google Scholar]
  51. Robinson DA. 1970. Oculomotor unit behavior in the monkey. J. Neurophysiol. 33:393–404 [Google Scholar]
  52. Robinson DL, Wurtz RH. 1976. Use of an extraretinal signal by monkey superior colliculus neurons to distinguish real from self-induced stimulus movements. J. Neurophysiol. 39:852–70 [Google Scholar]
  53. Rolfs M, Jonikaitis D, Deubel H, Cavanagh P. 2011. Predictive remapping of attention across eye movements. Nat. Neurosci. 14:252–56 [Google Scholar]
  54. Roll R, Velay JL, Roll JP. 1991. Eye and neck proprioceptive messages contribute to the spatial coding of retinal input in visually oriented activities. Exp. Brain Res. 85:423–31 [Google Scholar]
  55. Ross J, Morrone MC, Burr DC. 1997. Compression of visual space before saccades. Nature 386:598–601 [Google Scholar]
  56. Salinas E, Abbott L. 1997. Invariant visual responses from attentional gain fields. J. Neurophysiol. 77:3267–72 [Google Scholar]
  57. Sherrington CS. 1918. Observations on the sensual role of the proprioceptive nerve-supply of the extrinsic ocular muscles. Brain 41:332–43 [Google Scholar]
  58. Skavenski AA. 1972. Inflow as a source of extraretinal eye position information. Vis. Res. 12:221–29 [Google Scholar]
  59. Sommer MA, Wurtz RH. 2002. A pathway in the primate brain for the internal monitoring of movements. Science 296:1480–82 [Google Scholar]
  60. Sommer MA, Wurtz RH. 2006. Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444:374–77 [Google Scholar]
  61. Sperry RW. 1950. Neural basis of the spontaneous optokinetic response produced by visual inversion. J. Comp. Physiol. Psychol. 43:482–89 [Google Scholar]
  62. Steenrod SC, Phillips MH, Goldberg ME. 2013. The lateral intraparietal area codes the location of saccade targets and not the dimension of the saccades that will be made to acquire them. J. Neurophysiol. 109:2596–605 [Google Scholar]
  63. Steinbach MJ, Smith DR. 1981. Spatial localization after strabismus surgery: evidence for inflow. Science 213:1407–9 [Google Scholar]
  64. Tolias AS, Moore T, Smirnakis SM, Tehovnik EJ, Siapas AG, Schiller PH. 2001. Eye movements modulate visual receptive fields of V4 neurons. Neuron 29:757–67 [Google Scholar]
  65. Tozer FM, Sherrington CS. 1910. Receptors and afferents of the third, fourth, and sixth cranial nerves. Proc. R. Soc. B 82:450–57 [Google Scholar]
  66. Umeno MM, Goldberg ME. 1997. Spatial processing in the monkey frontal eye field. I. Predictive visual responses. J. Neurophysiol. 78:1373–83 [Google Scholar]
  67. Umeno MM, Goldberg ME. 2001. Spatial processing in the monkey frontal eye field. II. Memory responses. J. Neurophysiol. 86:2344–52 [Google Scholar]
  68. von Helmholtz H. 1928. Handbook of Physiological Optics, transl. J.P.C. Southall 242–81 New York: Opt. Soc. Am, 3rd ed..
  69. von Holst E, Mittelstaedt H. 1950. Das Reafferenzprinzip. Wechselwirkungen zwischen Zentralnervensystem und Peripherie. Naturwissenschaften 37:464–76 [Google Scholar]
  70. Walker MF, Fitzgibbon EJ, Goldberg ME. 1995. Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements. J. Neurophysiol. 73:1988–2003 [Google Scholar]
  71. Wang X, Fung CC, Guan S, Wu S, Goldberg ME, Zhang M. 2016. Perisaccadic receptive field expansion in the lateral intraparietal area. Neuron 90:400–9 [Google Scholar]
  72. Wang X, Zhang M, Cohen IS, Goldberg ME. 2007. The proprioceptive representation of eye position in monkey primary somatosensory cortex. Nat. Neurosci. 10:640–46 [Google Scholar]
  73. Wurtz RH. 1969. Comparison of effects of eye movements and stimulus movements on striate cortex neurons of the monkey. J. Neurophysiol. 32:987–94 [Google Scholar]
  74. Xu BY, Karachi C, Goldberg ME. 2012. The postsaccadic unreliability of gain fields renders it unlikely that the motor system can use them to calculate target position in space. Neuron 76:1201–9 [Google Scholar]
  75. Young L, Stark L. 1963. A discrete model for eye tracking movements. IEEE Trans. Mil. Electron. MIL-7:113–15 [Google Scholar]
  76. Zimmermann E, Morrone MC, Fink GR, Burr D. 2013. Spatiotopic neural representations develop slowly across saccades. Curr. Biol. 23:R193–94 [Google Scholar]
  77. Zimmermann L, Morado-Díaz CJ, Davis-López de Carrizosa MAA, de la Cruz RR, May PJ. et al. 2013. Axons giving rise to the palisade endings of feline extraocular muscles display motor features. J. Neurosci. 33:2784–93 [Google Scholar]
  78. Zipser D, Andersen RA. 1988. A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331:679–84 [Google Scholar]
  79. Zirnsak M, Gerhards RG, Kiani R, Lappe M, Hamker FH. 2011. Anticipatory saccade target processing and the presaccadic transfer of visual features. J. Neurosci. 31:17887–91 [Google Scholar]
  80. Zirnsak M, Steinmetz NA, Noudoost B, Xu KZ, Moore T. 2014. Visual space is compressed in prefrontal cortex before eye movements. Nature 507:504–7 [Google Scholar]
  81. Zivotofsky AZ, Goldberg ME, Powell KD. 2005. Rhesus monkeys behave as if they perceive the Duncker Illusion. J. Cogn. Neurosci. 17:1011–17 [Google Scholar]
  82. Zivotofsky AZ, Rottach KG, Averbuch-Heller L, Kori AA, Thomas CW. et al. 1996. Saccades to remembered targets: the effects of smooth pursuit and illusory stimulus motion. J. Neurophysiol. 76:3617–32 [Google Scholar]
/content/journals/10.1146/annurev-vision-082114-035407
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Corollary Discharge and Oculomotor Proprioception: Cortical Mechanisms for Spatially Accurate Vision
Annual Review of Vision Science 2, 61 (2016); https://doi.org/10.1146/annurev-vision-082114-035407
/content/journals/10.1146/annurev-vision-082114-035407
/content/journals/10.1146/annurev-vision-082114-035407
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