Advertisement

Journal of Comparative Physiology A

, Volume 201, Issue 2, pp 195–214 | Cite as

Eye movements of vertebrates and their relation to eye form and function

  • Michael F. LandEmail author
Review

Abstract

The types of eye movements shown by all vertebrates originated in the earliest fishes. These consisted of compensatory movements, both vestibular and visual, to prevent image motion, and saccades to relocate gaze. All vertebrates fixate food items with their heads to enable ingestion, but from teleosts onwards some species also use eye movements to target particular objects, especially food. Eye movement use is related to the resolution distribution in the retina, with eyes that contain foveas, or areas of high ganglion cell density, being more likely to make targeting eye movements, not seen in animals with more uniform retinas. Birds, in particular, tend mainly to use head movements when shifting gaze. Many birds also make translatory head saccades (head bobbing) when walking. It is common for animals to use both eyes when locating food items ahead, but the use of binocular disparity for distance judgment is rare, and has only been demonstrated in toads, owls, cats and primates. Smooth tracking with eyes alone is probably confined to primates. The extent of synchrony and directional symmetry in the movements of the two eyes varies greatly, from complete independence in the sandlance and chameleon, to perfect coordination in primates.

Keywords

Saccade Compensatory eye movement Fixation Binocularity Resolution distribution 

Abbreviations

VOR

Vestibular-ocular reflex

OKR

Optokinetic reflex

Notes

Acknowledgments

I am grateful to Jessica Yorzinski (Cornell) for reading and commenting on the manuscript, and for useful comments by two referees.

References

  1. Aho AC (1997) The visual acuity of the frog (Rana pipiens). J Comp Physiol A 180:19–24PubMedCrossRefGoogle Scholar
  2. Barlow HB, Blakemore C, Pettigrew JD (1967) The neural mechanism of binocular depth discrimination. J Physiol 193:327–342PubMedCentralPubMedCrossRefGoogle Scholar
  3. Becker W (1991) Saccades. In: Carpenter RHS (ed) Eye movements. Vision and visual dysfunction, vol 8. Macmillan, Basingstoke, pp 95–137Google Scholar
  4. Carpenter RHS (1988) Movements of the eyes, 2nd edn. Pion, LondonGoogle Scholar
  5. Carpenter RHS (ed) (1991) Eye movements. Vision and visual dysfunction, vol 8. Macmillan, BasingstokeGoogle Scholar
  6. Collett TS (1977) Stereopsis in toads. Nature 267:349–351PubMedCrossRefGoogle Scholar
  7. Collewijn H (1977) Eye- and head movements in freely moving rabbits. J Physiol 266:471–498PubMedCentralPubMedCrossRefGoogle Scholar
  8. Collewijn H, Tamminga EP (1984) Human smooth pursuit and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol 351:217–250PubMedCentralPubMedCrossRefGoogle Scholar
  9. Collin SP (2008) A database of retinal topography maps. Clin Exp Optom 1(1):85–95. http://www.retinalmaps.com.au
  10. Collin SP, Pettigrew JD (1988) Retinal topography in reef teleosts. I. Some species with well-developed areae but poorly-developed streaks. Brain Behav Evol 31:269–282PubMedCrossRefGoogle Scholar
  11. Collin SP, Pettigrew JD (1989) Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain Behav Evol 24:184–192CrossRefGoogle Scholar
  12. Collin SP, Davies WL, Hart NS, Hunt DM (2009) The evolution of early vertebrate photoreceptors. Phil Trans R Soc B 364:2925–2940PubMedCentralPubMedCrossRefGoogle Scholar
  13. Dawkins MS (2002) What are birds looking at? Head movements and eye use in chickens. Anim Behav 63:991–998CrossRefGoogle Scholar
  14. Dieringer N, Precht W (1982) Compensatory head and eye movements in the frog and their contribution to gaze stabilization. Exp Brain Res 47:394–406PubMedGoogle Scholar
  15. Dieringer N, Cochran SL, Precht W (1983) Differences in the central organization of gaze stabilizing reflexes between frog and turtle. J Comp Physiol 153:495–508CrossRefGoogle Scholar
  16. Dolan T, Fernández-Juricic E (2010) Retinal ganglion cell topography in five species of ground-foraging birds. Brain Behav Evol 75:111–121PubMedCentralPubMedCrossRefGoogle Scholar
  17. Easter SS Jr (1971) Spontaneous eye movements in restrained goldfish. Vision Res 11:333–342PubMedCrossRefGoogle Scholar
  18. Easter SS Jr (1972) Pursuit eye movements in goldfish (Carassius auratus). Vision Res 12:673–688PubMedCrossRefGoogle Scholar
  19. Easter SS, Johns PR, Heckenlively D (1974) Horizontal compensatory eye movements in goldfish (Carassius auratus). I. The normal animal. J Comp Physiol 92:23–35CrossRefGoogle Scholar
  20. Einhäuser W, Moeller GU, Schumann F, Conradt J, Vockeroth J, Bartl K, Schneider E, König P (2009) Eye-head coordination during free exploration in human and cat. Ann N Y Acad Sci 1164:353–366PubMedCrossRefGoogle Scholar
  21. Evinger C, Fuchs AF (1978) Saccadic, smooth pursuit and optokinetic eye movements of the trained cat. J Physiol 285:209–229PubMedCentralPubMedCrossRefGoogle Scholar
  22. Fernández-Juricic E (2012) Sensory basis of vigilance in birds: synthesis and future prospects. Behav Process 89:143–152CrossRefGoogle Scholar
  23. Fernández-Juricic E, O’Rourke C, Pitlik T (2010) Visual coverage and scanning behaviour in two corvid species: American crow and Western scrub jay. J Comp Physiol A 196:879–888CrossRefGoogle Scholar
  24. Fernández-Juricic E, Moore BA, Doppler M, Freeman J, Blackwell BF, Lima SL, DeVault TL (2011) Testing the terrain hypothesis: Canada geese see their world laterally and obliquely. Brain Behav Evol 77:147–158PubMedCrossRefGoogle Scholar
  25. Friedburg C, Allen CP, Mason PJ, Lamb TD (2004) Contribution of cone photoreceptors and post-receptoral mechanisms to the human photopic electroretinogram. J Physiol 556:819–843PubMedCentralPubMedCrossRefGoogle Scholar
  26. Fritsches KA, Marshall NJ (1999) A new category of eye movements in a small fish. Curr Biol 9:R272–R273PubMedCrossRefGoogle Scholar
  27. Fritsches KA, Marshall NJ (2002) Independent and conjugate eye movements during optokinesis in teleost fish. J Exp Biol 205:1241–1252PubMedGoogle Scholar
  28. Fritzsch B, Sonntag R, Dubuc R, Ohta Y, Grillner S (1990) Organization of the six motor nuclei innervating the ocular muscles in lamprey. J Comp Neurol 294:491–506PubMedCrossRefGoogle Scholar
  29. Frost BJ (1978) The optokinetic basis of head-bobbing in pigeons. J Exp Biol 74:187–195Google Scholar
  30. Gaffney MF, Hodos W (2003) The visual acuity and refractive state of the American kestrel. Vision Res 43:2053–2059PubMedCrossRefGoogle Scholar
  31. Gaillard F (1985) Binocularly driven neurons in the rostral part of the frog optic tectum. J Comp Physiol A 157:47–55PubMedCrossRefGoogle Scholar
  32. Gioanni H (1988a) Stabilizing gaze reflexes in the pigeon (Columba livia). I. Horizontal and vertical optokinetic (OKN) and head (OCR) reflexes. Exp Brain Res 69:567–582PubMedCrossRefGoogle Scholar
  33. Gioanni H (1988b) Stabilizing gaze reflexes in the pigeon (Columba livia). II. Vestibulo-ocular (VOR) and vestibulo-colic (closed-loop VCR) reflexes. Exp Brain Res 69:583–593PubMedCrossRefGoogle Scholar
  34. Gioanni H, Bennis M, Sansonetti A (1993) Visual and vestibular reflexes that stabilize gaze in the chameleon. Vis Neurosci 10:947–956PubMedCrossRefGoogle Scholar
  35. Graf W, Gilland E, McFarlane M, Knott L, Baker R (2002) Central pathways mediating oculomotor reflexes in an elasmobranch, Scyliorhinus canicula. Biol Bull 203:236–238PubMedCrossRefGoogle Scholar
  36. Guitton D (1992) Control of eye-head coordination during orienting gaze shifts. Trends Neurosci 15:174–179PubMedCrossRefGoogle Scholar
  37. Guitton D, Volle M (1987) Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J Neurophysiol 58:427–459PubMedGoogle Scholar
  38. Guitton D, Douglas RM, Volle M (1984) Eye-head coordination in cats. J Neurophysiol 52:1030–1050PubMedGoogle Scholar
  39. Gungi M, Fujita M, Higuchi H (2013) Function of head-bobbing behaviour in diving little grebes. J Comp Physiol A 199:703–709CrossRefGoogle Scholar
  40. Haque A, Dickman JD (2005) Vestibular gaze stabilization: different behavioural strategies for arboreal and terrestrial avians. J Neurophysiol 93:1165–1173PubMedCrossRefGoogle Scholar
  41. Harkness L (1977) Chameleons use accommodation cues to judge distance. Nature 267:346–349PubMedCrossRefGoogle Scholar
  42. Harris AJ (1965) Eye movements in the dogfish Squalus Acanthias L. J Exp Biol 43:107–130PubMedCrossRefGoogle Scholar
  43. Heath JE, Northcutt RG, Barber RP (1969) Rotational optokinesis in reptiles and its bearing on pupillary shape. Z Vergl Physiologie 62:75–85CrossRefGoogle Scholar
  44. Hughes A (1971) Topographical relationships between the anatomy and physiology of the rabbit visual system. Doc Ophthalmol 30:33–159PubMedCrossRefGoogle Scholar
  45. Hughes A (1977) The topography of vision in mammals of contrasting life style: comparative optics and retinal organization. In: Crescitelli F (ed) Handbook of sensory physiology VII/5. The visual system in vertebrates. Springer, Berlin, pp 615–756Google Scholar
  46. Jacobson SG, Franklin KBJ, McDonald WI (1976) Visual acuity in the cat. Vision Res 16:1141–1143PubMedCrossRefGoogle Scholar
  47. Kane SA, Zamani M (2014) Falcons pursue prey using visual motion cues: new perspectives from animal-borne cameras. J Exp Biol 217:225–234PubMedCentralPubMedCrossRefGoogle Scholar
  48. Kowler E (1991) The stability of gaze and its implications for vision. In: Carpenter RHS (ed) Eye movements. Vision and visual dysfunction, vol 8. Macmillan, Basingstoke, pp 71–92Google Scholar
  49. Lamb TD, Collin SP, Pugh EN Jr (2007) Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci 8:960–975PubMedCentralPubMedCrossRefGoogle Scholar
  50. Land MF (1999a) The sandlance breaks all the rules. Curr Biol 9:R286–R288PubMedCrossRefGoogle Scholar
  51. Land MF (1999b) The roles of head movements in the search and capture strategy of a tern (Aves, Laridae). J Comp Physiol A 184:265–272CrossRefGoogle Scholar
  52. Land MF (1999c) Motion and vision: why animals move their eyes. J Comp Physiol A 185:341–352PubMedCrossRefGoogle Scholar
  53. Land MF, Nilsson D-E (2012) Animal eyes, 2nd edn. Oxford University Press, OxfordCrossRefGoogle Scholar
  54. Land MF, Tatler BW (2009) Looking and acting: vision and eye movements in natural behaviour. Oxford University Press, OxfordCrossRefGoogle Scholar
  55. Land MF, Mennie N, Rusted J (1999) The roles of vision and eye movements in the control of activities of daily living. Perception 28:1311–1328PubMedCrossRefGoogle Scholar
  56. Lettvin JY, Maturana HR, McCulloch WS, Pitts WH (1959) What the frog’s eye tells the frog’s brain. Proc Inst Radio Eng 47:1940–1951Google Scholar
  57. Lisney TJ, Collin SP (2008) Retinal ganglion cell distribution and resolving power in elasmobranchs. Brain Behav Evol 72:59–77PubMedCrossRefGoogle Scholar
  58. Lisney TJ, Stecyk K, Kolominsky J, Schmidt BK, Corfield JR, Iwaniuk AN, Wylie DR (2013) Ecomorphology of eye shape and retinal topography in waterfowl (Aves: Anseriformes: Anatidae) with different foraging modes. J Comp Physiol A 199:385–402CrossRefGoogle Scholar
  59. Liversedge SP, Gilchrist ID, Everling S (2011) The Oxford handbook of eye movements. Oxford University Press, OxfordCrossRefGoogle Scholar
  60. Lock A, Collett T (1979) A toad’s devious approach to its prey: a study of some complex uses of depth vision. J Comp Physiol 131:179–189CrossRefGoogle Scholar
  61. Lock A, Collett T (1980) The 3 dimensional world of a toad. Proc R Soc B 206:481–487CrossRefGoogle Scholar
  62. Lowenstein O, Osborne MP, Thornhill RA (1968) The anatomy and ultrastructure of the lamprey (Lampetra fluviatilis L.). Proc R Soc Lond B 170:113–134PubMedCrossRefGoogle Scholar
  63. Martin GR (2007) Visual fields and their functions in birds. J Ornithol 148(suppl 2):S546–S562Google Scholar
  64. Martin GR (2009) What is binocular vision for? A bird’s eye view. J Vis 9(11):14, 1–19Google Scholar
  65. Martinez-Conde S, Macknik SL (2008) Fixational eye movements across vertebrates: comparative dynamics, physiology, and perception. J Vis 8(14):28, 1–16Google Scholar
  66. Masseck OA, Hoffmann K-P (2009) Comparative neurobiology of the optokinetic reflex. Ann N Y Acad Sci 1164:430–439PubMedCrossRefGoogle Scholar
  67. Mather G (2009) Foundations of sensation and perception, 2nd edn, Chapter 10. Psychology Press, HoveGoogle Scholar
  68. McComb DM, Tricas TC, Kajiura SM (2009) Enhanced visual fields in hammerhead sharks. J Exp Biol 212:4010–4018PubMedCrossRefGoogle Scholar
  69. de Brooke ML, Hanley S, Laughlin SB (1999) The scaling of eye size with body mass in birds. Proc R Soc Lond B 266:405–412CrossRefGoogle Scholar
  70. Mitchell DE, Kaye M, Timney B (1979) Assessment of depth perception in cats. Perception 8:389–396PubMedCrossRefGoogle Scholar
  71. Moore BA, Doppler M, Young JE, Fernández-Juricic E (2013) Interspecific differences in the visual system and scanning behaviour of three forest passerines that form heterospecific flocks. J Comp Physiol A 199:263–277CrossRefGoogle Scholar
  72. Mustari MJ, Ono S (2014) Neural mechanisms for smooth pursuit eye movements. In: Werner JS, Chalupa LM (eds) The new visual neurosciences. MIT Press, Cambridge, pp 893–906Google Scholar
  73. Nalbach H-O, Wolf-Oberhollenzer F, Remy M (1993) Exploring the image. In: Zeigler HP, Bischof H-J (eds) Vision, brain and behavior in birds. MIT Press, Cambridge MA, pp 25–46Google Scholar
  74. Necker R (2007) Head-bobbing of walking birds. J Comp Physiol A 193:1177–1183CrossRefGoogle Scholar
  75. Neumeyer C (2003) Wavelength dependence of visual acuity in goldfish. J Comp Physiol A 189:811–821CrossRefGoogle Scholar
  76. Ott M (2001) Chameleons have independent eye movements but synchronise both eyes during saccadic prey tracking. Exp Brain Res 139:173–179PubMedCrossRefGoogle Scholar
  77. Ott M, Schaeffel F (1995) A negatively powered lens in the chameleon. Nature 373:692–694PubMedCrossRefGoogle Scholar
  78. Ott M, Schaeffel F, Kirmse W (1998) Binocular vision and accommodation in prey-catching chameleons. J Comp Physiol A 182:319–330CrossRefGoogle Scholar
  79. Pettigrew JD, Collin SP (1995) Terrestrial optics in an aquatic eye: the sandlance, Limnichthyes fasciatus (Creediidae, Teleostei). J Comp Physiol A 177:397–408CrossRefGoogle Scholar
  80. Pettigrew JD, Collin SP, Ott M (1999) Convergence of specialised behaviour, eye movements and visual optics in the sandlance (Teleostei) and the chameleon (Reptilia). Curr Biol 9:424–431CrossRefGoogle Scholar
  81. Pettigrew JD, Collin SP, Fritsches K (2000) Prey capture and accommodation in the sandlance, Limnichthyes fasciatus (Creediidae; Teleostei). J Comp Physiol A 186:247–260PubMedCrossRefGoogle Scholar
  82. Pola J, Wyatt HJ (1991) Smooth pursuit: response characteristics, stimuli and mechanisms. In: Carpenter RHS (ed) Vision and visual dysfunction, vol 8., Eye movementsMacmillan, Basingstoke, pp 138–156Google Scholar
  83. Prusky GT, West PW, Douglas RM (2000) Behavioral assessment of visual acuity in mice and rats. Vision Res 40:2201–2209PubMedCrossRefGoogle Scholar
  84. Reymond L (1985) Spatial acuity of the eagle Aquila audax: a behavioural, optical and anatomical investigation. Vision Res 25:1477–1491PubMedCrossRefGoogle Scholar
  85. Rovainen CM (1976) Vestibulo-ocular reflexes in the adult sea lamprey. J Comp Physiol 112:159–164CrossRefGoogle Scholar
  86. Saitoh K, Ménard A, Grillner S (2007) Tectal control of locomotion, steering and eye movements in lamprey. J Neurophysiol 97:3093–3208PubMedCrossRefGoogle Scholar
  87. Schuster S (2007) Archerfish. Curr Biol 17:R494–R495PubMedCrossRefGoogle Scholar
  88. Schuster S, Wöhl S, Griebsch M, Klostermeier I (2006) Animal cognition: how archer fish learn to down rapidly moving targets. Curr Biol 16:378–383PubMedCrossRefGoogle Scholar
  89. Simpson JI, Graf W (1981) Eye-muscle geometry and compensatory eye movements in lateral-eyed and frontal-eyed animals. Ann N Y Acad Sci 374:20–30PubMedCrossRefGoogle Scholar
  90. Schuster S, Rossel S, Schmidtmann A, Jäger I, Poralla J (2004) Archer fish learn to compensate for complex optical distortions to determine the absolute size of their prey. Curr Biol 14:1565–1568PubMedCrossRefGoogle Scholar
  91. Stryker M, Blakemore C (1972) Saccadic and disjunctive eye movements in cats. Vision Res 12:2005–2013PubMedCrossRefGoogle Scholar
  92. Temple S, Hart NS, Marshall NJ, Collin SP (2010) A spitting image: specializations in archerfish eyes for vision at the interface between air and water. Proc R Soc B 277:2607–2615PubMedCentralPubMedCrossRefGoogle Scholar
  93. Temple SE, Manietta D, Collin SP (2013) A comparison of the behavioural (Landoldt C) and anatomical estimates of visual acuity in archerfish (Toxotes chatareus). Vision Res 83:1–8PubMedCrossRefGoogle Scholar
  94. Tommasi L, Andrew RJ (2002) The use of viewing posture to control visual processing by lateralised mechanisms. J Exp Biol 205:1451–1457PubMedGoogle Scholar
  95. Tucker VA, Tucker AE, Akers K, Enderson JH (2000) Curved flight paths and sideways vision in peregrine falcons (Falco peregrinus). J Exp Biol 203:3755–3763PubMedGoogle Scholar
  96. Ullén F, Deliagina TG, Orlovsky GN, Grillner S (1995) Spatial orientation in the lamprey. II. Visual influence on orientation during locomotion and in the attached state. J Exp Biol 198:675–681Google Scholar
  97. van der Willigen RF, Frost BJ, Wagner H (1998) Stereoscopic depth perception in the owl. NeuroReport 9:1233–1237PubMedCrossRefGoogle Scholar
  98. Voss J, Bischof H-J (2009) Eye movements of laterally eyed birds are not independent. J Exp Biol 212:1568–1575PubMedCrossRefGoogle Scholar
  99. Wallace DJ, Greenberg DS, Sawinski J, Rulla S, Notaro G, Kerr JND (2013) Rats maintain an overhead binocular field at the expense of constant fusion. Nature 498:65–69PubMedCrossRefGoogle Scholar
  100. Wallman J, Letelier JC (1993) Eye movements, head movements, and gaze stabilization in birds. In: Zeigler HP, Bischof HJ (eds) Vision, brain and behavior in birds. MIT Press, Cambridge, pp 245–263Google Scholar
  101. Wallman J, Pettigrew JD (1985) Conjugate and disjunctive saccades in two avian species with contrasting oculomotor strategies. J Neurosci 5:317–329PubMedGoogle Scholar
  102. Walls GL (1942) The vertebrate eye and its adaptive radiation. The Cranbrook Institute, Bloomington Hills, MI. Reprint (1967). Hafner, New YorkGoogle Scholar
  103. Walls GL (1962) The evolutionary history of eye movements. Vision Res 2:69–80CrossRefGoogle Scholar
  104. Werner JS, Chalupa LM (eds) (2014) The new visual neurosciences. MIT Press, CambridgeGoogle Scholar
  105. Yorzinski JL, Patricelli GL, Babcock JS, Pearson JM, Platt ML (2013) Through their eyes: selective attention in peahens during courtship. J Exp Biol 216:3035–3046PubMedCentralPubMedCrossRefGoogle Scholar
  106. Young GC (2007) Number and arrangement of extraocular muscles in primitive gnathostomes: evidence from extinct placoderm fishes. Biol Lett 4:110–114PubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.School of Life SciencesUniversity of SussexBrightonUK

Personalised recommendations