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

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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.

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Abbreviations

VOR:

Vestibular-ocular reflex

OKR:

Optokinetic reflex

References

  • Aho AC (1997) The visual acuity of the frog (Rana pipiens). J Comp Physiol A 180:19–24

    Article  CAS  PubMed  Google Scholar 

  • Barlow HB, Blakemore C, Pettigrew JD (1967) The neural mechanism of binocular depth discrimination. J Physiol 193:327–342

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Becker W (1991) Saccades. In: Carpenter RHS (ed) Eye movements. Vision and visual dysfunction, vol 8. Macmillan, Basingstoke, pp 95–137

  • Carpenter RHS (1988) Movements of the eyes, 2nd edn. Pion, London

    Google Scholar 

  • Carpenter RHS (ed) (1991) Eye movements. Vision and visual dysfunction, vol 8. Macmillan, Basingstoke

  • Collett TS (1977) Stereopsis in toads. Nature 267:349–351

    Article  CAS  PubMed  Google Scholar 

  • Collewijn H (1977) Eye- and head movements in freely moving rabbits. J Physiol 266:471–498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Collewijn H, Tamminga EP (1984) Human smooth pursuit and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol 351:217–250

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Collin SP (2008) A database of retinal topography maps. Clin Exp Optom 1(1):85–95. http://www.retinalmaps.com.au

  • Collin SP, Pettigrew JD (1988) Retinal topography in reef teleosts. I. Some species with well-developed areae but poorly-developed streaks. Brain Behav Evol 31:269–282

    Article  CAS  PubMed  Google Scholar 

  • 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 24:184–192

    Article  Google Scholar 

  • Collin SP, Davies WL, Hart NS, Hunt DM (2009) The evolution of early vertebrate photoreceptors. Phil Trans R Soc B 364:2925–2940

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dawkins MS (2002) What are birds looking at? Head movements and eye use in chickens. Anim Behav 63:991–998

    Article  Google Scholar 

  • Dieringer N, Precht W (1982) Compensatory head and eye movements in the frog and their contribution to gaze stabilization. Exp Brain Res 47:394–406

    CAS  PubMed  Google Scholar 

  • Dieringer N, Cochran SL, Precht W (1983) Differences in the central organization of gaze stabilizing reflexes between frog and turtle. J Comp Physiol 153:495–508

    Article  Google Scholar 

  • Dolan T, Fernández-Juricic E (2010) Retinal ganglion cell topography in five species of ground-foraging birds. Brain Behav Evol 75:111–121

    Article  PubMed Central  PubMed  Google Scholar 

  • Easter SS Jr (1971) Spontaneous eye movements in restrained goldfish. Vision Res 11:333–342

    Article  PubMed  Google Scholar 

  • Easter SS Jr (1972) Pursuit eye movements in goldfish (Carassius auratus). Vision Res 12:673–688

    Article  PubMed  Google Scholar 

  • Easter SS, Johns PR, Heckenlively D (1974) Horizontal compensatory eye movements in goldfish (Carassius auratus). I. The normal animal. J Comp Physiol 92:23–35

    Article  Google Scholar 

  • 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 1164:353–366

    Article  PubMed  Google Scholar 

  • Evinger C, Fuchs AF (1978) Saccadic, smooth pursuit and optokinetic eye movements of the trained cat. J Physiol 285:209–229

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fernández-Juricic E (2012) Sensory basis of vigilance in birds: synthesis and future prospects. Behav Process 89:143–152

    Article  Google Scholar 

  • 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 196:879–888

    Article  Google Scholar 

  • 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 77:147–158

    Article  PubMed  Google Scholar 

  • Friedburg C, Allen CP, Mason PJ, Lamb TD (2004) Contribution of cone photoreceptors and post-receptoral mechanisms to the human photopic electroretinogram. J Physiol 556:819–843

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fritsches KA, Marshall NJ (1999) A new category of eye movements in a small fish. Curr Biol 9:R272–R273

    Article  CAS  PubMed  Google Scholar 

  • Fritsches KA, Marshall NJ (2002) Independent and conjugate eye movements during optokinesis in teleost fish. J Exp Biol 205:1241–1252

    PubMed  Google Scholar 

  • 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 294:491–506

    Article  CAS  PubMed  Google Scholar 

  • Frost BJ (1978) The optokinetic basis of head-bobbing in pigeons. J Exp Biol 74:187–195

    Google Scholar 

  • Gaffney MF, Hodos W (2003) The visual acuity and refractive state of the American kestrel. Vision Res 43:2053–2059

    Article  PubMed  Google Scholar 

  • Gaillard F (1985) Binocularly driven neurons in the rostral part of the frog optic tectum. J Comp Physiol A 157:47–55

    Article  CAS  PubMed  Google Scholar 

  • Gioanni H (1988a) Stabilizing gaze reflexes in the pigeon (Columba livia). I. Horizontal and vertical optokinetic (OKN) and head (OCR) reflexes. Exp Brain Res 69:567–582

    Article  CAS  PubMed  Google Scholar 

  • 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 69:583–593

    Article  CAS  PubMed  Google Scholar 

  • Gioanni H, Bennis M, Sansonetti A (1993) Visual and vestibular reflexes that stabilize gaze in the chameleon. Vis Neurosci 10:947–956

    Article  CAS  PubMed  Google Scholar 

  • Graf W, Gilland E, McFarlane M, Knott L, Baker R (2002) Central pathways mediating oculomotor reflexes in an elasmobranch, Scyliorhinus canicula. Biol Bull 203:236–238

    Article  PubMed  Google Scholar 

  • Guitton D (1992) Control of eye-head coordination during orienting gaze shifts. Trends Neurosci 15:174–179

    Article  CAS  PubMed  Google Scholar 

  • 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 58:427–459

    CAS  PubMed  Google Scholar 

  • Guitton D, Douglas RM, Volle M (1984) Eye-head coordination in cats. J Neurophysiol 52:1030–1050

    CAS  PubMed  Google Scholar 

  • Gungi M, Fujita M, Higuchi H (2013) Function of head-bobbing behaviour in diving little grebes. J Comp Physiol A 199:703–709

    Article  Google Scholar 

  • Haque A, Dickman JD (2005) Vestibular gaze stabilization: different behavioural strategies for arboreal and terrestrial avians. J Neurophysiol 93:1165–1173

    Article  PubMed  Google Scholar 

  • Harkness L (1977) Chameleons use accommodation cues to judge distance. Nature 267:346–349

    Article  CAS  PubMed  Google Scholar 

  • Harris AJ (1965) Eye movements in the dogfish Squalus Acanthias L. J Exp Biol 43:107–130

    Article  CAS  PubMed  Google Scholar 

  • Heath JE, Northcutt RG, Barber RP (1969) Rotational optokinesis in reptiles and its bearing on pupillary shape. Z Vergl Physiologie 62:75–85

    Article  Google Scholar 

  • Hughes A (1971) Topographical relationships between the anatomy and physiology of the rabbit visual system. Doc Ophthalmol 30:33–159

    Article  CAS  PubMed  Google Scholar 

  • 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 615–756

    Google Scholar 

  • Jacobson SG, Franklin KBJ, McDonald WI (1976) Visual acuity in the cat. Vision Res 16:1141–1143

    Article  CAS  PubMed  Google Scholar 

  • Kane SA, Zamani M (2014) Falcons pursue prey using visual motion cues: new perspectives from animal-borne cameras. J Exp Biol 217:225–234

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 71–92

  • Lamb TD, Collin SP, Pugh EN Jr (2007) Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat Rev Neurosci 8:960–975

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Land MF (1999a) The sandlance breaks all the rules. Curr Biol 9:R286–R288

    Article  CAS  PubMed  Google Scholar 

  • Land MF (1999b) The roles of head movements in the search and capture strategy of a tern (Aves, Laridae). J Comp Physiol A 184:265–272

    Article  Google Scholar 

  • Land MF (1999c) Motion and vision: why animals move their eyes. J Comp Physiol A 185:341–352

    Article  CAS  PubMed  Google Scholar 

  • Land MF, Nilsson D-E (2012) Animal eyes, 2nd edn. Oxford University Press, Oxford

    Book  Google Scholar 

  • Land MF, Tatler BW (2009) Looking and acting: vision and eye movements in natural behaviour. Oxford University Press, Oxford

    Book  Google Scholar 

  • Land MF, Mennie N, Rusted J (1999) The roles of vision and eye movements in the control of activities of daily living. Perception 28:1311–1328

    Article  CAS  PubMed  Google Scholar 

  • Lettvin JY, Maturana HR, McCulloch WS, Pitts WH (1959) What the frog’s eye tells the frog’s brain. Proc Inst Radio Eng 47:1940–1951

    Google Scholar 

  • Lisney TJ, Collin SP (2008) Retinal ganglion cell distribution and resolving power in elasmobranchs. Brain Behav Evol 72:59–77

    Article  PubMed  Google Scholar 

  • 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 199:385–402

    Article  Google Scholar 

  • Liversedge SP, Gilchrist ID, Everling S (2011) The Oxford handbook of eye movements. Oxford University Press, Oxford

    Book  Google Scholar 

  • 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 131:179–189

    Article  Google Scholar 

  • Lock A, Collett T (1980) The 3 dimensional world of a toad. Proc R Soc B 206:481–487

    Article  Google Scholar 

  • Lowenstein O, Osborne MP, Thornhill RA (1968) The anatomy and ultrastructure of the lamprey (Lampetra fluviatilis L.). Proc R Soc Lond B 170:113–134

    Article  CAS  PubMed  Google Scholar 

  • Martin GR (2007) Visual fields and their functions in birds. J Ornithol 148(suppl 2):S546–S562

    Google Scholar 

  • Martin GR (2009) What is binocular vision for? A bird’s eye view. J Vis 9(11):14, 1–19

  • Martinez-Conde S, Macknik SL (2008) Fixational eye movements across vertebrates: comparative dynamics, physiology, and perception. J Vis 8(14):28, 1–16

  • Masseck OA, Hoffmann K-P (2009) Comparative neurobiology of the optokinetic reflex. Ann N Y Acad Sci 1164:430–439

    Article  PubMed  Google Scholar 

  • Mather G (2009) Foundations of sensation and perception, 2nd edn, Chapter 10. Psychology Press, Hove

    Google Scholar 

  • McComb DM, Tricas TC, Kajiura SM (2009) Enhanced visual fields in hammerhead sharks. J Exp Biol 212:4010–4018

    Article  CAS  PubMed  Google Scholar 

  • de Brooke ML, Hanley S, Laughlin SB (1999) The scaling of eye size with body mass in birds. Proc R Soc Lond B 266:405–412

    Article  Google Scholar 

  • Mitchell DE, Kaye M, Timney B (1979) Assessment of depth perception in cats. Perception 8:389–396

    Article  CAS  PubMed  Google Scholar 

  • 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 199:263–277

    Article  Google Scholar 

  • 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 893–906

    Google Scholar 

  • 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 25–46

    Google Scholar 

  • Necker R (2007) Head-bobbing of walking birds. J Comp Physiol A 193:1177–1183

    Article  Google Scholar 

  • Neumeyer C (2003) Wavelength dependence of visual acuity in goldfish. J Comp Physiol A 189:811–821

    Article  CAS  Google Scholar 

  • Ott M (2001) Chameleons have independent eye movements but synchronise both eyes during saccadic prey tracking. Exp Brain Res 139:173–179

    Article  CAS  PubMed  Google Scholar 

  • Ott M, Schaeffel F (1995) A negatively powered lens in the chameleon. Nature 373:692–694

    Article  CAS  PubMed  Google Scholar 

  • Ott M, Schaeffel F, Kirmse W (1998) Binocular vision and accommodation in prey-catching chameleons. J Comp Physiol A 182:319–330

    Article  Google Scholar 

  • Pettigrew JD, Collin SP (1995) Terrestrial optics in an aquatic eye: the sandlance, Limnichthyes fasciatus (Creediidae, Teleostei). J Comp Physiol A 177:397–408

    Article  Google Scholar 

  • 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 9:424–431

    Article  Google Scholar 

  • Pettigrew JD, Collin SP, Fritsches K (2000) Prey capture and accommodation in the sandlance, Limnichthyes fasciatus (Creediidae; Teleostei). J Comp Physiol A 186:247–260

    Article  CAS  PubMed  Google Scholar 

  • 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 138–156

    Google Scholar 

  • Prusky GT, West PW, Douglas RM (2000) Behavioral assessment of visual acuity in mice and rats. Vision Res 40:2201–2209

    Article  CAS  PubMed  Google Scholar 

  • Reymond L (1985) Spatial acuity of the eagle Aquila audax: a behavioural, optical and anatomical investigation. Vision Res 25:1477–1491

    Article  CAS  PubMed  Google Scholar 

  • Rovainen CM (1976) Vestibulo-ocular reflexes in the adult sea lamprey. J Comp Physiol 112:159–164

    Article  Google Scholar 

  • Saitoh K, Ménard A, Grillner S (2007) Tectal control of locomotion, steering and eye movements in lamprey. J Neurophysiol 97:3093–3208

    Article  PubMed  Google Scholar 

  • Schuster S (2007) Archerfish. Curr Biol 17:R494–R495

    Article  CAS  PubMed  Google Scholar 

  • Schuster S, Wöhl S, Griebsch M, Klostermeier I (2006) Animal cognition: how archer fish learn to down rapidly moving targets. Curr Biol 16:378–383

    Article  CAS  PubMed  Google Scholar 

  • Simpson JI, Graf W (1981) Eye-muscle geometry and compensatory eye movements in lateral-eyed and frontal-eyed animals. Ann N Y Acad Sci 374:20–30

    Article  CAS  PubMed  Google Scholar 

  • 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 14:1565–1568

    Article  CAS  PubMed  Google Scholar 

  • Stryker M, Blakemore C (1972) Saccadic and disjunctive eye movements in cats. Vision Res 12:2005–2013

    Article  CAS  PubMed  Google Scholar 

  • 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 277:2607–2615

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 83:1–8

    Article  CAS  PubMed  Google Scholar 

  • Tommasi L, Andrew RJ (2002) The use of viewing posture to control visual processing by lateralised mechanisms. J Exp Biol 205:1451–1457

    PubMed  Google Scholar 

  • Tucker VA, Tucker AE, Akers K, Enderson JH (2000) Curved flight paths and sideways vision in peregrine falcons (Falco peregrinus). J Exp Biol 203:3755–3763

    CAS  PubMed  Google Scholar 

  • 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 198:675–681

    Google Scholar 

  • van der Willigen RF, Frost BJ, Wagner H (1998) Stereoscopic depth perception in the owl. NeuroReport 9:1233–1237

    Article  PubMed  Google Scholar 

  • Voss J, Bischof H-J (2009) Eye movements of laterally eyed birds are not independent. J Exp Biol 212:1568–1575

    Article  PubMed  Google Scholar 

  • 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 498:65–69

    Article  CAS  PubMed  Google Scholar 

  • 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 245–263

  • Wallman J, Pettigrew JD (1985) Conjugate and disjunctive saccades in two avian species with contrasting oculomotor strategies. J Neurosci 5:317–329

    CAS  PubMed  Google Scholar 

  • Walls GL (1942) The vertebrate eye and its adaptive radiation. The Cranbrook Institute, Bloomington Hills, MI. Reprint (1967). Hafner, New York

  • Walls GL (1962) The evolutionary history of eye movements. Vision Res 2:69–80

    Article  Google Scholar 

  • Werner JS, Chalupa LM (eds) (2014) The new visual neurosciences. MIT Press, Cambridge

    Google Scholar 

  • Yorzinski JL, Patricelli GL, Babcock JS, Pearson JM, Platt ML (2013) Through their eyes: selective attention in peahens during courtship. J Exp Biol 216:3035–3046

    Article  PubMed Central  PubMed  Google Scholar 

  • Young GC (2007) Number and arrangement of extraocular muscles in primitive gnathostomes: evidence from extinct placoderm fishes. Biol Lett 4:110–114

    Article  PubMed Central  Google Scholar 

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Acknowledgments

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

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    Michael F. Land

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Land, M.F. Eye movements of vertebrates and their relation to eye form and function. J Comp Physiol A 201, 195–214 (2015). https://doi.org/10.1007/s00359-014-0964-5

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