No retraction, correction or concern found when last checked on Nov 4, 2026.
Two Distinct Types of Eye-Head Coupling in Freely Moving Mice
Arne F. Meyer, John O’Keefe, Jasper Poort
Current Biology · 2020 · CC BY
Abstract
Animals actively interact with their environment to gather sensory information. There is conflicting evidence about how mice use vision to sample their environment. During head restraint, mice make rapid eye movements coupled between the eyes, similar to conjugate saccadic eye movements in humans. However, when mice are free to move their heads, eye movements are more complex and often non-conjugate, with the eyes moving in opposite directions. We combined head and eye tracking in freely moving mice and found both observations are explained by two eye-head coupling types, associated with vestibular mechanisms. The first type comprised non-conjugate eye movements, which compensate for head tilt changes to maintain a similar visual field relative to the horizontal ground plane. The second type of eye movements was conjugate and coupled to head yaw rotation to produce a "saccade and fixate" gaze pattern. During head-initiated saccades, the eyes moved together in the head direction but during subsequent fixation moved in the opposite direction to the head to compensate for head rotation. This saccade and fixate pattern is similar to humans who use eye movements (with or without head movement) to rapidly shift gaze but in mice relies on combined head and eye movements. Both couplings were maintained during social interactions and visually guided object tracking. Even in head-restrained mice, eye movements were invariably associated with attempted head motion. Our results reveal that mice combine head and eye movements to sample their environment and highlight similarities and differences between eye movements in mice and humans.
References 79
- 1.
Kleinfeld D., Ahissar E., Diamond M.E. Active sensation: insights from the rodent vibrissa sensorimotor system. Curr. Opin. Neurobiol. 2006;16:435-444.
Not in our library10.1016/j.conb.2006.06.009
- 2.
Gottlieb J., Oudeyer P.Y. Towards a neuroscience of active sampling and curiosity. Nat. Rev. Neurosci. 2018;19:758-770.
Not in our library10.1038/s41583-018-0078-0
- 3.
Sağlam M., Lehnen N., Glasauer S. Optimal control of natural eye-head movements minimizes the impact of noise. J. Neurosci. 2011;31:16185-16193.
Not in our library10.1523/jneurosci.3721-11.2011
- 4.
Land M., Mennie N., Rusted J. The roles of vision and eye movements in the control of activities of daily living. Perception. 1999;28:1311-1328.
Not in our library10.1068/p2935
- 5.
Hayhoe M. Vision using routines: a functional account of vision. Vis. Cogn. 2000;7:43-64.
Not in our library
- 6.
Hayhoe M., Ballard D. Modeling task control of eye movements. Curr. Biol. 2014;24:R622-R628.
Not in our library10.1016/j.cub.2014.05.020
- 7.
Land M.F. Eye movements of vertebrates and their relation to eye form and function. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 2015;201:195-214.
Not in our library10.1007/s00359-014-0964-5
- 8.
Seabrook T.A., Burbridge T.J., Crair M.C., Huberman A.D. Architecture, function, and assembly of the mouse visual system. Annu. Rev. Neurosci. 2017;40:499-538.
Not in our library10.1146/annurev-neuro-071714-033842
- 9.
Yilmaz M., Meister M. Rapid innate defensive responses of mice to looming visual stimuli. Curr. Biol. 2013;23:2011-2015.
Not in our library10.1016/j.cub.2013.08.015
- 10.
Hoy J.L., Yavorska I., Wehr M., Niell C.M. Vision drives accurate approach behavior during prey capture in laboratory mice. Curr. Biol. 2016;26:3046-3052.
Not in our library10.1016/j.cub.2016.09.009
- 11.
Huberman A.D., Niell C.M. What can mice tell us about how vision works? Trends Neurosci. 2011;34:464-473.
Not in our library10.1016/j.tins.2011.07.002
- 12.
Carandini M., Churchland A.K. Probing perceptual decisions in rodents. Nat. Neurosci. 2013;16:824-831.
Not in our library10.1038/nn.3410
- 13.
Horner A.E., Heath C.J., Hvoslef-Eide M., Kent B.A., Kim C.H., Nilsson S.R.O., Alsiö J., Oomen C.A., Holmes A., Saksida L.M., Bussey T.J. The touchscreen operant platform for testing learning and memory in rats and mice. Nat. Protoc. 2013;8:1961-1984.
Not in our library10.1038/nprot.2013.122
- 14.
Wagor E., Mangini N.J., Pearlman A.L. Retinotopic organization of striate and extrastriate visual cortex in the mouse. J. Comp. Neurol. 1980;193:187-202.
Not in our library10.1002/cne.901930113
- 15.
Dräger U.C. Observations on monocular deprivation in mice. J. Neurophysiol. 1978;41:28-42.
Not in our library10.1152/jn.1978.41.1.28
- 16.
Hübener M. Mouse visual cortex. Curr. Opin. Neurobiol. 2003;13:413-420.
Not in our library10.1016/s0959-4388(03)00102-8
- 17.
Samonds J.M., Geisler W.S., Priebe N.J. Natural image and receptive field statistics predict saccade sizes. Nat. Neurosci. 2018;21:1591-1599.
Not in our library10.1038/s41593-018-0255-5
- 18.
Dräger U.C., Olsen J.F. Ganglion cell distribution in the retina of the mouse. Invest. Ophthalmol. Vis. Sci. 1981;20:285-293.
Not in our library
- 19.
Jeon C.J., Strettoi E., Masland R.H. The major cell populations of the mouse retina. J. Neurosci. 1998;18:8936-8946.
Not in our library10.1523/jneurosci.18-21-08936.1998
- 20.
Sakatani T., Isa T. Quantitative analysis of spontaneous saccade-like rapid eye movements in C57BL/6 mice. Neurosci. Res. 2007;58:324-331.
Not in our library10.1016/j.neures.2007.04.003
- 21.
Wang L., Liu M., Segraves M.A., Cang J. Visual experience is required for the development of eye movement maps in the mouse superior colliculus. J. Neurosci. 2015;35:12281-12286.
Not in our library10.1523/jneurosci.0117-15.2015
- 22.
- 23.
- 24.
Payne H.L., Raymond J.L. Magnetic eye tracking in mice. eLife. 2017;6:e29222.
Not in our library10.7554/elife.29222
- 25.
Wallace D.J., Greenberg D.S., Sawinski J., Rulla S., Notaro G., Kerr J.N.D. Rats maintain an overhead binocular field at the expense of constant fusion. Nature. 2013;498:65-69.
Not in our library10.1038/nature12153
- 26.
Oommen B.S., Stahl J.S. Eye orientation during static tilts and its relationship to spontaneous head pitch in the laboratory mouse. Brain Res. 2008;1193:57-66.
Not in our library10.1016/j.brainres.2007.11.053
- 27.
Maruta J., Simpson J.I., Raphan T., Cohen B. Orienting otolith-ocular reflexes in the rabbit during static and dynamic tilts and off-vertical axis rotation. Vision Res. 2001;41:3255-3270.
Not in our library10.1016/s0042-6989(01)00091-8
- 28.
Khan S.I., Della Santina C.C., Migliaccio A.A. Angular vestibuloocular reflex responses in Otop1 mice. I. Otolith sensor input is essential for gravity context-specific adaptation. J. Neurophysiol. 2019;121:2291-2299.
Not in our library10.1152/jn.00811.2018
- 29.
Meister M., Cox D. Rats maintain a binocular field centered on the horizon. F1000Res. 2013;2:176.
Not in our library10.12688/f1000research.2-176.v1
- 30.
Land M. Eye movements in man and other animals. Vision Res. 2019;162:1-7.
Not in our library10.1016/j.visres.2019.06.004
- 31.
van Alphen A.M., Stahl J.S., De Zeeuw C.I. The dynamic characteristics of the mouse horizontal vestibulo-ocular and optokinetic response. Brain Res. 2001;890:296-305.
Not in our library10.1016/s0006-8993(00)03180-2
- 32.
Migliaccio A.A., Meierhofer R., Della Santina C.C. Characterization of the 3D angular vestibulo-ocular reflex in C57BL6 mice. Exp. Brain Res. 2011;210:489-501.
Not in our library10.1007/s00221-010-2521-y
- 33.
Andreescu C.E., De Ruiter M.M., De Zeeuw C.I., De Jeu M.T.G. Otolith deprivation induces optokinetic compensation. J. Neurophysiol. 2005;94:3487-3496.
Not in our library10.1152/jn.00147.2005
- 34.
Guitton D., Volle M. Gaze control in humans: eye-head coordination during orienting movements to targets within and beyond the oculomotor range. J. Neurophysiol. 1987;58:427-459.
Not in our library10.1152/jn.1987.58.3.427
- 35.
Guitton D., Douglas R.M., Volle M. Eye-head coordination in cats. J. Neurophysiol. 1984;52:1030-1050.
Not in our library10.1152/jn.1984.52.6.1030
- 36.
Guitton D. Control of eye-head coordination during orienting gaze shifts. Trends Neurosci. 1992;15:174-179.
Not in our library10.1016/0166-2236(92)90169-9
- 37.
Collewijn H. Eye- and head movements in freely moving rabbits. J. Physiol. 1977;266:471-498.
Not in our library10.1113/jphysiol.1977.sp011778
- 38.
Collewijn H., Erkelens C.J., Steinman R.M. Binocular co-ordination of human horizontal saccadic eye movements. J. Physiol. 1988;404:157-182.
Not in our library10.1113/jphysiol.1988.sp017284
- 39.
Strasser S., Dixon A.K. Effects of visual and acoustic deprivation on agonistic behaviour of the albino mouse (M. musculus L.). Physiol. Behav. 1986;36:773-778.
Not in our library10.1016/0031-9384(86)90367-7
- 40.
Pellis S.M., McKenna M.M., Field E.F., Pellis V.C., Prusky G.T., Whishaw I.Q. Uses of vision by rats in play fighting and other close-quarter social interactions. Physiol. Behav. 1996;59:905-913.
Not in our library10.1016/0031-9384(95)02162-0
Cited by papers we hold 1
Reads
Read by people on this page
None yet.
Checked or read by AI through naulon
None yet.
A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.
Are you an author?
Is this your paper?
Claim it to add your note and be paid when agents cite it. Free.