Two Distinct Types of Eye-Head Coupling in Freely Moving Mice

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. 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. 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. 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. 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. 5.

   Hayhoe M. Vision using routines: a functional account of vision. Vis. Cogn. 2000;7:43-64.

   Not in our library

6. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 16.

    Hübener M. Mouse visual cortex. Curr. Opin. Neurobiol. 2003;13:413-420.

    Not in our library10.1016/s0959-4388(03)00102-8

17. 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. 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. 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. 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. 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. 22.
    Streamlined sensory motor communication through cortical reciprocal connectivity in a visually guided eye movement task · 2018

    Not checked
23. 23.
    A Head-Mounted Camera System Integrates Detailed Behavioral Monitoring with Multichannel Electrophysiology in Freely Moving Mice · 2018

    No notice
24. 24.

    Payne H.L., Raymond J.L. Magnetic eye tracking in mice. eLife. 2017;6:e29222.

    Not in our library10.7554/elife.29222

25. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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. 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

41. 41.

    Chen P., Hong W. Neural circuit mechanisms of social behavior. Neuron. 2018;98:16-30.

    Not in our library10.1016/j.neuron.2018.02.026

42. 42.

    Bussey T.J., Muir J.L., Everitt B.J., Robbins T.W. Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. Behav. Neurosci. 1997;111:920-936.

    Not in our library10.1037//0735-7044.111.5.920

43. 43.

    Mar A.C., Horner A.E., Nilsson S.R.O., Alsiö J., Kent B.A., Kim C.H., Holmes A., Saksida L.M., Bussey T.J. The touchscreen operant platform for assessing executive function in rats and mice. Nat. Protoc. 2013;8:1985-2005.

    Not in our library10.1038/nprot.2013.123

44. 44.

    Stahl J.S. Using eye movements to assess brain function in mice. Vision Res. 2004;44:3401-3410.

    Not in our library10.1016/j.visres.2004.09.011

45. 45.

    Sakatani T., Isa T. PC-based high-speed video-oculography for measuring rapid eye movements in mice. Neurosci. Res. 2004;49:123-131.

    Not in our library10.1016/j.neures.2004.02.002

46. 46.

    Applebury M.L., Antoch M.P., Baxter L.C., Chun L.L., Falk J.D., Farhangfar F., Kage K., Krzystolik M.G., Lyass L.A., Robbins J.T. The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron. 2000;27:513-523.

    Not in our library10.1016/s0896-6273(00)00062-3

47. 47.

    Szatko K.P., Korympidou M.M., Ran Y., Berens P., Dalkara D., Schubert T., Euler T., Franke K. Neural circuits in the mouse retina support color vision in the upper visual field. bioRxiv. 2019.

    Not in our library10.1101/745539

48. 48.

    Baden T., Schubert T., Chang L., Wei T., Zaichuk M., Wissinger B., Euler T. A tale of two retinal domains: near-optimal sampling of achromatic contrasts in natural scenes through asymmetric photoreceptor distribution. Neuron. 2013;80:1206-1217.

    Not in our library10.1016/j.neuron.2013.09.030

49. 49.

    Welker W.I. Analysis of sniffing of the albino rat. Behaviour. 1964;22:223-244.

    Not in our library

50. 50.

    Deschênes M., Moore J., Kleinfeld D. Sniffing and whisking in rodents. Curr. Opin. Neurobiol. 2012;22:243-250.

    Not in our library10.1016/j.conb.2011.11.013

51. 51.

    Walls G.L. The evolutionary history of eye movements. Vision Res. 1962;2:69-80.

    Not in our library

52. 52.

    Einhäuser W., Moeller G.U., Schumann F., Conradt J., Vockeroth J., Bartl K., Schneider E., König P. Eye-head coordination during free exploration in human and cat. Ann. N Y Acad. Sci. 2009;1164:353-366.

    Not in our library10.1111/j.1749-6632.2008.03709.x

53. 53.

    Freedman E.G. Coordination of the eyes and head during visual orienting. Exp. Brain Res. 2008;190:369-387.

    Not in our library10.1007/s00221-008-1504-8

54. 54.

    Vidal P.P., Roucoux A., Berthoz A. Horizontal eye position-related activity in neck muscles of the alert cat. Exp. Brain Res. 1982;46:448-453.

    Not in our library10.1007/bf00238639

55. 55.

    Paré M., Guitton D. Gaze-related activity of brainstem omnipause neurons during combined eye-head gaze shifts in the alert cat. Exp. Brain Res. 1990;83:210-214.

    Not in our library10.1007/bf00232210

56. 56.

    Lestienne F., Vidal P.P., Berthoz A. Gaze changing behaviour in head restrained monkey. Exp. Brain Res. 1984;53:349-356.

    Not in our library10.1007/bf00238165

57. 57.

    Mitchell J.F., Reynolds J.H., Miller C.T. Active vision in marmosets: a model system for visual neuroscience. J. Neurosci. 2014;34:1183-1194.

    Not in our library10.1523/jneurosci.3899-13.2014

58. 58.

    Stahl J.S., James R.A., Oommen B.S., Hoebeek F.E., De Zeeuw C.I. Eye movements of the murine P/Q calcium channel mutant tottering, and the impact of aging. J. Neurophysiol. 2006;95:1588-1607.

    Not in our library10.1152/jn.00318.2005

59. 59.

    Maruta J., MacDougall H.G., Simpson J.I., Raphan T., Cohen B. Eye velocity asymmetry, ocular orientation, and convergence induced by angular rotation in the rabbit. Vision Res. 2006;46:961-969.

    Not in our library10.1016/j.visres.2005.10.015

60. 60.

    Scholl B., Burge J., Priebe N.J. Binocular integration and disparity selectivity in mouse primary visual cortex. J. Neurophysiol. 2013;109:3013-3024.

    Not in our library10.1152/jn.01021.2012

61. 61.

    La Chioma A., Bonhoeffer T., Hübener M. Area-specific mapping of binocular disparity across mouse visual cortex. Curr. Biol. 2019;29:2954-2960.e5.

    Not in our library10.1016/j.cub.2019.07.037

62. 62.

    Cullen K.E. Vestibular processing during natural self-motion: implications for perception and action. Nat. Rev. Neurosci. 2019;20:346-363.

    Not in our library10.1038/s41583-019-0153-1

63. 63.

    Freedman E.G., Stanford T.R., Sparks D.L. Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. J. Neurophysiol. 1996;76:927-952.

    Not in our library10.1152/jn.1996.76.2.927

64. 64.

    Choi W.Y., Guitton D. Firing patterns in superior colliculus of head-unrestrained monkey during normal and perturbed gaze saccades reveal short-latency feedback and a sluggish rostral shift in activity. J. Neurosci. 2009;29:7166-7180.

    Not in our library10.1523/jneurosci.5038-08.2009

65. 65.

    Wilson J.J., Alexandre N., Trentin C., Tripodi M. Three-dimensional representation of motor space in the mouse superior colliculus. Curr. Biol. 2018;28:1744-1755.e12.

    Not in our library10.1016/j.cub.2018.04.021

66. 66.

    Masullo L., Mariotti L., Alexandre N., Freire-Pritchett P., Boulanger J., Tripodi M. Genetically defined functional modules for spatial orienting in the mouse superior colliculus. Curr. Biol. 2019;29:2892-2904.e8.

    Not in our library10.1016/j.cub.2019.07.083

67. 67.

    Sylvestre P.A., Cullen K.E. Premotor correlates of integrated feedback control for eye-head gaze shifts. J. Neurosci. 2006;26:4922-4929.

    Not in our library10.1523/jneurosci.4099-05.2006

68. 68.
    A Kinematic Model for 3-D Head-Free Gaze-Shifts · 2015

    Not checked
69. 69.

    Haji-Abolhassani I., Guitton D., Galiana H.L. Modeling eye-head gaze shifts in multiple contexts without motor planning. J. Neurophysiol. 2016;116:1956-1985.

    Not in our library10.1152/jn.00605.2015

70. 70.

    Chaplin T.A., Margrie T.W. Cortical circuits for integration of self-motion and visual-motion signals. Curr. Opin. Neurobiol. 2020;60:122-128.

    Not in our library10.1016/j.conb.2019.11.013

71. 71.

    Voigts J., Harnett M.T. Somatic and dendritic encoding of spatial variables in retrosplenial cortex differs during 2D navigation. Neuron. 2020;105:237-245.e4.

    Not in our library10.1016/j.neuron.2019.10.016

72. 72.

    Stowers J.R., Hofbauer M., Bastien R., Griessner J., Higgins P., Farooqui S., Fischer R.M., Nowikovsky K., Haubensak W., Couzin I.D. Virtual reality for freely moving animals. Nat. Methods. 2017;14:995-1002.

    Not in our library10.1038/nmeth.4399

73. 73.

    Del Grosso N.A., Graboski J.J., Chen W., Blanco Hernández E., Sirota A. Virtual reality system for freely-moving rodents. bioRxiv. 2017.

    Not in our library10.1101/161232

74. 74.

    Luo L., Callaway E.M., Svoboda K. Genetic dissection of neural circuits. Neuron. 2008;57:634-660.

    Not in our library10.1016/j.neuron.2008.01.002

75. 75.

    Mathis A., Mamidanna P., Cury K.M., Abe T., Murthy V.N., Mathis M.W., Bethge M. DeepLabCut: markerless pose estimation of user-defined body parts with deep learning. Nat. Neurosci. 2018;21:1281-1289.

    Not in our library10.1038/s41593-018-0209-y

76. 76.

    Siegle J.H., López A.C., Patel Y.A., Abramov K., Ohayon S., Voigts J. Open Ephys: an open-source, plugin-based platform for multichannel electrophysiology. J. Neural Eng. 2017;14:045003.

    Not in our library10.1088/1741-2552/aa5eea

77. 77.

    Oliphant T.E. Python for scientific computing. Comput. Sci. Eng. 2007;9:10-20.

    Not in our library

78. 78.

    Pedregosa F., Varoquaux G., Gramfort A., Michel V., Thirion B., Grisel O., Blondel M., Prettenhofer P., Weiss R., Dubourg V. Scikit-learn: machine learning in Python. J. Mach. Learn. Res. 2011;12:2825-2830.

    Not in our library

79. 79.

    MacKay D.J.C., Heidbreder G.R. Bayesian non-linear modeling for the prediction competition. Maximum Entropy and Bayesian Methods. 1996;221-234.

    Not in our library

Cited by papers we hold 1

• Dynamics of gaze control during prey capture in freely moving mice · 2020
  No notice

Reads

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.