Abstract
We measured rotation (horizontal, vertical and torsional) and translation (horizontal and vertical) of the paralysed cat's eye in response to 45° steps of orientation presented in a pseudorandom order around the roll and pitch axes (with respect to the horizontal canals). During changes of position of the animal in the roll plane, the eyes rotated towards the lowest part of the orbit (left with left ear down; top when the cat was upside down, etc.) by an average of 0.55°. Changing orientation in the pitch plane evoked vertical rotations of ±1.42° (upwards eye movement during forwards head pitch) and torsional rotations of ±1.3°. All these rotations taken together suggest that the centre of mass is in front of, below and temporal to the centre of rotation. The eyes translated temporally (thus separating by 0.72 mm) during forward pitching and there was a small vertical displacement (0.23 mm) when the animal was upside down. These findings are discussed with respect to a possible role of the extraocular proprioception system.
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References
Alvarado-Mallart RM, Pinçon-Raymond M (1976) Nerve endings on the intramuscular tendons of cat extraocular muscles. Neurosci Lett 2:121–125
Alvarado-Mallart RM, Pinçon-Raymond M (1979) The palisade endings of cat extraocular muscles: a light and electron microscope study. Tissue Cell 11:567–584
Anderson JH (1981) Ocular torsion in the cat after lesions of the interstitial nucleus of Cajal. Ann NY Acad Sci 374:865–871
Bach-y-Rita P, Ito F (1966) Properties of stretch receptors in cat extraocular muscles. J Physiol (Lond) 186:663–688
Barlow HB, Derrington AM, Harris LR, Lennie P (1977) The effects of remote visual stimulation on the responses of cat retinal ganglion cells. J Physiol (Lond) 269:177–194
Blanks RHI, Curthoys IS, Markham CH (1972) Planar relationships of semicircular canals in the cat. A J Physiol 223:55–62
Cilimbaris PA (1910) Histologische Untersuchungen über die Muskelspindeln der Augenmuskeln. Arch Mikrosk Anat 75:692–747
Clément G, Andre-Deshays C, Lathan CE (1989) Effects of gravitoinertial force variations on vertical gaze direction during oculomotor reflexes and visual fixation. Aviat Space Environ Med 60:1194–1198
Collins CC (1971) Orbital mechanics. In: Beach-y-Rita P, Collins CC, Hyde JE (eds) The control of eye movements. Academic, New York pp 285–325
Cooper S, Daniel PM, Whitteridge D (1955) Muscle spindles and other sensory endings in the extrinsic eye muscles: the physiology and anatomy of the receptors and of their connections with the brain stem. Brain 78:564–583
De Beer GR (1947) How animals hold their heads. Proc Linnean Soc (London) 159:125–139
Goltz HC, Harris LR, Steinbach MJ (1992) Gravity as a passive force on the cat's eye: implications for oculomotor control. Invest Ophthalmol Vis Sci [Suppl] 33:1150
Gnadt JW, Bracewell RM, Andersen RA (1991) Sensorimotor transformation during eye movements to remembered visual targets. Vision Res 31:693–715
Harker DW (1972) The structure and innervation of sheep superior rectus and levator palpebrae muscles. II. Muscle spindles. Invest Ophthalmol 11:970–979
Harris ER (1987) Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis. Exp Brain Res 66:522–532
Harris ER, Steinbach MJ, Goltz HC (1991) Gravity affects the position of the paralysed cat's eye. Soc Neurosci Abstr 17:337.4
Matthews PBC (1972) Mammalian muscle receptors and their central actions. Arnold, London
Matthews PBC (1982) Where does Sherrington's muscular sense originate? Muscles, joints, corollary discharges? Annu Rev Neurosci 5:189–218
Matthews PBC (1988) Proprioceptors and their contribution to somatosensory mapping — complex messages require complex processing. C J Physiol Pharmacol 66:430–438
Porter JD, Spencer RF (1982) Localization and morphology of cat extraocular muscle afferent neurones identified by retrograde transport of horseradish peroxidase. J Comp Neurol 204:56–64
Rodieck RW, Pettigrew JD, Bishop PO, Nikara T (1967) Residual eye movements in receptive-field studies of paralyzed cats. Vision Res 7:107–110
Rude SW, Powell KD, Baker JF (1991) Effects of roll tilt on pitch vertical vestibuloocular reflex. Soc Neurosci Abstr 17:127.14
Spencer RF, Porter JD (1988) Structural organization of the extraocular muscles. In: Büttner-Ennever JA (eds) Neuroanatomy of the oculomotor system. Elsevier, Amsterdam, pp 33–79
Steinbach MJ (1987) Proprioceptive knowledge of eye position. Vision Res 27:1737–1744
Steinbach MJ (1992) The need for eye muscle proprioception. In: Jami E, Pierrot-Deseilligny E, Zytnicki D (eds) Muscle afferents and spinal control of movement. Pergamon, London, pp 239–244
Steinbach MJ, Lerman J (1990) Gravity affects resting eye position in humans. Invest Ophthalmol Vis Sci [Suppl] 31:533
Tripathi RC (1974) Comparative physiology and anatomy of the outflow pathway. In: Davson H, Graham LT (eds) The eye, vol 5. Academic, New York, pp 163–335
Wilson VJ, Jones GM (1979) Mammalian vestibular physiology. Plenum, New York
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Harris, L.R., Goltz, H.C. & Steinbach, M.J. The effect of gravity on the resting position of the cat's eye. Exp Brain Res 96, 107–116 (1993). https://doi.org/10.1007/BF00230444
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DOI: https://doi.org/10.1007/BF00230444