Abstract
Rapid shifts of the point of visual fixation between equidistant targets require equal-sized saccades of each eye. The brainstem medial longitudinal fasciculus (MLF) plays a cardinal role in ensuring that horizontal saccades between equidistant targets are tightly yoked. Lesions of the MLF—internuclear ophthalmoparesis (INO)—cause horizontal saccades to become disjunctive: adducting saccades are slow, small, or absent. However, in INO, convergence movements may remain intact. We studied horizontal gaze shifts between equidistant targets and between far and near targets aligned on the visual axis of one eye (Müller test paradigm) in five cases of INO and five control subjects. We estimated the saccadic component of each movement by measuring peak velocity and peak acceleration. We tested whether the ratio of the saccadic component of the adducting/abducting eyes stayed constant or changed for the two types of saccades. For saccades made by control subjects between equidistant targets, the group mean ratio (±SD) of adducting/abducting peak velocity was 0.96 ± 0.07 and adducting/abducting peak acceleration was 0.94 ± 0.09. Corresponding ratios for INO cases were 0.45 ± 0.10 for peak velocity and 0.27 ± 0.11 for peak acceleration, reflecting reduced saccadic pulses for adduction. For control subjects, during the Müller paradigm, the adducting/abducting ratio was 1.25 ± 0.14 for peak velocity and 1.03 ± 0.12 for peak acceleration. Corresponding ratios for INO cases were 0.82 ± 0.18 for peak velocity and 0.48 ± 0.13 for peak acceleration. When adducting/abducting ratios during Müller versus equidistant targets paradigms were compared, INO cases showed larger relative increases for both peak velocity and peak acceleration compared with control subjects. Comparison of similar-sized movements during the two test paradigms indicated that whereas INO patients could decrease peak velocity of their abducting eye during the Müller paradigm, they were unable to modulate adducting velocity in response to viewing conditions. However, the initial component of each eye’s movement was similar in both cases, possibly reflecting activation of saccadic burst neurons. These findings support the hypothesis that horizontal saccades are governed by disjunctive signals, preceded by an initial, high-acceleration conjugate transient and followed by a slower vergence component.
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References
Collewijn H, Erkelens CJ, Steinman RM (1995) Voluntary binocular gaze-shifts in the plane of regard: dynamics of version and vergence. Vision Res 35:3335–3358
Cullen KE, Guitton D (1997) Analysis of primate IBN spike trains using system identification techniques. I. Relationship to eye movement dynamics during head-fixed saccades. J Neurophysiol 78:3259–3282
Davis SL, Frohman TC, Crandall CG, Brown MJ, Mills DA, Kramer PD, Stuve O, Frohman EM (2008) Modeling Uhthoff’s phenomenon in MS patients with internuclear ophthalmoparesis. Neurology 70:1098–1106
Gamlin PDR, Gnadt JW, Mays LE (1989a) Abducens internuclear neurons carry an inappropriate signal for ocular convergence. J Neurophysiol 62:70–81
Gamlin PDR, Gnadt JW, Mays LE (1989b) Lidocaine-induced unilateral internuclear ophthalmoplegia: effects on convergence and conjugate eye movements. J Neurophysiol 62:82–95
Horn AKE, Büttner-Ennever JA, Suzuki Y, Henn V (1997) Histological identification of premotor neurons for horizontal saccades in monkey and man by parvalbumin immunostaining. J Comp Neurol 359:350–363
King WM, Zhou W (1995) Initiation of disjunctive smooth pursuit in monkeys: evidence that Hering’s law of equal innervation is not obeyed by the smooth pursuit system. Vision Res 35:3389–3400
King WM, Zhou W (2000) New ideas about binocular coordination of eye movements: is there a chameleon in the primate family tree? Anat Rec 261:153–161
King WM, Zhou W (2002) Neural basis of disjunctive eye movements. Ann N Y Acad Sci 956:273–283
Kumar AN, Han Y, Dell’osso LF, Durand DM, Leigh RJ (2004) Directional asymmetry during combined saccade-vergence movements. J Neurophysiol
Leigh RJ, Serra A (2008) Taking the temperature of MS with INO. Neurology 70:1063–1064
Leigh RJ, Zee DS (2006) The neurology of eye movements (Book/DVD), 4th edn. Oxford University Press, New York
Liao K, Walker MF, Joshi A, Reschke M, Leigh RJ (2008) Vestibulo-ocular responses to vertical translation in normal human subjects. Exp Brain Res 185:553–562
Matta M, Leigh RJ, Pugliatti M, Aiello I, Serra A (2009) Using fast eye movements to study fatigue in multiple sclerosis. Neurology 73:798–804
Mays LE (1998) Has Hering been hooked? Nat Med 4:889–890
Mays LE, Porter JD, Gamlin PD, Tello CA (1986) Neural control of vergence eye movements: neurons encoding vergence velocity. J Neurophysiol 56:1007–1021
McConville K, Tomlinson RD, King WM, Paige G, EQ NA (1994) Eye position signals in the vestibular nuclei: consequences for models of integrator function. J Vestib Res 4:391–400
Ramat S, Zee DS (2005) Binocular coordination in fore/aft motion. Ann N Y Acad Sci 1039:36–53
Ramat S, Das VE, Somers JT, Leigh RJ (1999a) Tests of two hypotheses to account for different-sized saccades during disjunctive gaze shifts. Exp Brain Res 129:500–510
Ramat S, Somers JT, Das VE, Leigh RJ (1999b) Conjugate ocular oscillations during shifts of the direction and depth of visual fixation. Invest Ophthalmol Vis Sci 40:1681–1686
Ramat S, Leigh RJ, Zee DS, Optican LM (2004) Ocular oscillations generated by coupling of brainstem excitatory and inhibitory saccadic burst neurons. Exp Brain Res 160:89–106
Robinson DA (1964) The mechanics of human saccadic eye movement. J Physiol (Lond) 174:245–264
Serra A, Liao K, Matta M, Leigh RJ (2008) Diagnosing disconjugate eye movements: phase-plane analysis of horizontal saccades. Neurology 71:1167–1175
Sylvestre PA, Cullen KE (2002) Dynamics of abducens nucleus neuron discharges during disjunctive saccades. J Neurophysiol 88:3452–3468
Sylvestre PA, Choi JT, Cullen KE (2003) Discharge dynamics of oculomotor neural integrator neurons during conjugate and disjunctive saccades and fixation. J Neurophysiol 90:739–754
Van Gisbergen JAM, Robinson DA, Gielen S (1981) A quantitative analysis of generation of saccadic eye movements by burst neurons. J Neurophysiol 45:417–442
Van Horn MR, Cullen KE (2009) Dynamic characterization of agonist and antagonist oculomotoneurons during conjugate and disconjugate eye movements. J Neurophysiol 102:28–40
Zee DS (1992) Internuclear ophthalmoplegia: pathophysiology and diagnosis. Baillieres Clin Neurol 1:455–470
Zee DS, Hain TC, Carl JR (1987) Abduction nystagmus in internuclear ophthalmoplegia. Ann Neurol 21:383–388
Zee DS, FitzGibbon EJ, Optican LM (1992) Saccade-vergence interactions in humans. J Neurophysiol 68:1624–1641
Zhang Y, Gamlin PD, Mays LE (1991) Antidromic identification of midbrain near response cells projecting to the oculomotor nucleus. Exp Brain Res 84:525–528
Zhou W, King WM (1998) Premotor commands encode monocular eye movements. Nature 393:692–695
Acknowledgments
Supported by the Office of Research and Development, Medical Research Service, and MS Centers of Excellence, Department of Veterans Affairs; NIH grant R01 EY06717, and the Evenor Armington Fund. We are grateful to Dr. W. M. King for his critical comments, to Drs. K. E. Cullen, and P. D. R. Gamlin for helpful advice, and to Dr. Ke Liao for technical assistance.
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Chen, A.L., Ramat, S., Serra, A. et al. The role of the medial longitudinal fasciculus in horizontal gaze: tests of current hypotheses for saccade-vergence interactions. Exp Brain Res 208, 335–343 (2011). https://doi.org/10.1007/s00221-010-2485-y
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DOI: https://doi.org/10.1007/s00221-010-2485-y