Abstract
The rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) contains burst neurons whose activity precedes rapid eye movements with a vertical and/or torsional component. To ascertain their causal role in the generation of conjugate eye movements, we placed uni- and bilateral kainic acid lesions in that region. Unilateral inactivation of the riMLF leads to a loss of all rapid eye movements with an ipsitorsional component (ipsitorsional is defined as movement of the upper pole of the ipsilateral eye in a temporal direction). Vertical eye movements are impaired in an asymmetric way, with downward movements slowed and upward movements little affected. Listing's plane is shifted in the contratorsional direction, i.e., we find a constant torsional offset for all eye positions. With bilateral lesions one observes a total loss of all vertical and torsional eye movements, while Listing's plane retains its shape and position. These results show that burst neurons in the riMLF play a decisive role in generating rapid eye movements with a vertical and torsional component.
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Büttner U, Büttner-Ennever JA, Henn V (1977) Vertical eye movement related unit activity in the rostral mesencephalic reticular formation of the alert monkey. Brain Res 130:239–252
Büttner-Ennever JA, Büttner U (1978) A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Res 151:31–47
Coyle JT, Molliver ME, Kuhar MJ (1978) In situ injection of kainic acid: a new method for selectively lesioning neuronal cell bodies while sparing axons of passage. J Comp Neurol 180:301–324
Crawford JD, Vilis (1991) Axes of eye rotation and Listing's law during rotations of the head. J Neurophysiol 65:407–423
Crawford JD, Vilis T (1992) Symmetry of oculomotor burst neuron coordinates about Listing's plane. J Neurophysiol 68:432–448
Crawford JD, Cadera W, Vilis T (1991) Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal. Science 252:1551–1553
Fukushima K, Kaneko CRS, Fuchs AF (1992) The neuronal substrate of integration in the oculomotor system. Prog Neurobiol 39:609–639
Graybiel AM (1977) Organization of oculomotor pathways in the cat and rhesus monkey. In: Baker R, Berthoz A (eds) Control of gaze by brain stem neurons. Elsevier, Amsterdam, pp 79–88
Haslwanter T, Straumann D, Hepp K, Hess BJM, Henn V (1991) Smooth pursuit eye movements obey Listing's law in the monkey. Exp Brain Res 87:470–472
Haslwanter T, Straumann D, Hess BJM, Henn V (1992) Static roll and pitch in the monkey: shift and rotation of Listing's plane. Vision Res 32:1341–1348
Haustein W (1989) Considerations on Listing's law and the primary position by means of a matrix description of eye position control. Biol Cybern 60:411–420
Helmholtz H (1867) Handbuch der Physiologischen Optik. Voss, Leipzig
Henke H, Cuénod M (1980) Specific [3H] kainic acid binding in the vertebrate CNS. In: Littauer VZ, Dudai Y, Silman I, Teichberg VI, Vogel Z (eds) Neurotransmitters and their receptors. Wiley, Chichester, pp 373–390
Henn V, Lang W, Hepp K, Reisine H (1984) Experimental gaze palsies in monkeys and their relation to human pathology. Brain 107:619–636
Henn V, Schnyder H, Hepp K, Reisine H (1983) Loss of vertical rapid eye movements after kainic acid lesions in the rostral mesencephalon in the rhesus monkey. Soc Neurosci Abstr 9:749
Henn V, Suzuki Y, Straumann D (1993) Characteristics of rapid eye movements after lesions of the rostral interstitial nucleus of the MLF in the rhesus monkey. Soc Neurosci Abstr 19:1593
Hepp K, Vilis T, Henn V (1988) On the generation of rapid eye movements in three dimensions. Ann NY Acad Sci 545:140–153
Hepp K, Henn V, Vilis T, Cohen B (1989) Brainstem regions related to saccade generation. In: Wurtz RH, Goldberg ME (eds) The neurobiology of saccadic eye movements. Elsevier, Amsterdam, pp 105–212
Hepp K, Opstal AJ van, Straumann D, Hess BJM, Henn V (1993) Monkey superior colliculus represents rapid eye movements in a two-dimensional motor map. J Neurophysiol 69:965–979
Hepp K, Suzuki Y, Straumann D, Hess BJM (1994) On the three-dimensional rapid eye movement generator in the monkey. In: Delgado-Garcia JM, Godeaux E, Vidal PP (eds) Information processing underlying gaze control. Pergamon, Oxford, pp 65–74
Hess BJM (1990) Dual-search coil for measuring three-dimensional eye movements in experimental animals. Vision Res 30:597–602
Hess BJM, Opstal AJ van, Straumann D, Hepp K (1992) Calibration of three-dimensional eye position using search coil signals in the rhesus monkey. Vision Res 32:1647–1654
King WM, Fuchs AF (1979) Reticular control of vertical saccadic eye movements by mesencephalic burst neurons. J Neurophysiol 42:861–876
Kömpf D, Pasik T, Pasik P, Bender MB (1979) Downward gaze in monkeys — stimulation and lesion studies. Brain 102:527–558
Lang W, Henn V, Hepp K (1982) Gaze palsies after selective pontine lesions in monkeys. In: Roucoux A, Crommelinck M (eds) Physiological and pathological aspects of eye movements. Junk, The Hague, pp 209–218
McGeer EG, Olney JW, McGeer PL (1978) Kainic acid as a tool in neurobiology. Raven, New York
Monakow C von (1905) Gehirnpathologie. Hölder, Vienna
Moschovakis AK, Scudder CA, Highstein M (1991a) Structure of the primate oculomotor burst generator I. Medium-lead burst neurons with upward on-directions. J Neurophysiol 65:203–217
Moschovakis AK, Scudder CA, Highstein M, Warren JD (1991b) Structure of the primate oculomotor burst generator II. Medium-lead burst neurons with downward on-directions. J Neurophysiol 65:218–229
Robinson DA (1963) A method of measuring eye movements using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10:137–145
Schnabolk C, Raphan T (1994) Modeling three-dimensional velocity-to-position transformations in oculomotor control. J Neurophsyiol 71:623–638
Straumann D, Suzuki M, Henn V, Hess BJM, Haslwanter T (1992) Visual suppression of torsional vestibular nystagmus in rhesus monkeys. Vision Res 32:1067–1074
Suzuki Y, Straumann D, Hess BJM, Henn V (1993) Torsional eye position and movements after lesions of the rostral interstitial nucleus of the MLF. Soc Neurosci Abstr 19:1593
Suzuki Y, Straumann D, Hess BJM, Henn V (1994) Changes of Listing's plane under physiological and pathological conditions. In: Delgado-Garcia JM, Godeaux E, Vidal PP (eds) Information processing underlying gaze control: Pergamon, Oxford, pp 75–86
Tweed D, Vilis T (1990) Geometric relations of eye position and velocity vectors during saccades. Vision Res 30:111–127
Tweed D, Fetter M, Andreadaki S, Koenig E, Dichgans J (1992) Three-dimensional properties of human pursuit eye movement. Vision Res 32:1225–1238
Tweed D, Misslisch H, Fetter M (1994) Testing models of the oculomotor velocity to position transformation. J Neurophysiol 72:1425–1429
Vilis T, Hepp K, Schwarz U, Henn V (1989) On the generation of vertical and torsional rapid eye movements in the monkey. Exp Brain Res 77:1–11
Wurtz RH (1969) Visual receptive fields of striate cortex neurons in awake monkeys. J Neurophysiol 52:727–742
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Suzuki, Y., Büttner-Ennever, J.A., Straumann, D. et al. Deficits in torsional and vertical rapid eye movements and shift of Listing's plane after uni- and bilateral lesions of the rostral interstitial nucleus of the medial longitudinal fasciculus. Exp Brain Res 106, 215–232 (1995). https://doi.org/10.1007/BF00241117
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DOI: https://doi.org/10.1007/BF00241117