Abstract
The oculomotor integrator is a brainstem neural network that converts velocity signals into the position commands necessary for eye-movement control. The cerebellum can independently adjust the amplitude of eye-movement commands and the temporal characteristics of neural integration, but the percentage of integrator neurons that receive cerebellar input is very small. Adaptive dynamic systems models, configured using the genetic algorithm, show how sparse cerebellar inputs could morph the dynamics of the oculomotor integrator and independently adjust its overall response amplitude and time course. Dynamic morphing involves an interplay of opposites, in which some model Purkinje cells exert positive feedback on the network, while others exert negative feedback. Positive feedback can be increased to prolong the integrator time course at virtually any level of negative feedback. The more these two influences oppose each other, the larger become the response amplitudes of the individual units and of the overall integrator network.
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References
Anastasio TJ (1998) Nonuniformity in the linear network model of the oculomotor integrator produces approximately fractional-order dynamics and more realistic neuron behavior. Biol. Cybern. 79: 377–391.
Anastasio TJ (2001) A pattern correlation model of vestibulo-ocular reflex habituation. Neural Netw. 14: 1–22.
Anastasio TJ, Robinson DA (1991) Failure of the oculomotor neural integrator from a discrete midline lesion between the abducens nuclei in the monkey. Neurosci. Lett. 127: 82–86.
Arnold DB, Robinson DA (1991) A learning network model of the neural integrator of the oculomotor system. Biol. Cybern. 64: 447–454.
Arnold DB, Robinson DA (1997) The oculomotor integrator: Testing of a neural network model. Exp. Brain. Res. 113: 57–74.
Babalian AL, Vidal PP (2000) Floccular modulation of vestibuloocular pathways and cerebellum-related plasticity: An in vitro whole brain study. J. Neurophysiol. 84: 2514–2528.
Belton T, McCrea RA (2004) Context contingent signal processing in the cerebellar flocculus and ventral paraflocculus during gaze saccades. J. Neurophysiol. 92: 797–807.
Bevington PR (1969) Data Reduction and Error Analysis for the Physical Sciences. McGraw-Hill, New York.
Blazquez PM, Hirata Y, Heiney SA, Green AM, Highstein SM (2003) Cerebellar signatures of vestibulo-ocular reflex motor learning. J. Neurosci. 23: 9742–9751.
Büttner-Ennever JA (ed.) (1988) Neuroanatomy of the Oculomotor System. Elsevier, Amsterdam.
Cannon SC, Robinson DA (1987) Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. J. Neurophysiol. 57: 1383–1409.
Cannon SC, Robinson DA, Shamma S (1983) A proposed neural network for the integrator of the oculomotor system. Biol. Cybern. 49: 127–136.
Chan WWP, Galiana HL (2005) Integrator function in the oculomotor system is dependent on sensory context. J. Neurophysiol. 93: 3709–3717.
Chelazzi L, Ghirardi M, Rossi F, Strata P, Tempia F (1990) Spontaneous saccades and gaze holding ability in the pigmented rat. II. Effects of localized cerebellar lesions. Eur. J. Neurosci. 2: 1085–1094.
Cheron G, Escudero M, Godaux E (1996) Discharge properties of brain stem neurons projecting to the flocculus in the alert cat. I. Medial vestibular nucleus. J. Neurophysiol. 76: 1759–1774.
Cheron G, Godaux E, Laune JM, Vanderkelen B (1986) Lesions in the cat prepositus complex: Effects on the vestibulo-ocular reflex and saccades. J. Physiol. 372: 75–94.
Dufossé M, Ito M, Jastreboff PJ, Miyashita Y (1978) A neuronal correlate in rabbit's cerebellum to adaptive modification of the vestibulo-ocular reflex. Brain Res. 150: 611–616.
Epema AH, Gerrits NM, Voogd J (1990) Secondary vestibulocerebellar projections to the flocculus and uvulo-nodular lobule of the rabbit: A study using HRP and double fluorescent tracer techniques. Exp. Brain Res. 80: 72–82.
Godaux E, Vanderkelen B (1984) Vestibulo-ocular reflex, optokinetic response and their interactions in the cerebellectomized cat. J. Physiol. 346: 155–170.
Goldberg E (1989) Genetic Algorithms in Search, Optimization and Machine Learning. Addison-Wesley, Boston.
Holland H (1975) Adaptation in Natural and Artificial Systems. University of Michigan Press, Ann Arbor.
Ito M (1982) Cerebellar control of the vestibulo-ocular reflex – around the flocculus hypothesis. Ann. Rev. Neurosci. 5: 275–296.
Katoh A, Yoshida T, Himeshima Y, Mishina M, Hirano T (2005) Defective control and adaptation of reflex eye movements in mutant mice deficient in either the glutamate receptor δ2 subunit or Purkinje cells. Eur J Neurosci 21: 1315–1326.
Keller EL, Precht W (1979) Adaptive modification of central vestibular neurons in response to visual stimulation through reversing prisms. J. Neurophysiol. 42: 896–911.
du Lac S, Raymond JL, Sejnowski TJ, Lisberger SG (1995) Learning and memory in the vestibulo-ocular reflex. Ann. Rev. Neurosci. 18: 409–441.
Langer T, Fuchs AF, Scudder CA, Chubb MC (1985a) Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. J. Comp. Neurol. 235: 1–25.
Langer T, Fuchs AF, Chubb MC, Scudder CA, Lisberger SG (1985b) Flocculuar efferents in the rhesus macaque as revealed by autoradiography and horseradish peroxidase. J. Comp. Neurol. 235: 26–37.
Leigh RJ, Zee DS (1983) The Neurology of Eye Movements. Davis, Philadelphia.
Lisberger SG, Miles FA (1980) Role of primate medial vestibular nucleus in long-term adaptive plasticity of vestibuloocular reflex. J. Neurophysiol. 43: 1725–1745.
Lisberger SG, Pavelko TA (1988) Brain stem neurons in modified pathways for motor learning in the primate vestibulo-ocular reflex. Science 242: 771–773.
Lisberger SG, Pavelko TA, Broussard DM (1994a) Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons. J. Neurophysiol. 72: 928–953.
Lisberger SG, Pavelko TA, Bronte-Stewart HM, Stone LS (1994b) Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocclus and ventral paraflocculus. J. Neurophysiol. 72: 954–973.
Luenberger G (1979) Introduction to Dynamic Systems. John Wiley, New York.
McCrea RA, Strassman A, May E, Highstein SM (1987) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J. Comp. Neurol. 264: 547–570.
McFarland JL, Fuchs AF (1992) Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. J. Neurophysiol. 68: 319–332.
Miles FA, Fuller JH, Braitman DJ (1980a) Long term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J. Neurophysiol. 43: 1437–1476.
Miles FA, Braitman DJ, Dow BM (1980b) Long term adaptive changes in primate vestibuloocular reflex. IV. Electrophysiological observations in flocculus of adapted monkeys. J. Neurophysiol. 43: 1477–1493.
Nagao S (1983) Effect of vestibulo-cerebellar lesion upon dynamic characteristics and adaptation of the vestibuloocular and optokinetic responses in pigmented rabbits. Exp. Brain Res. 53: 36–46.
Nagao S (1989) Behavior of floccular Purkinje cells correlated with adaptation of vestibulo-ocular reflex in pigmented rabbits. Exp. Brain Res. 77: 531–540.
Nagao S, Kitazawa H (2003) Effects of reversible shutdown of the monkey flocculus on the retention of adaptation of the horizontal vestibulo-ocular reflex. Neuroscience 118: 563–570.
Rambold H, Churchland A, Selig Y, Jasmin L, Lisberger SG (2002) Partial ablations of the flocculus and ventral paraflocculus in monkeys cause linked deficits in smooth pursuit eye movements and adaptive modification of the VOR. J. Neurophysiol. 87: 912–924.
Robinson D (1974) The effect of cerebellectomy on the cat's vestibulo-ocular integrator. Brain Res. 71: 195–207.
Robinson DA (1976) Adaptive gain control of vestibuloocular reflex by the cerebellum. J. Neurophysiol. 39: 954–969.
Robinson DA (1989a) Integrating with neurons. Annu. Rev. Neurosci. 12: 33–45.
Robinson DA (1989b) Control of eye movements. In: V.B. Brooks ed. Handbook of Physiology, Sect. 1: The Nervous System, Vol. II part 2. American Physiological Society, Bethesda, pp. 1275–1320.
Sekirnjak C, du Lac S (2006) Physiological and anatomical properties of mouse medial vestibular nucleus neurons projecting to the oculomotor nucleus. J. Neurophysiol. 95: 3012–3023.
Sekirnjak C, Vissel B, Bollinger J, Faulstich M, du Lac S (2003) Pur-kinje cell synapses target physiologically unique brainstem neurons. J. Neurosci. 23: 6392–6398.
Stahl JS (2004) Eye movements of the murine P/Q calcium channel mutant Rocker, and the impact of aging. J. Neurophysiol. 91: 2066–2078.
Stahl JS, James RA (2005) Neural integrator function in murine CACNA1A mutants. Ann. NY Acad. Sci. 1039: 580–582.
Stahl JS, Simpson JI (1995) Dynamics of rabbit vestibular nucleus neurons and the influence of the flocculus. J. Neurophysiol. 73: 1396–1413.
Sutton RS, Barto AG (1998) Reinforcement Learning: An Introduction. MIT Press, Cambridge.
Tan H, Gerrits NM (1992) Laterality in the vestibulo-cerebellar mossy fiber projection to flocculus and caudal vermis in the rabbit: A retrograde fluorescent double-labeling study. Neuroscience 47: 909–919.
Tiliket C, Shelhamer M, Roberts D, Zee DS (1994) Short term vestibulo-ocular reflex adaptation in humans. I. Effect on the ocular motor velocity-to-position neural integrator. Exp. Brain Res. 100: 316–327.
Watanabe E (1985) Role of the primate flocculus in adaptation of the vestibulo-ocular reflex. Neurosci. Res. 3: 20–38.
Wilson VJ, Melvill Jones JG (1979) Mammalian Vestibular Physiology. Plenum Press, New York.
Yoshida T, Katoh A, Ohtsuki G, Mishina M, Hirano T (2004) Oscillating Purkinje neuron activity causing involuntary eye movement in a mutant mouse deficient in the glutamate receptor δ2 subunit. J. Neurosci. 24: 2440–2448.
Zee S, Yamazaki A, Butler PH, Gücer G (1981) Effects of ablation of flocculus and paraflocculus on eye movements in primate. J. Neurophysiol. 46: 878–899.
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We thank J. Bronski for mathematical consultation and J. Malpeli for suggestions. We also thank the two anonymous reviewers for constructive comments.
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Anastasio, T.J., Gad, Y.P. Sparse cerebellar innervation can morph the dynamics of a model oculomotor neural integrator. J Comput Neurosci 22, 239–254 (2007). https://doi.org/10.1007/s10827-006-0010-x
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DOI: https://doi.org/10.1007/s10827-006-0010-x