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Vestibulo-ocular reflexes (VORs) are the dominating contributors to gaze stabilization in all vertebrates. During horizontal head movements, abducens motoneurons form the final element of the reflex arc that integrates visuovestibular inputs into temporally precise motor commands for the lateral rectus eyemuscle. Here, we studied a possible differentiation of abducens motoneurons into subtypes by evaluating their morphology, discharge properties, and synaptic pharmacology in semi-intact in vitro preparations of larval Xenopus laevis Extracellular nerve recordings during sinusoidal head motion revealed a continuum of resting rates and activation thresholds during vestibular stimulation. Differences in the sensitivity to changing stimulus frequencies and velocities allowed subdividing abducens motoneurons into two subgroups, one encoding the frequency and velocity of head motion (Group I), and the other precisely encoding angular velocity independent of stimulus frequency (Group II). Computational modeling indicated that Group II motoneurons are the major contributor to actual eye movements over the tested stimulus range. The segregation into two functional subgroups coincides with a differential activation of glutamate receptor subtypes. Vestibular excitatory inputs in Group I motoneurons are mediated predominantly by NMDA receptors and to a lesser extent by AMPA receptors, whereas an AMPA receptor-mediated excitation prevails in Group II motoneurons. Furthermore, glycinergic ipsilateral vestibular inhibitory inputs are activated during the horizontal VOR, whereas the tonic GABAergic inhibition is presumably of extravestibular origin. These findings support the presence of physiologically and pharmacologically distinct functional subgroups of extraocular motoneurons that act in concert to mediate the large dynamic range of extraocular motor commands during gaze stabilization.SIGNIFICANCE STATEMENT Outward-directed gaze-stabilizing eye movements are commanded by abducens motoneurons that combine different sensory inputs including signals from the vestibular system about ongoing head movements (vestibulo-ocular reflex). Using an amphibian model, this study investigates whether different types of abducens motoneurons exist that become active during different types of eye movements. The outcome of this study demonstrates the presence of specific motoneuronal populations with pharmacological profiles that match their response dynamics. The evolutionary conservation of the vestibulo-ocular circuitry makes it likely that a similar motoneuronal organization is also implemented in other vertebrates. Accordingly, the physiological and pharmacological understanding of specific motoneuronal contributions to eye movements might help in designing drug therapies for human eye movement dysfunctions such as abducensnerve palsy.
Beraneck,
Differential intrinsic response dynamics determine synaptic signal processing in frog vestibular neurons.
2007, Pubmed
Beraneck,
Differential intrinsic response dynamics determine synaptic signal processing in frog vestibular neurons.
2007,
Pubmed
Birch,
6,7-Dinitro-quinoxaline-2,3-dion and 6-nitro,7-cyano-quinoxaline-2,3-dion antagonise responses to NMDA in the rat spinal cord via an action at the strychnine-insensitive glycine receptor.
1988,
Pubmed
Branoner,
Semicircular canal-dependent developmental tuning of translational vestibulo-ocular reflexes in Xenopus laevis.
2015,
Pubmed
,
Xenbase
Broussard,
Inputs from the ipsilateral and contralateral vestibular apparatus to behaviorally characterized abducens neurons in rhesus monkeys.
1995,
Pubmed
Büttner-Ennever,
Oculomotor system: a dual innervation of the eye muscles from the abducens, trochlear, and oculomotor nuclei.
2002,
Pubmed
Büttner-Ennever,
Motoneurons of twitch and nontwitch extraocular muscle fibers in the abducens, trochlear, and oculomotor nuclei of monkeys.
2001,
Pubmed
Carrascal,
Changes in somatodendritic morphometry of rat oculomotor nucleus motoneurons during postnatal development.
2009,
Pubmed
Chagnaud,
Spinal corollary discharge modulates motion sensing during vertebrate locomotion.
2015,
Pubmed
,
Xenbase
Davis-López de Carrizosa,
Dual encoding of muscle tension and eye position by abducens motoneurons.
2011,
Pubmed
Dean,
Simulated recruitment of medial rectus motoneurons by abducens internuclear neurons: synaptic specificity vs. intrinsic motoneuron properties.
1997,
Pubmed
Delgado-Garcia,
Behavior of neurons in the abducens nucleus of the alert cat--I. Motoneurons.
1986,
Pubmed
Dieringer,
Modification of synaptic input following unilateral labyrinthectomy.
1977,
Pubmed
Dietrich,
Prolonged vestibular stimulation induces homeostatic plasticity of the vestibulo-ocular reflex in larval Xenopus laevis.
2016,
Pubmed
,
Xenbase
Durand,
L-glutamate and N-methyl-D-asparatate actions on membrane potential and conductance of cat abducens motoneurones.
1987,
Pubmed
Durand,
NMDA Actions on Rat Abducens Motoneurons.
1991,
Pubmed
Eberhorn,
Identification of motoneurons supplying multiply- or singly-innervated extraocular muscle fibers in the rat.
2006,
Pubmed
Eberhorn,
Histochemical differences between motoneurons supplying multiply and singly innervated extraocular muscle fibers.
2005,
Pubmed
Edmonds,
Mechanisms of activation of glutamate receptors and the time course of excitatory synaptic currents.
1995,
Pubmed
Gensberger,
Galvanic Vestibular Stimulation: Cellular Substrates and Response Patterns of Neurons in the Vestibulo-Ocular Network.
2016,
Pubmed
,
Xenbase
Goldberg,
Afferent diversity and the organization of central vestibular pathways.
2000,
Pubmed
Hänzi,
Locomotor corollary activation of trigeminal motoneurons: coupling of discrete motor behaviors.
2015,
Pubmed
,
Xenbase
Hänzi,
Developmental changes in head movement kinematics during swimming in Xenopus laevis tadpoles.
2017,
Pubmed
,
Xenbase
Holstein,
Convergence of excitatory and inhibitory hair cell transmitters shapes vestibular afferent responses.
2004,
Pubmed
Holt,
Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons.
1996,
Pubmed
Horn,
The anatomy and physiology of the ocular motor system.
2011,
Pubmed
Jamali,
Strong correlations between sensitivity and variability give rise to constant discrimination thresholds across the otolith afferent population.
2013,
Pubmed
Keifer,
Abducens conditioning in in vitro turtle brain stem without cerebellum requires NMDA receptors and involves upregulation of GluR4-containing AMPA receptors.
2003,
Pubmed
Lahjouji,
Evidence for colocalization of GABA and glycine in afferents to retrogradely labelled rat abducens motoneurones.
1996,
Pubmed
Lambert,
Semicircular canal size determines the developmental onset of angular vestibuloocular reflexes in larval Xenopus.
2008,
Pubmed
,
Xenbase
Lambert,
Gaze stabilization by efference copy signaling without sensory feedback during vertebrate locomotion.
2012,
Pubmed
,
Xenbase
Long,
Effect of 6-cyano-2,3-dihydroxy-7-nitro-quinoxaline (CNQX) on dorsal root-, NMDA-, kainate- and quisqualate-mediated depolarization of rat motoneurones in vitro.
1990,
Pubmed
Lorenzo,
Differential organization of gamma-aminobutyric acid type A and glycine receptors in the somatic and dendritic compartments of rat abducens motoneurons.
2007,
Pubmed
Malinvaud,
Functional organization of vestibular commissural connections in frog.
2010,
Pubmed
Mendell,
The size principle: a rule describing the recruitment of motoneurons.
2005,
Pubmed
Nieto-Gonzalez,
Phasic and tonic firing properties in rat oculomotor nucleus motoneurons, studied in vitro.
2007,
Pubmed
Pastor,
Recruitment order of cat abducens motoneurons and internuclear neurons.
2003,
Pubmed
Pastor,
Discharge characteristics of medial rectus and abducens motoneurons in the goldfish.
1991,
Pubmed
Pfanzelt,
Differential dynamic processing of afferent signals in frog tonic and phasic second-order vestibular neurons.
2008,
Pubmed
Priesol,
Frequency-dependent effects of glutamate antagonists on the vestibulo-ocular reflex of the cat.
2000,
Pubmed
Ramlochansingh,
Efficacy of tricaine methanesulfonate (MS-222) as an anesthetic agent for blocking sensory-motor responses in Xenopus laevis tadpoles.
2014,
Pubmed
,
Xenbase
Rössert,
Cellular and network contributions to vestibular signal processing: impact of ion conductances, synaptic inhibition, and noise.
2011,
Pubmed
Russier,
GABA and glycine co-release optimizes functional inhibition in rat brainstem motoneurons in vitro.
2002,
Pubmed
Schindelin,
Fiji: an open-source platform for biological-image analysis.
2012,
Pubmed
Spencer,
Evidence for glycine as an inhibitory neurotransmitter of vestibular, reticular, and prepositus hypoglossi neurons that project to the cat abducens nucleus.
1989,
Pubmed
Stahl,
Dynamics of abducens nucleus neurons in the awake mouse.
2012,
Pubmed
Sterling,
Anatomy and physiology of goldfish oculomotor system. I. Structure of abducens nucleus.
1977,
Pubmed
Straka,
Rhombomeric organization of vestibular pathways in larval frogs.
2001,
Pubmed
Straka,
Xenopus laevis: an ideal experimental model for studying the developmental dynamics of neural network assembly and sensory-motor computations.
2012,
Pubmed
,
Xenbase
Straka,
Rhombomeric organization of brainstem motor neurons in larval frogs.
1998,
Pubmed
Straka,
Vestibulo-ocular signal transformation in frequency-tuned channels.
2009,
Pubmed
Straka,
Preservation of segmental hindbrain organization in adult frogs.
2006,
Pubmed
Straka,
Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity.
2005,
Pubmed
Straka,
Electrophysiological and pharmacological characterization of vestibular inputs to identified frog abducens motoneurons and internuclear neurons in vitro.
1993,
Pubmed
Straka,
Basic organization principles of the VOR: lessons from frogs.
2004,
Pubmed
Torres-Torrelo,
Modulation of the input-output function by GABAA receptor-mediated currents in rat oculomotor nucleus motoneurons.
2014,
Pubmed
Ugolini,
Horizontal eye movement networks in primates as revealed by retrograde transneuronal transfer of rabies virus: differences in monosynaptic input to "slow" and "fast" abducens motoneurons.
2006,
Pubmed
