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The Journal of Neuroscience, October 8, 2008, 28(41):10349-10362; doi:10.1523/JNEUROSCI.3368-08.2008
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Behavioral/Systems/Cognitive
Differential Dynamic Processing of Afferent Signals in Frog Tonic and Phasic Second-Order Vestibular Neurons
Sandra Pfanzelt,1,2 Christian Rössert,2 Martin Rohregger,3 Stefan Glasauer,2 Lee E. Moore,1 andHans Straka1 1Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, UMR 7060, Université Paris Descartes, 75270 Paris Cedex 06, France, 2Department of Neurology, Bernstein Center for Computational Neuroscience, Ludwig-Maximilians-Universität München, 81377 Munich, Germany, and 3Department of Physiology, Ludwig-Maximilians-Universität München, 80336 Munich, Germany
Correspondence should be addressed to Dr. Hans Straka, Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, UMR 7060, Université Paris Descartes, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France. Email: hans.straka{at}univ-paris5.fr
The sensory–motor transformation of the large dynamic spectrum of head-motion-related signals occurs in separate vestibulo-ocular pathways. Synaptic responses of tonic and phasic second-order vestibular neurons were recorded in isolated frog brains after stimulation of individual labyrinthine nerve branches with trains of single electrical pulses. The timing of the single pulses was adapted from spike discharge patterns of frog semicircular canal nerve afferents during sinusoidal head rotation. Because each electrical pulse evoked a single spike in afferent fibers, the resulting sequences with sinusoidally modulated intervals and peak frequencies up to 100 Hz allowed studying the processing of presynaptic afferent inputs with in vivo characteristics in second-order vestibular neurons recorded in vitro in an isolated whole brain. Variation of pulse-train parameters showed that the postsynaptic compound response dynamics differ in the two types of frog vestibular neurons. In tonic neurons, subthreshold compound responses and evoked discharge patterns exhibited relatively linear dynamics and were generally aligned with pulse frequency modulation. In contrast, compound responses of phasic neurons were asymmetric with large leads of subthreshold response peaks and evoked spike discharge relative to stimulus waveform. These nonlinearities were caused by the particular intrinsic properties of phasic vestibular neurons and were facilitated by GABAergic and glycinergic inhibitory inputs from tonic type vestibular interneurons and by cerebellar circuits. Coadapted intrinsic filter and emerging network properties thus form dynamically different neuronal elements that provide the appropriate cellular basis for a parallel processing of linear, tonic, and nonlinear phasic vestibulo-ocular response components in central vestibular neurons.
Key words: semicircular canal; phasic; tonic; afferent fibers; vestibular; macula
Received July 8, 2008; revised Aug. 22, 2008; accepted Aug. 28, 2008.
Correspondence should be addressed to Dr. Hans Straka, Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, UMR 7060, Université Paris Descartes, 45 rue des Saints-Pères, 75270 Paris Cedex 06, France. Email: hans.straka{at}univ-paris5.fr
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[Abstract] [Full Text] [PDF]
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