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The Journal of Neuroscience, April 18, 2007, 27(16):4283-4296; doi:10.1523/JNEUROSCI.5232-06.2007

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Behavioral/Systems/Cognitive
Differential Intrinsic Response Dynamics Determine Synaptic Signal Processing in Frog Vestibular Neurons

Mathieu Beraneck,^1 * Sandra Pfanzelt,^1 * Isabelle Vassias,¹ Martin Rohregger,² Nicolas Vibert,¹ Pierre-Paul Vidal,¹ Lee E. Moore,¹ and Hans Straka¹

¹Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7060, Université Paris Descartes, 75270 Paris cedex 06, France, and ²Department of Physiology, Ludwigs-Maximilians-Universität Munich, 80336 Munich, Germany

Correspondence should be addressed to Dr. H. Straka, Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7060, Université Paris Descartes, 45, rue des Saints-Pères, 75270 Paris cedex 06, France. Email: hans.straka{at}univ-paris5.fr

Central vestibular neurons process head movement-related sensory signals over a wide dynamic range. In the isolated frog whole brain, second-order vestibular neurons were identified by monosynaptic responses after electrical stimulation of individual semicircular canal nerve branches. Neurons were classified as tonic or phasic vestibular neurons based on their different discharge patterns in response to positive current steps. With increasing frequency of sinusoidally modulated current injections, up to 100 Hz, there was a concomitant decrease in the impedance of tonic vestibular neurons. Subthreshold responses as well as spike discharge showed classical low-pass filter-like characteristics with corner frequencies ranging from 5 to 20 Hz. In contrast, the impedance of phasic vestibular neurons was relatively constant over a wider range of frequencies or showed a resonance at 40 Hz. Above spike threshold, single spikes of phasic neurons were synchronized with the sinusoidal stimulation between 20 and 50 Hz, thus showing characteristic bandpass filter-like properties. Both the subthreshold resonance and bandpass filter-like discharge pattern depend on the activation of an I_D potassium conductance. External current or synaptic stimulation that produced impedance increases (i.e., depolarization in tonic or hyperpolarization in phasic neurons) had opposite and complementary effects on the responses of the two types of neurons. Thus, membrane depolarization by current steps or repetitive synaptic excitation amplified synaptic inputs in tonic vestibular neurons and reduced them in phasic neurons. These differential, opposite membrane response properties render the two neuronal types particularly suitable for either integration (tonic neurons) or signal detection (phasic neurons), respectively, and dampens variations of the resting membrane potential in the latter.

Key words: semicircular canal; resonance; potassium; low-pass filter; bandpass filter; frequency-tuned channels

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Received Dec. 4, 2006; revised Feb. 9, 2007; accepted March 9, 2007.

Correspondence should be addressed to Dr. H. Straka, Laboratoire de Neurobiologie des Réseaux Sensorimoteurs, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 7060, Université Paris Descartes, 45, rue des Saints-Pères, 75270 Paris cedex 06, France. Email: hans.straka{at}univ-paris5.fr

This article has been cited by other articles:

				S. Pfanzelt, C. Rossert, M. Rohregger, S. Glasauer, L. E. Moore, and H. Straka Differential Dynamic Processing of Afferent Signals in Frog Tonic and Phasic Second-Order Vestibular Neurons J. Neurosci., October 8, 2008; 28(41): 10349 - 10362. [Abstract] [Full Text] [PDF]

				S. Biesdorf, D. Malinvaud, I. Reichenberger, S. Pfanzelt, and H. Straka Differential Inhibitory Control of Semicircular Canal Nerve Afferent-Evoked Inputs in Second-Order Vestibular Neurons by Glycinergic and GABAergic Circuits J Neurophysiol, April 1, 2008; 99(4): 1758 - 1769. [Abstract] [Full Text] [PDF]

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				M. Beraneck and K. E. Cullen Activity of Vestibular Nuclei Neurons During Vestibular and Optokinetic Stimulation in the Alert Mouse J Neurophysiol, September 1, 2007; 98(3): 1549 - 1565. [Abstract] [Full Text] [PDF]

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