Central vestibular neurons – new insights from modeling at single cell and population levels
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1
Ludwig-Maximilians-Universität, Institute of Clinical Neurosciences, Germany
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2
Ludwig-Maximilians-Universität, Integrated Center for Research and Treatment of Vertigo, Germany
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3
Ludwig-Maximilians-Universität, Department Biologie II, Germany
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4
Ludwig-Maximilians-Universität, Bernstein Center for Computational Neuroscience Munich, Germany
Central vestibular neurons in the brainstem are responsible for the major computational step that transforms head acceleration-related sensory vestibular signals into appropriate extraocular motor commands for retinal image stabilization during locomotion. In frog, these second-order vestibular neurons (2°VN) form two functional subgroups, tonic and phasic neurons, that can be distinguished by their distinctly different firing patterns. While tonic 2°VN exhibit a sustained discharge during constant current injection (class 1 excitability), the evoked discharge in phasic 2°VN is limited to one or a few spikes immediately after stimulus onset (class 3 excitability) (Straka et al. 2004, J. Neurophysiol 92:845-861). This difference is accompanied by differences in the frequency response characteristics. During injection of sinusoidally modulated currents, tonic 2°VN exhibit a low-pass subthreshold response and a band-pass spike discharge with a resonance peak at low frequencies (~ 5 Hz). In contrast, phasic 2°VN show band-pass characteristics in their subthreshold response as well as spike discharge with a resonance peak at higher frequencies (~ 30 Hz) (Beraneck et al. 2007, J. Neurosci 27:4283-4296).
During the activation of vestibular nerve afferent fibers with sinusoidally modulated pulse trains, the compound excitatory postsynaptic potential (EPSP) is characterized by a response peak that advances stimulus peak frequency and spikes are triggered only by the first few pulses of the stimulus train. In contrast, the subthreshold compound EPSP and the spike response frequency of tonic 2°VN are approximately aligned with the waveform of the stimulus frequency modulation. Physio-pharmacological analyses and modeling indicated that phasic 2°VN are embedded in a local network that causes a disynaptic feed-forward inhibition thereby contributing to the pronounced asymmetry of the response peak. However, the relative contributions of intrinsic and network properties to the differential discharge behavior of tonic and phasic 2°VN remain unknown. (Biesdorf et al. 2008, J. Neurophysiol 99:1758-1769; Pfanzelt et al. 2008, J. Neurosci. 28:10349-10362)
In the present study, available data on cellular properties of frog 2°VN have been used to create conductance-based cellular models that were fine-tuned by fitting to spike-frequency data. This modeling approach suggests that the distinct intrinsic characteristics of 2°VN are caused by a single additional potassium channel that is low-threshold and voltage-dependent in phasic 2°VN and spike-dependent in tonic 2°VN. By extending the intracellular models with conductance-based excitatory synapses and an inhibitory side-loop in phasic 2°VN, the relative contributions of intrinsic and synaptic properties on signal processing in 2°VN were revealed. Furthermore the cellular models were scaled to a population model. As a measure for frequency sensitivity, the theoretical post-synaptic conductance generated by the two populations was computed. Testing the population model with natural stimuli including asynchronous synaptic inputs from afferent fibers and synaptic noise revealed that the feed-forward inhibition in phasic 2°VN forms a high-pass filter that reinforces the intrinsic membrane properties in the latter vestibular neuronal subtype. In addition, the model suggests that noise and post-synaptic integration critically influence the effective signal transmission behavior, particularly in phasic 2°VN.
Acknowledgements
Funded by DFG (GRK 1091) and BMBF (BCCN 01GQ0440, IFB 01EO0901).
Keywords:
computational neuroscience
Conference:
Bernstein Conference on Computational Neuroscience, Berlin, Germany, 27 Sep - 1 Oct, 2010.
Presentation Type:
Poster Abstract
Topic:
Bernstein Conference on Computational Neuroscience
Citation:
Rössert
C,
Straka
H and
Glasauer
S
(2010). Central vestibular neurons – new insights from modeling at single cell and population levels.
Front. Comput. Neurosci.
Conference Abstract:
Bernstein Conference on Computational Neuroscience.
doi: 10.3389/conf.fncom.2010.51.00098
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Received:
09 Sep 2010;
Published Online:
23 Sep 2010.
*
Correspondence:
Mr. Christian Rössert, Ludwig-Maximilians-Universität, Institute of Clinical Neurosciences, Munich, Germany, christian.a@roessert.de