Reverse Engineering the Vestibular System: Intrinsic and Synaptic Contribution to Signal Processing in Frog Central Vestibular Neurons

Head motion-related sensory signals are transformed by second-order vestibular neurons (2°VN) into appropriate extraocular motor commands for retinal image stabilization during body motion. In frog, these 2°VN form two distinct subpopulations that have either linear (tonic 2°VN) or highly non-linear intrinsic properties (phasic 2°VN), compatible with lowpass and band-pass filter characteristics, respectively. In the present study, available physiological data on cellular properties of 2°VN have been used to construct conductancebased spiking cellular models that were fine-tuned by fitting to spike-frequency data. The obtained results of this approach suggest that the differential response characteristics of the two vestibular subtypes are mainly caused by a single additional potassium channel that is low-threshold and voltage-dependent in phasic and spike-dependent in tonic 2°VN. The insertion of phasic 2°VN into a local feed-forward inhibitory network was used to develop a cellular model with conductance-based synapses that allows simulation of the emerging properties of this network. This approach reveals the relative contributions of intrinsic and synaptic factors on afferent signal processing in phasic 2°VN. Extension of the single cell model to a population model allowed further testing under more natural conditions including asynchronous afferent labyrinthine input and synaptic noise. This latter approach indicated that the feed-forward inhibition from the local inhibitory network acts as a high-pass filter, which reinforces the impact of the intrinsic membrane properties of phasic 2°VN on peak response timing. Moreover, the model suggests that synaptic noise and postsynaptic properties of the target neurons critically influence the dynamics of vestibulo-motor