Functional organization of vestibular commissural connections in frog

Abstract

Central vestibular neurons receive substantial inputs from the contralateral labyrinth through inhibitory and excitatory brainstem commissural pathways. The functional organization of these pathways was studied by a multi-methodological approach in isolated frog whole brains. Retrogradely labeled vestibular commissural neurons were primarily located in the superior vestibular nucleus in rhombomeres 2/3 and the medial and descending vestibular nucleus in rhombomeres 5-7. Restricted projections to contralateral vestibular areas, without collaterals to other classical vestibular targets, indicate that vestibular commissural neurons form a feedforward push-pull circuitry. Electrical stimulation of the contralateral coplanar semicircular canal nerve evoked in canal-related second-order vestibular neurons (2°VN) commissural IPSPs (∼70%) and EPSPs (∼30%) with mainly (∼70%) disynaptic onset latencies. The dynamics of commissural responses to electrical pulse trains suggests mediation predominantly by tonic vestibular neurons that activate in all tonic 2°VN large-amplitude IPSPs with a reversal potential of -74 mV. In contrast, phasic 2°VN exhibited either nonreversible, smallamplitude IPSPs (∼40%) of likely dendritic origin or large-amplitude commissural EPSPs (∼60%). IPSPs with disynaptic onset latencies were exclusively GABAergic (mainly GABAA receptor-mediated) but not glycinergic, compatible with the presence of GABAimmunopositive (∼20%) and the absence of glycine-immunopositive vestibular commissural neurons. In contrast, IPSPs with longer, oligosynaptic onset latencies were GABAergic and glycinergic, indicating that both pharmacological types of local inhibitory neurons were activated by excitatory commissural fibers. Conservation of major morpho-physiological and pharmacological features of the vestibular commissural pathway suggests that this phylogenetically old circuitry plays an essential role for the processing of bilateral angular head acceleration signals in vertebrates. Copyright©2010 the authors.