Electrophysiological properties of morphologically-identified medial vestibular nucleus neurons projecting to the abducens nucleus in the chick embryo

Abstract

Neurons in the medial vestibular nucleus (MVN) show a wide range of axonal projection pathways, intrinsic firing properties, and responses to head movements. To determine whether MVN neurons participating in the vestibulocular reflexes (VOR) have distinctive electrophysiological properties related to their output pathways, a new preparation was devised using transverse brain slices containing the chicken MVN and abducens nucleus. Biocytin Alexa Fluor was injected extracellularly into the abducens nucleus so that MVN neurons whose axons projected to the ipsilateral (MVN/ABi) and contralateral (MVN/ABc) abducens nuclei were labeled selectively. Whole-cell, patch-clamp recordings were performed to study the active and passive membrane properties, sodium conductances, and spontaneous synaptic events in morphologically-identified MVN/AB neurons and compare them to MVN neurons whose axons could not be traced (MVN/n). Located primarily in the rostral half of the ventrolateral part of the MVN, MVN/AB neurons mainly have stellate cell bodies with diameters of 20-25 μm. Compared to MVNn neurons, MVN/ABi and MVN/ABc neurons had lower input resistances. Compared to all other MVN neuron groups studied, MVN/ABc neurons showed unique firing properties, including type A-like waveform, silence at resting membrane potential, and failure to fire repetitively on depolarization. It is interesting that the frequency of spontaneous excitatory and inhibitory synaptic events was similar for all the MVN neurons studied. However, the ratio for miniature to spontaneous inhibitory events was significantly lower for MVN/ABi neurons compared to MVN/n neurons, suggesting that MVN/ABi neurons retained a larger number and/or more active inhibitory presynaptic neurons within the brain slices. Also, MVN/ABi neurons had mEPSCs with slower decay time and half width compared to MVN/n neurons. Altogether, these findings underscore the diversity of electrophysiological properties of MVN neuron classes distinguished by axonal projection pathways. This represents the first study of MVN/AB neurons in brain slice preparations and supports the concept that the in vitro brain slice preparation provides an advantageous model to investigate the cellular and molecular events in vestibular signal processing.

Reconsidering the Role of Neuronal Intrinsic Properties and Neuromodulation in Vestibular Homeostasis

“…This synaptic uncoupling can be achieved by modifying the artificial cerebro-spinal fluid (ACSF), e.g., with high Mg 2+ /low Ca 2+ ACSF (Vibert et al, 2000 ; Darlington et al, 2002 ), or with a cocktail of synaptic blockers (Ris et al, 2001a ; Guilding and Dutia, 2005 ) as well as by complete isolation from other structures (Darlington and Smith, 2000 ). The 2° VN intrinsic properties, and in particular those of neurons from the medial vestibular nucleus, have been described in many Vertebrates, including Rats (Gallagher et al, 1985 ; Johnston et al, 1994 ), Mice (Dutia et al, 1995 ; Johnston and Dutia, 1996 ), Guinea pigs (Serafin et al, 1991a , b ), Amphibians (Straka et al, 2004 ), and Chicks (du Lac and Lisberger, 1995 ; Gottesman-Davis and Peusner, 2010 ; Gottesman-Davis et al, 2011 ). In all Vertebrates, medial 2° VN form a heterogeneous population dominated by tonic and phasic neurons (Straka et al, 2005 ; Eugène et al, 2007 ; Grassi et al, 2009 ; Camp et al, 2010 ).…”

Muscarinic receptor subtypes differentially control synaptic input and excitability of cerebellum‐projecting medial vestibular nucleus neurons

“…The MVN is highly heterogeneous and contains inhibitory and excitatory interneurons as well as projection neurons (Gottesman‐Davis et al . ; Kolkman et al . ).…”

Plasticity of spontaneous excitatory and inhibitory synaptic activity in morphologically defined vestibular nuclei neurons during early vestibular compensation

“…To characterize changes in signal processing after lesions, it is helpful to select a neuron subset with a known output target, since vestibular nuclei neurons with different axonal projections show diverse spike discharge patterns (Goldberg 2000;Sekirnjak and du Lac 2006;Gottesman-Davis et al 2011;Kolkman et al 2011) and neurotransmitter phenotypes, with glutamate, glycine, and GABA predominating (Spencer et al 1989;Takazawa et al 2004;Gittis and du Lac 2007). Furthermore, in other sensory systems, the response of morphologically defined neuron subsets to deafferentation depends on their role in the network (e.g., Francis and Manis 2000;Li et al 2009;Zhou et al 2009).…”