Second-Order Vestibular Neurons Form Separate Populations With Different Membrane and Discharge Properties

Abstract

Straka, H., M. Beraneck, M. Rohregger, L. E. Moore, P.-P, Vidal, and N. Vibert. Second-order vestibular neurons form separate populations with different membrane and discharge properties. J Neurophysiol 92: 845-861, 2004. First published March 24, 2004 10.1152/ jn.00107.2004. Membrane and discharge properties were determined in second-order vestibular neurons (2°VN) in the isolated brain of grass frogs. 2°VN were identified by monosynaptic excitatory postsynaptic potentials after separate electrical stimulation of the utricular nerve, the lagenar nerve, or individual semicircular canal nerves. 2°VN were classified as vestibulo-ocular or -spinal neurons by the presence of antidromic spikes evoked by electrical stimulation of the spinal cord or the oculomotor nuclei. Differences in passive membrane properties, spike shape, and discharge pattern in response to current steps and ramp-like currents allowed a differentiation of frog 2°VN into two separate, nonoverlapping types of vestibular neurons. A larger subgroup of 2°VN (78%) was characterized by brief, high-frequency bursts of up to five spikes and the absence of a subsequent continuous discharge in response to positive current steps. In contrast, the smaller subgroup of 2°VN (22%) exhibited a continuous discharge with moderate adaptation in response to positive current steps. The differences in the evoked spike discharge pattern were paralleled by differences in passive membrane properties and spike shapes. Despite these differences in membrane properties, both types, i.e., phasic and tonic 2°VN, occupied similar anatomical locations and displayed similar afferent and efferent connectivities. Differences in response dynamics of the two types of 2°VN match those of their pre-and postsynaptic neurons. The existence of distinct populations of 2°VN that differ in response dynamics but not in the spatial organization of their afferent inputs and efferent connectivity to motor targets suggests that frog 2°VN form one part of parallel vestibulomotor pathways.

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).…”

“…The functioning of the vestibular system critically depends on the range of head movements produced during locomotion (Straka et al, 2004; Beraneck and Straka, 2011). The synaptic and intrinsic properties of 2° VN are co-adapted and match these behavioral requirements.…”

Ontogenetic Development of Vestibulo-Ocular Reflexes in Amphibians

“…With respect to various morpho-physiological properties such as resting discharge rate and regularity, afferent fibers of both larval (Gensberger et al, 2016) and adult frogs (Honrubia et al, 1989) form a broad spectrum. Despite the apparent continuum of distinguishing features, afferent fibers in Xenopus tadpoles segregate into two distinct categorical groups (Gensberger et al, 2015) with physiological characteristics, reminiscent of phasic and tonic 2°VN of adult frogs (Straka et al, 2004). The obvious duality of the vestibular afferent population in Xenopus larvae complies with a separation into frequency-tuned pathways as a major organizational principle of the VOR (Straka et al, 2009) and its implementation already early after hatching.…”

The Frog Vestibular System as a Model for Lesion-Induced Plasticity: Basic Neural Principles and Implications for Posture Control

“…In contrast, changes in intrinsic membrane properties of vestibular neurons after a loss of one labyrinth as shown in guinea pig (Beraneck et al, 2003, 2004) have so far not been reported in frog. However, this is not due to a general absence of such a plasticity phenomenon in frog, but rather due to the lack of respective studies that compare known intrinsic neuronal properties of frog tonic and phasic 2°VN (Straka et al, 2004; Beraneck et al, 2007) before and after the lesion. Assuming the presence of basic reaction mechanisms that only differ in magnitude between different species, a general hypothesis is derived from the results obtained in guinea pigs after UL (Beraneck et al, 2003, 2004).…”