Differences in the Structure and Function of the Vestibular Efferent System Among Vertebrates

Abstract

The role of the mammalian vestibular efferent system in everyday life has been a long-standing mystery. In contrast to what has been reported in lower vertebrate classes, the mammalian vestibular efferent system does not appear to relay inputs from other sensory modalities to the vestibular periphery. Furthermore, to date, the available evidence indicates that the mammalian vestibular efferent system does not relay motor-related signals to the vestibular periphery to modulate sensory coding of the voluntary self-motion generated during natural behaviors. Indeed, our recent neurophysiological studies have provided insight into how the peripheral vestibular system transmits head movement-related information to the brain in a context independent manner. The integration of vestibular and extra-vestibular information instead only occurs at next stage of the mammalian vestibular system, at the level of the vestibular nuclei. The question thus arises: what is the physiological role of the vestibular efferent system in mammals? We suggest that the mammalian vestibular efferent system does not play a significant role in short-term modulation of afferent coding, but instead plays a vital role over a longer time course, for example in calibrating and protecting the functional efficacy of vestibular circuits during development and aging in a role analogous the auditory efferent system.

Keywords: efference copy; evolution; multimodal; neural coding; perception; somatosensory; vestibular; visual.

FIGURE 1

(A) of vestibular efferent (red) and afferent (blue) projections across vertebrates including: mammals (squirrel monkey: Goldberg and Fernandez, 1980), birds (pigeon: Eden and Correia, 1981), reptile (lizard: Barbas-Henry and Lohman, 1988), amphibians (toad: Pellegrini et al., 1985), and fish (toadfish: Highstein and Baker, 1986). (B) In mammals, irregular afferents (light blue) typically innervate both type I and II hair cells (i.e., dimorphic afferents), while regular afferent (dark blue) more selectively innervate type II hair cells. Note that the mammalian vestibular efferent system innervates type II hair cells and their afferent bouton endings, as well as the afferent calyces of type I hair cells (Lysakowski and Goldberg, 1997, 2008). In contrast, in lower vertebrates, which do not have hair cells with calyx endings, the vestibular efferent system innervates type II hair cells and, in some species, such as the toadfish (Sans and Highstein, 1984) also their afferent bouton endings [bottom inset, (A)]. (C) Comparison of the population-averaged efferent-mediated responses of irregular vs. regular afferents to electrical microstimulation of central “group-e” neurons (Goldberg and Fernandez, 1980). (D) Efferent-mediated population responses of irregular (left) vs. regular (right) afferents to sustained high amplitude rotation in the canal-null position (Sadeghi et al., 2009). Note, in contrast to their conventional evoked by natural head motion, afferents displayed excitatory responses for stimulation in both directions—termed a type III response. AO, nucleus anterior octavus; LSO, MSO, MT, lateral and medial superior olive and medial nucleus of the trapezoid body; MLF, medial longitudinal fasciculus; IO, inferior olive; S, L, M, superior, lateral and medial superior vestibular nucleus; SO, superior olive; V, trigeminal nucleus; VI, abducens nucleus; VII, facial nucleus.

FIGURE 2

Extra-vestibular sensory systems (somatosensory, visual, auditory) have been reported to alter peripheral vestibular processing in fish and amphibians but not in mammals. Studies that directly recorded from the vestibular efferent pathway (red boxes), vs. those that recorded efferent-mediated effects in vestibular afferents (blue boxes) are shown for studies in fish (A), amphibians (B), and mammals (C). Symbols: up arrows: excitation; down arrows: inhibition; up-down arrows: both excitation and inhibition.

FIGURE 3

Behaviorally-dependent efferent-mediated responses have been reported in fish and amphibians but not in mammals. (A) Left: Inducing a behavioral escape response in a head fixed toadfish activates vestibular efferent neurons. Middle: Behavioral activation of efferents alters vestibular afferent responses to passive whole-body rotation in the head-restrained fish. Right: bar plots comparing effects of electrical efferent stimulation on background and rotation-induced firing of horizontal canal afferents (data replotted from Boyle and Highstein, 1990). (B) Left: Afferent recordings made in a semi-isolated in vitro anaesthetized larval Xenopus preparation, during passive whole-body rotation. Responses to this passive rotation were compared before and during bouts of fictive swimming induced via applied electrical stimulation. Middle: The induction of fictive swimming alters vestibular afferent responses. Right: Bar plots compare the effects of fictive swimming on background and rotation-induced discharges of horizontal canal afferents (data replotted from Chagnaud et al., 2015). (C) Left: Afferent recordings made in rhesus monkeys during active and comparable passive head motion. Middle: Primate afferent responses are the same during active and comparable passive head motion (reviewed in Cullen, 2019). Right: Bar plots compare afferents resting rates and sensitivities in these two conditions (Cullen and Minor, 2002). Note: error bars represent SEM; **P ≤ 0.001 (Wilcoxon signed-rank test).