The Efferent Vestibular System

Holt, Joseph C.; Lysakowski, Anna; Goldberg, Jay M.

doi:10.1007/978-1-4419-7070-1_6

Cited by 40 publications

(67 citation statements)

References 218 publications

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“…Electrical stimulation of the efferent system leads to an increase in firing in mammalian vestibular afferents and calyx units show the largest responses to efferent stimulation (reviewed in Holt et al 2011). ACh is thought to be a major efferent neurotransmitter, but other candidate transmitter molecules include ATP, calcitonin gene-related peptide, opioid peptides, γ-aminobutyric acid, nitric oxide, and dopamine (Drescher et al 2010;Holt et al 2011).…”

Section: Is I H Modulated By Efferent Neurotransmitters?mentioning

confidence: 99%

Hyperpolarization-Activated Current (I h) in Vestibular Calyx Terminals: Characterization and Role in Shaping Postsynaptic Events

Meredith

Benke

Rennie

2012

JARO

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Calyx afferent terminals engulf the basolateral region of type I vestibular hair cells, and synaptic transmission across the vestibular type I hair cell/calyx is not well understood. Calyces express several ionic conductances, which may shape postsynaptic potentials. These include previously described tetrodotoxin-sensitive inward Na + currents, voltage-dependent outward K + currents and a K(Ca) current. Here, we characterize an inwardly rectifying conductance in gerbil semicircular canal calyx terminals (postnatal days 3-45), sensitive to voltage and to cyclic nucleotides. Using whole-cell patch clamp, we recorded from isolated calyx terminals still attached to their type I hair cells. A slowly activating, noninactivating current (I h ) was seen with hyperpolarizing voltage steps negative to the resting potential. External Cs + (1-5 mM) and ZD7288 (100 μM) blocked the inward current by 97 and 83 %, respectively, confirming that I h was carried by hyperpolarization-activated, cyclic nucleotide gated channels. Mean half-activation voltage of I h was −123 mV, which shifted to −114 mV in the presence of cAMP. Activation of I h was well described with a third order exponential fit to the current (mean time constant of activation, τ, was 190 ms at −139 mV). Activation speeded up significantly (τ0136 and 127 ms, respectively) when intracellular cAMP and cGMP were present, suggesting that in vivo I h could be subject to efferent modulation via cyclic nucleotide-dependent mechanisms. In current clamp, hyperpolarizing current steps produced a time-dependent depolarizing sag followed by either a rebound afterdepolarization or an action potential. Spontaneous excitatory postsynaptic potentials (EPSPs) became larger and wider when I h was blocked with ZD7288. In a three-dimensional mathematical model of the calyx terminal based on HodgkinHuxley type ionic conductances, removal of I h similarly increased the EPSP, whereas cAMP slightly decreased simulated EPSP size and width.

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Section: Is I H Modulated By Efferent Neurotransmitters?mentioning

confidence: 99%

Hyperpolarization-Activated Current (I h) in Vestibular Calyx Terminals: Characterization and Role in Shaping Postsynaptic Events

Meredith

Benke

Rennie

2012

JARO

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“…Efferent terminals not on the hair cells but on their auditory afferents, and possibly excitatory effects of efferent activity mediated by noncholinergic transmitters, appear to be later developments of the mammalian cochlea only [Köppl, 2011;Sewell, 2011]. In contrast, effects of efferent activity in the vestibular system are more varied all across the vertebrates and are typically mediated by both axosomatic contacts on the hair cells and by axodendritic contacts on their afferents [Eatock and Songer, 2011;Holt et al, 2011]. There is evidence for both nicotinic and muscarinic acetylcholine receptor subtypes being involved and both types can result in inhibition or excitation, depending on the downstream conductances that are activated [Holt et al, 2011;Li and Correia, 2011].…”

Section: Effects Of Efferent Activity At the Cellular Levelmentioning

confidence: 99%

“…This observation gains further significance when compared to the very different and highly derived efferent innervation patterns in archosaurs and mammals. Although very likely independently derived, both archosaurs and mammals are characterized by a strict separation of efferent neurons synapsing in vestibular end organs on the one hand and in the auditory basilar papilla or organ of Corti on the other [Holt et al, 2011;Köppl, 2011]. Furthermore, efferent neuron numbers have multiplied to several hundred vestibular and typically even more auditory efferents.…”

Section: A Brief Overview Of Octavolateral Efferent Innervation Pattementioning

confidence: 99%

“…It is mediated by nicotinic, heteromeric α 9/10 receptors that allow calcium entry into the hair cell. These ions, in turn, activate SK2-type potassium channels that hyperpolarize the cell membrane [Holt et al, 2011;Katz et al, 2011]. In the auditory system, this inhibitory action on hair cells is the dominant and presumed plesiomorphic condition.…”

Section: Effects Of Efferent Activity At the Cellular Levelmentioning

confidence: 99%

“…We focus on typical patterns and evolutionary trends, and refer to more in-depth recent summaries for details [Holt et al, 2011;Köppl, 2011]. The plesiomorphic condition is a highly divergent pattern in which typically a few tens of octavolateral efferent neurons located on each side of the hindbrain send profusely branching axon collaterals to many hair cell end organs.…”

Section: A Brief Overview Of Octavolateral Efferent Innervation Pattementioning

confidence: 99%

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Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Sienknecht¹,

Köppl²,

Fritzsch

2014

Brain Behav Evol

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The function of the inner ear critically depends on mechanoelectrically transducing hair cells and their afferent and efferent innervation. The first part of this review presents data on the evolution and development of polarized vertebrate hair cells that generate a sensitive axis for mechanical stimulation, an essential part of the function of hair cells. Beyond the cellular level, a coordinated alignment of polarized hair cells across a sensory epithelium, a phenomenon called planar cell polarity (PCP), is essential for the organ's function. The coordinated alignment of hair cells leads to hair cell orientation patterns that are characteristic of the different sensory epithelia of the vertebrate inner ear. Here, we review the developmental mechanisms that potentially generate molecular and morphological asymmetries necessary for the control of PCP. In the second part, this review concentrates on the evolution, development and function of the enigmatic efferent neurons terminating on hair cells. We present evidence suggestive of efferents being derived from motoneurons and synapsing predominantly onto a unique but ancient cholinergic receptor. A review of functional data shows that the plesiomorphic role of the efferent system likely was to globally shut down and protect the peripheral sensors, be they vestibular, lateral line or auditory hair cells, from desensitization and damage during situations of self-induced sensory overload. The addition of a dedicated auditory papilla in land vertebrates appears to have favored the separation of vestibular and auditory efferents and specializations for more sophisticated and more diverse functions.

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Aged mice are less susceptible to motion sickness and show decreased efferent vestibular activity compared to young adults

Lőrincz

Drury

et al. 2023

Brain and Behavior

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IntroductionThe efferent vestibular system (EVS) is a feedback circuit thought to modulate vestibular afferent activity by inhibiting type II hair cells and exciting calyx‐bearing afferents in the peripheral vestibular organs. In a previous study, we suggested EVS activity may contribute to the effects of motion sickness. To determine an association between motion sickness and EVS activity, we examined the effects of provocative motion (PM) on c‐Fos expression in brainstem efferent vestibular nucleus (EVN) neurons that are the source of efferent innervation in the peripheral vestibular organs.Methodsc‐Fos is an immediate early gene product expressed in stimulated neurons and is a well‐established marker of neuronal activation. To study the effects of PM, young adult C57/BL6 wild‐type (WT), aged WT, and young adult transgenic Chat‐gCaMP6f mice were exposed to PM, and tail temperature (Ttail) was monitored using infrared imaging. After PM, we used immunohistochemistry to label EVN neurons to determine any changes in c‐Fos expression. All tissue was imaged using laser scanning confocal microscopy.ResultsInfrared recording of Ttail during PM indicated that young adult WT and transgenic mice displayed a typical motion sickness response (tail warming), but not in aged WT mice. Similarly, brainstem EVN neurons showed increased expression of c‐Fos protein after PM in young adult WT and transgenic mice but not in aged cohorts.ConclusionWe present evidence that motion sickness symptoms and increased activation of EVN neurons occur in young adult WT and transgenic mice in response to PM. In contrast, aged WT mice showed no signs of motion sickness and no change in c‐Fos expression when exposed to the same provocative stimulus.

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The Efferent Vestibular System

Cited by 40 publications

References 218 publications

Hyperpolarization-Activated Current (I h) in Vestibular Calyx Terminals: Characterization and Role in Shaping Postsynaptic Events

Hyperpolarization-Activated Current (I h) in Vestibular Calyx Terminals: Characterization and Role in Shaping Postsynaptic Events

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Aged mice are less susceptible to motion sickness and show decreased efferent vestibular activity compared to young adults

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