Histochemical Characterization of the Vestibular Y-Group in Monkey

Christina Zeeh,Ümit S Mayadali,Anja K.E Horn

doi:10.1007/s12311-020-01200-z

Christina Zeeh, Ümit S Mayadali + Show 1 more

Open Access

https://doi.org/10.1007/s12311-020-01200-z

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Abstract

The Y-group plays an important role in the generation of upward smooth pursuit eye movements and contributes to the adaptive properties of the vertical vestibulo-ocular reflex. Malfunction of this circuitry may cause eye movement disorders, such as downbeat nystagmus. To characterize the neuron populations in the Y-group, we performed immunostainings for cellular proteins related to firing characteristics and transmitters (calretinin, GABA-related proteins and ion channels) in brainstem sections of macaque monkeys that had received tracer injections into the oculomotor nucleus. Two histochemically different populations of premotor neurons were identified: The calretinin-positive population represents the excitatory projection to contralateral upgaze motoneurons, whereas the GABAergic population represents the inhibitory projection to ipsilateral downgaze motoneurons. Both populations receive a strong supply by GABAergic nerve endings most likely originating from floccular Purkinje cells. All premotor neurons express nonphosphorylated neurofilaments and are ensheathed by strong perineuronal nets. In addition, they contain the voltage-gated potassium channels Kv1.1 and Kv3.1b which suggests biophysical similarities to high-activity premotor neurons of vestibular and oculomotor systems. The premotor neurons of Y-group form a homogenous population with histochemical characteristics compatible with fast-firing projection neurons that can also undergo plasticity and contribute to motor learning as found for the adaptation of the vestibulo-ocular reflex in response to visual-vestibular mismatch stimulation. The histochemical characterization of premotor neurons in the Y-group allows the identification of the homologue cell groups in human, including their transmitter inputs and will serve as basis for correlated anatomical-neuropathological studies of clinical cases with downbeat nystagmus.

Highlights

The Y-group plays an important role in the generation of smooth pursuit eye movements [1], but is involved in the adaptive properties of the vertical vestibuloocular reflex (VOR) for example in response to mismatch of visual and vestibular input by wearing optical devices, or in Christina Zeeh and Ümit S
Two histochemically different populations of premotor neurons projecting to the nIII were identified in Yd: The CRpositive population represents the excitatory projection to contralateral upgaze motoneurons, whereas the glutamate decarboxylase (GAD)-positive population represents the inhibitory projection to ipsilateral downgaze motoneurons
Both populations receive a strong GABAergic input from floccular Purkinje cells indicating that all premotor neurons in Yd represent floccular target neurons’ (FTN)

Summary

Introduction

The Y-group plays an important role in the generation of smooth pursuit (upward) eye movements [1], but is involved in the adaptive properties of the vertical vestibuloocular reflex (VOR) for example in response to mismatch of visual and vestibular input by wearing optical devices, or in Christina Zeeh and Ümit S. VOR suppression during combined eye-head tracking [2, 3]. Recording studies in monkey revealed a rather uniform neuron population in the Y-group that modulated in phase with eye velocity during visual following, modulated in phase with head velocity during VOR suppression, but did not modulate during the VOR in darkness [4]. The Y-group is part of a circuitry that uses vestibular and visual signals mediated by the cerebellar flocculus to control eye movements. Malfunction of this circuitry may cause eye movement disorders, such as downbeat nystagmus seen after floccular lesions [5]

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