The vestibular–basal ganglia connection: Balancing motor control

doi:10.1016/j.brainres.2014.11.063

Brain Research

Volume 1597, 9 February 2015, Pages 180-188

https://doi.org/10.1016/j.brainres.2014.11.063 Get rights and content

Highlights

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Connections between the vestibular system and the basal ganglia have been reported.
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A pathway exists from the vestibular nucleus to the striatum via the thalamus.
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The striatum is likely the main input centre for vestibular signals in the basal ganglia.
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The pathway between the vestibular system and striatum contributes to motor control.

Abstract

Connections between the vestibular system and the basal ganglia have been sporadically studied over the last century. Electrophysiological studies of field potentials in animals have shown that most areas of the striatum respond to electrical vestibular stimulation while human studies isolated responses to vestibular stimulation to the putamen of the striatum. Protein studies have shown inconsistent results regarding changes in receptor levels of a number of receptor types. Recent tracer studies identified a pathway between the vestibular nucleus and the striatum via the thalamus, completely bypassing the cortex. Vestibular sensory input is represented in the part of the striatum – the dorsolateral striatum – where fibres from the sensorimotor areas terminate. It is therefore possible that vestibular signals are used together with other sensorimotor inputs in the striatum for body and limb control. The combination of electrophysiological results, changes in protein levels and tracer studies have led to the idea that the dorsolateral striatum is likely to be the main input area for vestibular signals in the basal ganglia and these will have an influence on motor control. This may have clinical implications in the treatment of basal ganglia disorders and other movement disorders.

Introduction

In the last 100 years there has been speculation about connections between the vestibular system and the basal ganglia. Beginning with experiments by Muskens showing degeneration in the globus pallidus following vestibular lesions in cats (Muskens, 1914, Muskens, 1922), the following decades have seen sporadic study of the effects that the vestibular system exerts on the basal ganglia. Traditional thinking followed the idea that these signals were transmitted via neuronal connections through the cortex. Only recently have studies identified a pathway between the vestibular nucleus and the striatum via the thalamus, bypassing the cortex completely (Lai et al., 2000). However, as the basal ganglia is a highly connected area, it is likely to receive vestibular signals from a number of different pathways through regions including the hippocampus (Kelley and Domesick, 1982) and the motor cortex (Garcia-Rill, 1986). More recent studies of the vestibular-basal ganglia connection have focused on the study of behaviours due to vestibular loss, including the well-documented locomotor hyperactivity seen in rats, as well as circling behaviours. This article reviews the current literature on the connections between the vestibular system and the basal ganglia, which suggests that the dorsolateral striatum is the main input site for vestibular signals in the basal ganglia and that these signals contribute to the basal ganglia control of motor behaviours.

Section snippets

The vestibular system

The vestibular system is a sensory system that responds to angular and linear acceleration of the head and plays a vital role in the processing of information about the location and locomotion of an animal. Located in the inner ear, each peripheral vestibular labyrinth sends sensory information via the vestibular nerve to the ipsilateral vestibular nucleus complex (VNC) in the brainstem and the cerebellum. Hair cells in the ampullae of the three semicircular canals (the anterior, posterior, and

The basal ganglia

The basal ganglia are a group of nuclei that constitute one of the fundamental processing components of the brain. The largest nucleus is the striatum, which can be further divided into the caudate nucleus and the putamen. Also included in the basal ganglia are the globus pallidus, the substantia nigra, the subthalamic nucleus and the nucleus accumbens. The major task of the basal ganglia is to integrate sensory, motor, associative and limbic signals to produce context-dependent behaviours (

Vestibular–striatal pathways

Many neuronal pathways between the vestibular system and the basal ganglia have been proposed. Initial studies into the connection between the vestibular system and the basal ganglia were performed by Muskens in 1922. Using the Marchi technique, lesioning of the vestibular nuclei resulted in degradation of the neurons from the site of damage to the thalamus and neurons in the globus pallidus. Muskens took this to be evidence of a polysynaptic pathway to the basal ganglia that bypassed the

Vestibular signals in the basal ganglia

Responses to vestibular signals have been recorded in specific regions of the basal ganglia. Electrical stimulation of the vestibular nerve causes field potentials in the head of the caudate nucleus in anesthetised cats and squirrel monkeys (see Fig. 2) (Potegal et al., 1971, Liedgren and Schwarz, 1976). Signals in the caudate nucleus were also seen in response to electrical stimulation of the lateral and medial vestibular nuclei in cats (Spiegel et al., 1965). Segundo and Machne (1956) found

Neurochemical changes in the basal ganglia in response to changes in vestibular signalling

The location of vestibular signals in the striatum is supported by changes in the expression of c-fos protein following unilateral vestibular loss in rats. The striatum shows increases in c-fos mRNA and c-fos protein levels bilaterally in the putamen and caudate nucleus 3 h following unilateral vestibular deafferentation (UVD), compared to control rats (Cirelli et al., 1996). The change is transient and the levels return to normal by 6 h. No change is seen in the globus pallidus or the nucleus

Implications of vestibular–basal ganglia links

The current literature supports the idea that the striatum, in particular the putamen, is the main input station for vestibular information in the basal ganglia and this may have clinical implications in the treatment of basal ganglia disorders and other movement disorders. The location of vestibular sensory representation in the striatum, described by Lai et al. (2000), the dorsolateral striatum, has been shown to be the site where fibres from the sensorimotor areas terminate (McGeorge and

Acknowledgments

The authors would like to thank Assoc. Prof. John Reynolds for critical comments on the manuscript. LS was supported by a University of Otago PhD Scholarship.

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ReviewThe vestibular–basal ganglia connection: Balancing motor control

Highlights

Abstract

Introduction

Section snippets

The vestibular system

The basal ganglia

Vestibular–striatal pathways

Vestibular signals in the basal ganglia

Neurochemical changes in the basal ganglia in response to changes in vestibular signalling

Implications of vestibular–basal ganglia links

Acknowledgments

Toxicol. Appl. Pharmacol.

Neuroscience

Neurobiol. Learn. Mem.

Prog. Neurobiol.

Neuroscience

Trends Neurosci.

Neuroimage

Neuroscience

Neuroscience

Brain Res. Rev.

Brain Res.

Brain Res.

Neuroimage

Neuroscience

Brain Res.

Brain Res.

Toxicol. Appl. Pharmacol.

Neuroscience

Brain Res.

Neuron

Neuroscience

Trends Neurosci.

Pharmacol. Biochem. Behav.

Behav. Brain Res.

Exp. Neurol.

Neuron

Neuroscience

Brain Res.

Prog. Neurobiol.

Behav. Brain Res.

Toxicol. Appl. Pharmacol.

Parallel organization of functionally segregated circuits linking basal ganglia and cortex

Annu. Rev. Neurosci.

A causative link between inner ear defects and long-term striatal dysfunction

Science

The role of the substantia nigra in posture control

Eur. J. Neurosci.

Animal models of Parkinson׳s disease

Bioessays

Identification of the central vestibular projections in man: a positron emission tomography activation study

Exp. Brain Res.

Vestibulopathic gait: you׳re better off running than walking

Curr. Opin. Neurol.

You are better off running than walking with acute vestibulopathy

Lancet

Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans

Brain

Evidence for genetically mediated dysfunction of the central dopaminergic system in the stargazer rat

Psychopharmacology (Berl.)

A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem

J. Neurosci.

Interaction of brain areas of visual and vestibular simultaneous activity with fMRI

Exp. Brain Res.

Cortical projection of peripheral vestibular signaling

J. Neurophysiol.

Vestibular critical period, maturation of central vestibular neurons, and locomotor control

Ann. N. Y. Acad. Sci.

The intralaminar thalamus—an expressway linking visual stimuli to circuits determining agency and action selection

Front. Behav. Neurosci.

The localization of vestibular efferent neurons in the kitten with horseradish peroxidase

Acta Otolaryngol.

Review
The vestibular–basal ganglia connection: Balancing motor control