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I ANATOMY                 

III EXAMINATION: EYE MOVEMENTS & NYSTAGMUS 

IV FIXATION INSTABILITY

V SUPRANUCLEAR to NUCLEAR   

VI VESTIBULAR SYSTEM  

VII CEREBELLAR EYE MOVEMENTS    

VIII CN PALSIES, VISUAL FIELDS, PUPIL & THE EYE

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The afferent fibres of the vestibular component of the VIII nerve carry signals from the receptor cells of the cristae and otolith organs to the vestibular nuclei.  Thousands of axons of primary vestibular neurons enter each side of the brain stem to innervate second-order neurons in the vestibular nuclei, which consist of four distinct groups, and are located at the medullary-pontine junction at the floor of the fourth ventricle.  

These vestibular primary afferent neurons discharge spontaneously at rest when no stimulus is applied. Spontaneous discharge rates vary across species, ranging from as low as 13 spikes per second in a stingray, to a high of 115 spikes per second in macaque monkeys. In primates, since afferent vestibular neurons are characterized by their high level of spontaneous activity, the nuclei receive about 100 action potentials/nerve fibre/sec.
In humans, since each vestibular nerve has approximately 15,000 fibers, more than 1.5 million action potentials are received every second from the vestibular organs alone. Each fiber usually supplies a restricted number of secondary neurons in all four of the vestibular nuclei. There are clear separations of afferent fibers such that specific areas in each nucleus preferentially receive afferents from specific receptors of the vestibular apparatus.

Of importance, from its baseline firing rate of 100 Hz, firing in the vestibular nerve can be excited, nearly without limit, but can be inhibited only to zero.

The main vestibular nuclei are:

Figure 1. Distribution of primary vestibular afferent fibres (shaded blue) within the vestibular nucleus. 
         
         Left: superior vestibular nerve. AC, HC: Anterior (Superior) and Horizontal Canals; UT: Utricle
                   Right:inferior vestibular nerve. PC: Posterior Horizontal Canal; SA: Saccule


 The medial vestibular nucleus receives inputs mostly from the horizontal semicircular canals.
 The superior vestibular nucleus receives inputs mostly from the vertical semicircular canals.
 Most neurons in the vestibular nuclei receive convergent inputs from the otolith end organs and semicircular canals1.

 

 

Figure 2. Connections between the semicircular canals and otolith organs, illustrating output to oculomotor neurons:


 

 

 

Connections to the vestibular nuclei:

Semicircular Canals

Most of the primary afferent projections to the superior vestibular nucleus come from the cristae of the semicircular canals. 

Cerebellum

Figure 3. The vesibular system receives inputs from multiple regions:

 

The vestibular nuclei receive not only vestibulo-ocular signals, but also information related to other eye movements: pursuit, saccades, and optokinetic nystagmus.  In turn, the vestibular nuclei project directly to extraocular motor neurons2.

From: Cullen KE. Physiology of central pathways. Handb Clin Neurol. 2016;137:17-40.

 

The vestibular nuclei receive convergent motion information from the opposite ear through an inhibitory commissural pathway that uses GABA as a neurotransmitter3.   The commissural pathway is highly organized so that cells which receive horizontal excitatory canal signals from the ipsilateral ear will also receive contralateral inhibitory horizontal canal signals from the opposite ear. The majority of the commissural fibres originate in the medial vestibular nucleus.
This set-up gives rise to a “push-pull” vestibular function, whereby directional sensitivity to head movement is coded by opposing receptor signals. Because vestibular nuclei neurons receive information from bilateral inner ear receptors and because they maintain a high spontaneous firing rate, it is likely that they compare the relative discharge rates of left vs. right canal afferent firing activity.

For example, during a leftward head turn, nuclei in the left brainstem nuclei  receive high firing-rate information from the left horizontal canal and low firing-rate information from the right horizontal canal. The comparison of activity is interpreted as a left head turn. Similar responses exist when the head is pitched or rolled, with the vertical semicircular canals being stimulated by the rotational motion in the planes to which they are sensitive. However, the opposing push-pull response from the vertical canals occurs with the anterior semicircular canal of one ear and the posterior semicircular canal of the opposite ear3
Pairing of semicircular canals

Over time the commissural fibers provide vestibular compensation, a process by which the loss of unilateral vestibular receptor function is partially restored centrally and behavioral responses, such as the VOR and postural responses, ultimately recover3.

 

Figure 4. Input to the vestibular nuclei: showing the effect of a head turn to the left on afferent fibre firing rate

Redrawn from: Angelaki D, Dickman JD. The Vestibular System.. Retrieved from https://nobaproject.com/modules/the-vestibular-system#content 

 

Output of the vestibular nuclei

Axons from the neurons in the superior vestibular nucleus run in the ipsilateral and contralateral medial longitudinal fasciculus (MLF) to innervate the motor nuclei of the extrinsic eye muscles. others project to the cerebellum and dorsal pontine reticular formation. Due to its pattern of afferent and efferent connections, the superior vestibular nucleus is a major relay center for ocular reflexes mediated by the semicircular canals.

In the areas that receive primary afferents, signals from the vestibular organs interact with afferent fibers from other systems (visual and proprioceptive) and centers (especially the cerebellum): the emerging picture is a complex one of both separation (channeling) and convergence of afferent signals at the level of the vestibular nuclei4.  Secondary vestibular neurons receive a converging input of afferents from different sensory organs (the semicircular canals and otolith organs from both sides of the head). Conversely, secondary vestibular neurons of the vestibular nuclei project to many areas of the central nervous system, including the oculomotor nuclei, the spinal cord, and the flocculus of the cerebellum, as well as a thalamocortical pathway4.

Figure 5. Central neurons of the vestibular nuclei project to:
                  Upstream structures involved in the computation of self-motion.
                  Neural structures that control eye movements, posture, and balance.

Redrawn from: Cullen KE. The vestibular system: multimodal integration and encoding of self-motion for motor control. Trends Neurosci. 2012;35(3):185-96.

 

Neurons in the vestibular nuclei that receive direct input from the vestibular afferents can be categorized into two main categories:

 i) Neurons that control and modulate the vestibulo-ocular reflex to ensure gaze stability during everyday life:  these are the position-vestibular-pause (PVP) neurons, and the floccular target neurons (FTN).

The majority of vestibulo-ocular reflex (VOR) neurons are PVP neurons; a distinct group of neurons which derive their name from the signals they carry during passive head rotations and eye movements. 

FTNs also contribute to the direct vestibulo-ocular reflex pathway. In particular, FTNs receive input from the flocculus of the cerebellum as well inputs from the vestibular organs. The responses of FTNs complement those of PVP neurons during daily activities, and play an important role in calibrating the vestibulo-ocular reflex to maintain excellent performance in response to the effects of aging as well as changes in environmental requirements, such as those brought about by the corrective lenses worn to correct myopia or during the motor learning required during prism adaptation.

ii) Neurons that control posture and balance, and also project to higher order structures involved in the estimation of self-motion: these are the Vestibular-Only neurons (VO neurons).

Like VOR neurons, VO neurons receive direct inputs from the vestibular nerve. However, these neurons do not project to oculomotor structures, but project to the spinal cord and mediate the vestibulospinal reflexes.
VO neurons also appear to be the source of vestibular input to vestibular-sensitive neurons in thalamus and cortex.

 

References

 

  1. Cullen KE, Sadeghi S(2008) Vestibular system. Scholarpedia, 3(1):3013.
  2. Angelaki, D. E. (2009). Vestibulo-Ocular Reflex. In Encyclopedia of Neuroscience (pp. 139-146). Elsevier Ltd. https://doi.org/10.1016/B978-008045046-9.01107-4
  3. Angelaki D, Dickman JD. The Vestibular System.. Retrieved from https://nobaproject.com/modules/the-vestibular-system#content  
  4. Baloh RW, Kerber, K. Baloh and Honrubia's Clinical Neurophysiology of the Vestibular System. Oxford University Press; 2010.