SENSORY MODALITIES OF BALANCE CONTROL
The balance system coordinates compensatory eye, head, and body movements allowing for clear vision with head and body activities, perception of movement and direction, and postural control. The three primary systems that contribute to balance control include vestibular, visual, and somatosensory.
• The vestibular system is an internal sensory reference that provides cues of space perception and both direction and velocity of movement. A central role of this system is to stabilize retinal images during head movements.
• The visual system is an external sensory reference that indicates environmental movement and position.
• The somatosensory system is also an external sensory reference, including both proprioception and kinesthetics that detect changes in the support surface.
Located within the petrous portion of the temporal bone, two labyrinths (bony and membranous) comprises the vestibule, semicircular canals, and cochlea (Baloh & Honrubia, 2001). The bony labyrinth is a hollow chamber that houses the sensory organs for hearing (anterior part) and balance (posterior part). Perilymph fluid fills the space.
The membranous labyrinths (right and left) contain the cochlea and five vestibular organs: the utricle and saccule (otolith organs), and the three semicircular canals (horizontal, anterior/superior, and posterior; Figure 1–1). The vestibular organs contain receptors responsible for sensing both linear (otolith organs) and angular (semicircular canals) acceleration and deceleration. The membranous labyrinth is suspended within the bony labyrinth but is adhered to ligaments, so only the fluid within the membranous labyrinth moves with head and body movements. Endolymph fluid fills the membranous labyrinth. The membranous labyrinth also contains the endolymphatic duct and sac.
Semicircular Canals (SCCs)
Each SCC is positioned orthogonal to one another (at 90° angles) and responsible for converting angular acceleration into electrical code to interpret head and body movements. Vertical SCCs are positioned at 45° angles to the mid-sagittal plane, and horizontal SCCs are pitched upward approximately 30° (Schubert & Shepard, 2016). The SCCs work as functional pairs, concerning parallel planes:
Figure 1–1. The membranous labyrinth and innervation of the labyrinth. From Baloh and Honrubia, 2001, pp. 11, Figure 1–6. Reproduced with permission of the Licensor through PLSclear.
• Right anterior canal and left posterior canal (RALP)
• Left anterior canal and right posterior canal (LARP)
When one SCC of the “functional pair” is excited, the other (paired) canal is inhibited. This push/pull pairing of the canals is necessary for the central nervous system (CNS) to process asymmetrical neural activity and coordinate corresponding motor output.
Each SCC contains an expanded end called the ampulla. Within the ampulla is the crista ampullaris (sensory epithelium) that contains type one and type two hair cells and supporting cells. Positioned directly on top of the crista is a gelatinous structure called the cupula that extends to the top of the ampulla. The density (specific gravity) of the cupula (and the surrounding endolymph fluid) is similar in density to water; thus, the SCCs are non-gravity sensitive structures.
Stereocilia project from the sensory hair cells into the cupula. The stereocilia are bundled together and arranged in a pattern of increasing length from short to tall, with the tallest cilia called the kinocilium. Changes in membrane potentials of the hair cell result from the movement of the cupula (either moving toward or away from the utricle) due to the direction of endolymph flow within the SCC (Schubert & Minor, 2004). The kinocilium is important for morphological polarization. When stereocilia are moved toward the kinocilium, the neural firing activity in that hair cell is increased (opening of transduction channels). If moved away from the kinocilium, the neural firing activity is decreased (closing of transduction channels). Ewald’s 2nd and 3rd laws (Ewald, 1892) describe the endolymph flow patterns responsible for changes in neural activity within the horizontal and vertical SCCs (Table 1–1).
Otolith Organ System
Each utricle and saccule are responsive for converting linear acceleration/linear deceleration and gravitational forces into an electrical code to interpret perception and orientation (Schubert & Shepard, 2016). The organs act as gravito-inertial force sensors.
• Utricles are positioned horizontally and sense horizontal linear acceleration.
• Saccules are positioned vertically and detect vertical linear acceleration.
Each otolith organ contains a macula where hair cells and supporting cells are embedded. Stereocilia extends from the hair cells into a gelatinous layer called the otolithic membrane. This layer contains calcium carbonate crystals called otoconia, which are dense structures with a specific gravity greater than the surrounding endolymph, allowing the otolith organs to be gravity sensors (Schubert & Shepard, 2016).
The otolith organs are divided into two sections by a central line called the striola, or “line of polarity reversal” (Curthoys et al., 2018, p. 2). Similar to the SCCs, the stereocilia within the otolith organs are also arranged in a pattern of increasing length toward the kinocilium. The otolith organs also work as functional pairs (both saccules as one pair, and both utricles as the other pair); however, the orientation of the kinocilium on each side of the striola allow for both excitation and inhibition responses to also occur within a single otolith organ. Ewald’s 2nd and 3rd laws (Ewald, 1892) can also be applied to these organs (Schubert & Shepard, 2016). Refer to Table 1–2.
Table 1–1. Summary of Semi-Circular Canal (SCC) Morphological Polarization and Neural Responses Patterns
The labyrinthine artery is a branch of the anterior inferior cerebellar artery (AICA) that has two main branches to supply blood to the vestibular system:
• The anterior vestibular artery supplies the anterior and horizontal SCCs, and the utricle.
• The posterior vestibular artery supplies the posterior SCC and the saccule.
The vestibular nerve contains cell bodies called Scarpa’s ganglion and is a division of Cranial Nerve VIII with two distinct branches (superior and inferior).
• The superior vestibular nerve innervates the anterior and horizontal SCCs, the utricle, and part of the saccule.
• The inferior vestibular nerve innervates the posterior SCC and the majority of the saccule.
Table 1–2. Summary of Otolith Organ Morphological Polarization and Neural Response Patterns
Note: *Ewald’s laws apply to semicircular canal function, but these can be extended to otolith neural response patterns (Schubert & Shepard, 2016).
Nerve fibers discharge spontaneously at rates of approximately 90 spikes/second (Goldberg & Fernandez, 1971). Baseline spontaneous firing on both sides is symmetric and is therefore processed as no motion. With natural head and body movements, upwards of 400 spikes/second occur during excitation and 0 spikes/second during inhibition (Schubert & Shepard, 2016).
The vestibular nerve transmits afferent signals through the internal auditory canal (IAC), which synapse at the vestibular nucleus (medullary-pontine junction of the brainstem). The vestibular nuclei is divided into four divisions (superior, inferior, medial, and lateral), with the majority of neural signals synapsing within the medial and lateral divisions to initiate vestibular reflex responses (Naito, Newman, Lee, Beykirch, & Honrunbia, 1995; Schubert & Shepard, 2016).
Vestibulo-ocular reflex (VOR) preserves visual acuity and minimizes retinal slippage during head movements. This action allows the eyes to make equal and opposite movements (180 degrees out of phase) to head movements with a ratio value (gain) close to one (eye movement/head movement; Figure 1–2A). Based on Ewald’s 1st law (Ewald, 1892), each SCC directly influences a pair of corresponding extra-ocular muscles that move the eyes in the plane of that SCC and in the direction of endolymph flow (Table 1–3), referred as the angular (rotational) VOR (Leigh & Zee, 2015). The angular VOR pathway is composed of a three-neuron arc (Figure 1–3).
Figure 1–2. Illustration of angular and linear vestibular-ocular reflex (VOR). A. Head turn to the right activates angular VOR to produce equal and opposite conjugate eye movements to the left to fixate on target (letter E). B. Head heave to the right activates linear VOR to produce equal and opposite conjugate eye movements to the left to fixation on target (letter E).