The central nervous system vestibular pathways consist of¹:

(i) Vestibular nerve projections from the vestibular organs to the vestibular nucleus in the brainstem

(ii) Projections from the brainstem to thalamic nuclei, cerebellum, and spinal cord 

(iii) Projections from the thalamus to the cerebral cortex

Vestibular cortex differs in various ways from other sensory cortices. It consists of a network of several distinct and separate temporoparietal areas. Its core region, the parietoinsular vestibular cortex (PIVC), is located in the posterior insula and retroinsular region and includes the parietal operculum. The entire network is multisensory (in particular, vestibular, visual, and somatosensory).

The peripheral and central vestibular systems are bilaterally organized; there are various pontomesencephalic brainstem crossings and at least two transcallosal connections of both hemispheres, between the PIVC and the motion-sensitive visual cortex areas, which also mediate vestibular input.

From: Dieterich M, Brandt T. The parietal lobe and the vestibular system. Handb Clin Neurol. 2018;151:119-140.

Note the critical importance of convergent inputs at the level of the vestibular nuclei for processing of information, and that, as opposed to the standard sensory systems which encode information relative to different egocentric reference frames (eg, the eyes, head, or body), we perceive an allocentric (our position relative to our surroundings), gravity-centered representation of the world.  

For example, although the visual system encodes the environment in eye-centered coordinates, if one rolls one's head ear-downwards, one would still perceive buildings as being vertically oriented even though they are obliquely oriented on the eyes. This perceptual constancy is the result of computational mechanisms that perform cue disambiguation, dissociating the contributions of eye-in-world and object-in-world orientations to retinal images. Specifically, visual information is transformed from an eye-centered reference frame into a gravity-centered reference frame to achieve a stable, upright visual representation of the world." ².

Similarly, if standing on a bus or train, when it leaves the stop, the otolith organs will then no longer report just the gravitational vector but will also start to report the total gravitoinertial vector, which is currently tilted because of an additional component created by the acceleration of the moving vehicle or train. If only the otolith signal were present in order to align the internal representation of external space, the passenger would perceive a tilted world. It is clear that the brain needs other sensory signals concerning rotation of the head and joints in order to extract the gravitational and acceleration components of the total vector³.

The references frames for vestibular inputs include: 

• A body (or world)- centered allocentric frame in the ventral intraparietal area (VIP).  This region is closest to parietal association cortex; the reference frame of the vestibular perception of body motion is preferably allocentric within a 3D space (relative to the surroundings), in contrast to visual and auditory stimuli, which are preferably perceived in an egocentric frame (relative to the subject).
• A mixed head- and body-centered reference frame in the PIVC.  The PIVC corresponds to the parietal operculum; this region has also been identified in lesion studies of stroke patients who showed deviations of verticality perception². 
• Head- and eye- (but not body-) centered frame in the medial superior temporal cortex (MST) (note this is closest to the visual association cortex)

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

The vestibular system is concerned with the control of body position and self-motion in a 3D environment, as well as orientation and navigation during locomotion. These functions cannot be attributed to distinct areas, but are the result of the assimilation of the simultaneous inputs of various sensory systems within the temporoparietal networks.  The entire network is multisensory (in particular, vestibular, visual, and somatosensory), and the parietal cortex is part of a network for coordinating sensorimotor functions to maintain balance and to guide motor behavior within the gravitational field.

Multisensory convergence provides the basic sensory information for motor behavior such as walking and balance control within the gravitational field, and also for being able to make grasping movements and reaching movements.
These functions require separate reference frames:

• Allocentric for continuous updating of an internal model of body position in the environment, and
• Egocentric, for localization of objects within one's own field of view.

These functions are acquired in early infancy when children begin to explore their surroundings. These early interactions with the environment lead to the development of internal spatial maps and models of movements which lay the foundation for later orientation and navigation. Orientation and navigation require involvement of the hippocampal complex which encodes episodic and spatial memory⁴.

The most striking aspect of the higher vestibular systems are their close connections with the visual system, especially the human motion-sensitive medial temporal (MT) and medial superior temporal (MST) areas. To emphasize this interaction, neurons within the temporoparietal vestibular network are activated in both hemispheres during vestibular stimulation, and this is associated with a downregulation (deactivation) occurs within the visual cortex bilaterally; the converse occurs with visually induced self-motion perception. These reciprocal interactions like shift strength of the inputs from the less to the more reliable modality in order to resolve potential perceptual conflicts in situations with mismatched sensory input.
Optic flow patterns indicating self-motion relative to the stationary environment typically result in congruent visual-vestibular self-motion signals⁵.  Incongruent signals can arise due to object motion, vestibular dysfunction, or artificial stimulation, leading to disorientation and motion sickness if there is a mismatch between visual and vestibular inputs. A classical example of an extreme version of a disturbed visual-vestibular interaction is the room tilt illusion, as seen in a dorsolateral medullary syndrome. Spatial determination of vertical depends on interactions between the visual and vestibular systems, which in this case are markedly different. Since one cannot perceive two verticals at one time, initially the vestibular input must be dominant (at the time of tilt), and this is typically followed by rapid recovery to normal perception of vertical as the visual sense takes command.

The vestibular sense is distinct from other sensory modalities and characterized by various special features:

• The hemispheres must provide a “global vestibular percept” because an individual cannot perceive two different body positions or body motions at one and the same time.
• Natural stimulation of the vestibular system by head motion and locomotion is always multisensory (visual, vestibular, somatosensory).
• The vestibular system is the only sensory modality exhibiting hemispheric dominance: for right handers it is the right hemisphere, and for left handers the left hemisphere ⁴.

As could be expected, given the degree of multimodal processing at the level of the vestibular nuclei, there is no primary vestibular cortex that receives only vestibular signals. All cortical neurons receiving vestibular signals also receive other sensory signals, especially visual and somatosensory.  
Multiple sensory inputs converge at all levels of the central vestibular system from the vestibular nuclei to the temporoparietal cortex: the central vestibular system combines ascending vestibular information from both sides, and has a hierarchial level of control, which may be reflexive, at the level of the brainstem and cerebellum.  This may be contrasted with conscious perception of motion and control of voluntary movement. All levels of the system, from reflexive to voluntary and conscious necessarily need to interact and integrate with one another in order to achieve optimal function⁴.

The primary functions of higher vestibular centres are:

1. Perception of self-motion and verticality within the three-dimensional (3D) gravitational field.
2. Sensory input for apropriate motor output to gaze centres and for balance. 
3. Projections to the hippocampal formation for cognitive vestibular functions, especially spatial memory, orientation, and navigation.