The thalamocortical vestibular system in animals and humans

Abstract

The vestibular system provides the brain with sensory signals about three-dimensional head rotations and translations. These signals are important for postural and oculomotor control, as well as for spatial and bodily perception and cognition, and they are subtended by pathways running from the vestibular nuclei to the thalamus, cerebellum and the “vestibular cortex.” The present review summarizes current knowledge on the anatomy of the thalamocortical vestibular system and discusses data from electrophysiology and neuroanatomy in animals by comparing them with data from neuroimagery and neurology in humans. Multiple thalamic nuclei are involved in vestibular processing, including the ventroposterior complex, the ventroanterior–ventrolateral complex, the intralaminar nuclei and the posterior nuclear group (medial and lateral geniculate nuclei, pulvinar). These nuclei contain multisensory neurons that process and relay vestibular, proprioceptive and visual signals to the vestibular cortex. In non-human primates, the parieto-insular vestibular cortex (PIVC) has been proposed as the core vestibular region. Yet, vestibular responses have also been recorded in the somatosensory cortex (area 2v, 3av), intraparietal sulcus, posterior parietal cortex (area 7), area MST, frontal cortex, cingulum and hippocampus. We analyze the location of the corresponding regions in humans, and especially the human PIVC, by reviewing neuroimaging and clinical work. The widespread vestibular projections to the multimodal human PIVC, somatosensory cortex, area MST, intraparietal sulcus and hippocampus explain the large influence of vestibular signals on self-motion perception, spatial navigation, internal models of gravity, one's body perception and bodily self-consciousness.

Introduction

The vestibular system has a unique role in the sensorimotor control and perception. By sensing the angular and linear accelerations, the vestibular system codes three dimensional head movements in space. By sensing gravitational acceleration, the vestibular receptors are also an essential basis for a spatial frame of reference allowing the brain to organize the erected human posture with respect to the ground (Berthoz, 2000). In turn, activation of the vestibular receptors is responsible for many reflexes acting on extraocular muscles devoted to gaze stabilization, as well as reflexes acting on postural muscles devoted to body orientation and stabilization in space (Wilson and Melvill Jones, 1979).

There is increasing evidence that the vestibular system is not only involved in perception, oculomotor and postural control, but also takes part in spatial cognition. In particular, how animals and human navigate in space – i.e. integrate and memorize the paths taken, elaborate and use cognitive maps of the spatial displacements – has been associated with vestibular processing (Berthoz et al., 1995, Mittelstaedt, 1999, Smith et al., 2010). In addition, vestibular signals, and the neural structures involved in vestibular processing, are crucial for distinguishing self-motion and object-motion (Straube and Brandt, 1987), perceiving the world as upright (Brandt and Dieterich, 1994, Lopez et al., 2007, Mittelstaedt, 1999), elaborating an internal model of gravity and of one's body motion (Angelaki et al., 2004, Merfeld et al., 1999), as well as for visual perception related to gravity (Indovina et al., 2005, Lopez et al., 2009). More recent studies conducted in neurological patients even suggested that vestibular signals are crucial for various aspects of one's body perception and awareness (Bottini et al., 1995, Vallar et al., 1993), and more generally for human bodily self-consciousness (Blanke et al., 2002, Lopez et al., 2008).

Thus, the understanding of the neural correlates of these aspects of vestibular function (spatial perception and cognition, spatial navigation, and own body perception), as well as the understanding of the complex spatial and bodily symptoms observed in patients suffering from vestibular disorders, necessitate a clear description of the vestibular pathways to the thalamus and cerebral cortex. Yet, as compared to what is known about the central structures involved in visual, auditory and somatosensory processing, only a few comprehensive reviews have been written on the localization of the vestibular thalamus and cortex in the last 25 years (see Berthoz, 1996, Brandt and Dieterich, 1999, Fredrickson and Rubin, 1986, Fukushima, 1997, Guldin and Grüsser, 1998; for reviews up to 1999). Electrophysiological and tracer studies in animals have identified at least ten regions that are clearly involved in vestibular processing and that are widely distributed in parieto-insular, somatosensory, posterior parietal, and frontal cortices. As early as the 1990s, with the development of functional neuroimaging in human neuroscience, the number of studies aiming at determining the corresponding vestibular regions in the human brain has increased considerably. The variety of the techniques used for determining vestibular projections (cold and warm caloric vestibular stimulation, monaural or binaural galvanic vestibular stimulation, auditory stimulation) has led to a large body of functional and anatomical data, which has not been reviewed recently and systematically compared between animals and humans.

The aim of the present review is to summarize current knowledge on the anatomy of the vestibulothalamocortical system by establishing theoretical connections between data from animal electrophysiology and neuroanatomy with data from functional neuroimagery and neurology in humans. The latter include electrical stimulation of the cortex in epileptic patients and the description of patients with focal brain damage reporting vestibular dysfunctions. As the anatomy and physiology of the vestibular nuclei and cerebellum have been largely described in the literature (Angelaki and Cullen, 2008, Barmack, 2003, Berthoz and Vidal, 1993, Carpenter, 1988, Cullen et al., 2003, Lacour and Borel, 1993), the present review focuses on the identification of the multiple thalamic nuclei and cortical areas receiving vestibular inputs in animals and humans. Moreover, because the electrophysiological responses of single neurons in vestibular cortex have been reviewed in detail previously (Angelaki and Cullen, 2008, Berthoz, 1996, Fukushima, 1997, Grüsser et al., 1994, Guldin and Grüsser, 1998), they will not be discussed here.