Towards a concept of disorders of “higher vestibular function”

Background: Vestibular disorders are commonly characterized by a combination of perceptual, ocular motor, postural, and vegetative manifestations, which cause the symptoms of vertigo, nystagmus, ataxia, and nausea. Multisensory convergence and numerous polysynaptic pathways link the bilaterally organized central vestibular network with limbic, hippocampal, cerebellar, and non-vestibular cortex structures to mediate “higher” cognitive functions. Anatomical classification of vestibular disorders: The traditional classification of vestibular disorders is based on the anatomical site of the lesion. While it distinguishes between the peripheral and the central vestibular systems, certain weaknesses become apparent when applied clinically. There are two reasons for this: first, peripheral and central vestibular disorders cannot always be separated by the clinical syndrome; second, a third category, namely disorders of “higher vestibular function”, is missing. These disorders may be caused by peripheral as well as central vestibular lesions. Functional classification: Here we discuss a new concept of disorders of higher vestibular function which involve cognition and more than one sensory modality. Three conditions are described that exemplify such higher disorders: room tilt illusion, spatial hemineglect, and bilateral vestibulopathy all of which present with deficits of orientation and spatial memory. Conclusions: Further elaboration of such disorders of higher multisensory functions with respect to lesion site and symptomatology is desirable. The room tilt illusion and spatial hemineglect involve vestibular and visual function to the extent that both conditions can be classified as either disorders of higher vestibular or of higher visual functions. A possible way of separating these disorders in a first step is to determine whether the causative lesion site affects the vestibular or the visual system. For the vestibular system this lesion site may be peripheral or central. The criterion of “higher function” is fulfilled if cognition or senses other than the primarily affected one come into play.

[1]  J F Thayer,et al.  Neurological bases for balance-anxiety links. , 2001, Journal of anxiety disorders.

[2]  Thomas Brandt,et al.  Vertigo and Dizziness: Common Complaints , 2005 .

[3]  Stefan Glasauer,et al.  Model approach to neurological variants of visuo-spatial neglect , 2012, Biological Cybernetics.

[4]  Michael Strupp,et al.  Bedside differentiation of vestibular neuritis from central “vestibular pseudoneuritis” , 2008, Journal of Neurology, Neurosurgery, and Psychiatry.

[5]  T. Brandt,et al.  Vestibular syndromes in the roll plane: Topographic diagnosis from brainstem to cortex , 1994, Annals of neurology.

[6]  Mark Solms,et al.  Inverted Vision After Frontal Lobe Disease , 1988, Cortex.

[7]  E. Bisiach,et al.  Remission of hemineglect and anosognosia during vestibular stimulation , 1987, Neuropsychologia.

[8]  Albert Postma,et al.  Spatial memory deficits in patients after unilateral selective amygdalohippocampectomy , 2004, Journal of the International Neuropsychological Society.

[9]  Hyun-Ah Kim,et al.  Isolated Vestibular Nucleus Infarction Mimicking Acute Peripheral Vestibulopathy , 2010, Stroke.

[10]  O. Grüsser,et al.  Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey , 1994, The Journal of comparative neurology.

[11]  T. Brandt,et al.  Functional brain imaging of peripheral and central vestibular disorders. , 2008, Brain : a journal of neurology.

[12]  O J Grüsser,et al.  Localization and responses of neurones in the parieto‐insular vestibular cortex of awake monkeys (Macaca fascicularis). , 1990, The Journal of physiology.

[13]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

[14]  D. Perani,et al.  The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man , 1986, Neuropsychologia.

[15]  W. Kofman,et al.  On the usefulness of , 1999 .

[16]  D. Newman-Toker,et al.  Normal head impulse test differentiates acute cerebellar strokes from vestibular neuritis , 2008, Neurology.

[17]  Paul F. Smith,et al.  Vestibular–hippocampal interactions , 1997, Hippocampus.

[18]  H. Lanfermann,et al.  Engagement of Lateral and Medial Prefrontal Areas in the Ecphory of Sad and Happy Autobiographical Memories , 2003, Cortex.

[19]  B. Seemungal,et al.  The cognitive neurology of the vestibular system. , 2014, Current opinion in neurology.

[20]  T. Brandt,et al.  Vertigo and Dizziness , 2011 .

[21]  T. Brandt Vertigo: Its Multisensory Syndromes , 1991, Clinical Medicine and the Nervous System.

[22]  A. Vighetto,et al.  Room tilt illusion. A central otolith dysfunction. , 1996, Archives of neurology.

[23]  T. Brandt,et al.  Ocular torsion and tilt of subjective visual vertical are sensitive brainstem signs , 1993, Annals of neurology.

[24]  H. Karnath,et al.  The anatomy of spatial neglect , 2012, Neuropsychologia.

[25]  Cynthia L. Darlington,et al.  Vestibular influences on CA1 neurons in the rat hippocampus: an electrophysiological study in vivo , 2004, Experimental Brain Research.

[26]  Armin Schnider,et al.  The attention network of the human brain: Relating structural damage associated with spatial neglect to functional imaging correlates of spatial attention , 2011, Neuropsychologia.

[27]  C. Balaban Projections from the parabrachial nucleus to the vestibular nuclei: potential substrates for autonomic and limbic influences on vestibular responses , 2004, Brain Research.

[28]  O. Pompeiano,et al.  Gene expression in rat vestibular and reticular structures during and after space flight , 2002, Neuroscience.

[29]  Dora E Angelaki,et al.  Convergence of Vestibular and Visual Self-Motion Signals in an Area of the Posterior Sylvian Fissure , 2011, The Journal of Neuroscience.

[30]  O. Grüsser,et al.  Vestibular neurones in the parieto‐insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses. , 1990, The Journal of physiology.

[31]  T. Brandt,et al.  Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation , 2007, Hippocampus.

[32]  L. Luxon,et al.  Vertigo. Its Multisensory Syndromes , 2000, Journal of neurology, neurosurgery, and psychiatry.

[33]  H. Karnath,et al.  Subjective body orientation in neglect and the interactive contribution of neck muscle proprioception and vestibular stimulation. , 1994, Brain : a journal of neurology.

[34]  R. Sterzi,et al.  Exploring somatosensory hemineglect by vestibular stimulation. , 1993, Brain : a journal of neurology.

[35]  M Dieterich,et al.  Vestibular cortex lesions affect the perception of verticality , 1994, Annals of neurology.

[36]  Marianne Dieterich,et al.  Spatial neglect--a vestibular disorder? , 2006, Brain : a journal of neurology.

[37]  T. Brandt,et al.  Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. , 2005, Brain : a journal of neurology.

[38]  M. Goodale Transforming vision into action , 2011, Vision Research.

[39]  H. Lee,et al.  Recent advances in central acute vestibular syndrome of a vascular cause , 2012, Journal of the Neurological Sciences.

[40]  D. Newman-Toker,et al.  HINTS to Diagnose Stroke in the Acute Vestibular Syndrome: Three-Step Bedside Oculomotor Examination More Sensitive Than Early MRI Diffusion-Weighted Imaging , 2009, Stroke.

[41]  E. de Pablo-Fernández,et al.  Clinical and imaging features of the room tilt illusion , 2012, Journal of Neurology.

[42]  Bernard H. Smith Vestibular disturbances in epilepsy , 1960, Neurology.

[43]  T. Brandt,et al.  An ipsilateral vestibulothalamic tract adjacent to the medial lemniscus in humans. , 2008, Brain : a journal of neurology.

[44]  Marianne Dieterich,et al.  A Pathway in the Brainstem for Roll-Tilt of the Subjective Visual Vertical: Evidence from a Lesion–Behavior Mapping Study , 2012, The Journal of Neuroscience.

[45]  T. Brandt,et al.  Dominance for vestibular cortical function in the non-dominant hemisphere. , 2003, Cerebral cortex.

[46]  Simon B. Eickhoff,et al.  Meta-analytical definition and functional connectivity of the human vestibular cortex , 2012, NeuroImage.

[47]  T. Brandt,et al.  Cortical matching of visual and vestibular 3D coordinate maps , 1997, Annals of Neurology.

[48]  A. Ropper Illusion of tilting of the visual environment. Report of five cases. , 1983, Journal of clinical neuro-ophthalmology.

[49]  Alan Cowey,et al.  On the usefulness of ‘what’ and ‘where’ pathways in vision , 2011, Trends in Cognitive Sciences.

[50]  T. Brandt,et al.  The Vestibular Cortex: Its Locations, Functions, and Disorders , 1999, Annals of the New York Academy of Sciences.

[51]  Philippe Kahane,et al.  Reappraisal of the human vestibular cortex by cortical electrical stimulation study , 2003, Annals of neurology.