Editorial: The Vestibular System in Cognitive and Memory Processes in Mammalians

摘要

In the nineteenth century Pierre–Jean–Marie Flourens ( 1825 ) and Ernst Mach described the vestibular system and its peripheral organs while Robert Barany, rewarded by the Nobel prize in 1914, was the first to investigate vestibular disorders with caloric tests making surgical treatments of the vestibular organ possible. Recently, Graf and Klam ( 2006 ) have reminded us that this ancient sensory system appeared more than 500 million years ago. Logically its influence would most likely not be restricted to balance reflexes at the brainstem level; it must have also shaped our brain. The vestibular system is the one sensory organ dedicated to gravity perception, which along with light and oxygen served as a motor of evolution. In the 1950s the groups of Otto–Joachim Grüsser in Germany, Wilder Penfield in Canada, and later the group of Alain Berthoz in France, demonstrated in elegant experiments on awake monkey (Guldin and Grüsser, 1998 ), epileptic patient (Penfield, 1957 ), and neurologically-normal human (Lobel et al., 1999 ) the existence of vestibular projections to the cortex and how they combine with visual and proprioceptive information. An increasing number of researchers, often fervent disciples, have built on these findings to produce a spate of publications that have consolidated the evidence for a sense of verticality and three-dimensional body representations within the vestibular cortical areas. In the 1990s Paul Smith and colleagues examined vestibular processing in the hippocampus and its role in spatial memory. Exploring this topic in the rodent (Smith, 1997 ), they began to elucidate the secrets and the previously silent functions of the vestibular system. These findings led to increasing clarity about how vestibular degeneration may be related to some aspects of dementia (Previc, 2013 ), psychiatric diseases (Gurvich et al., 2013 ), and cognitive impairments in the elderly (Bigelow et al., 2015 ; Semenov et al., 2015 ). The research by Marianne Dieterich and Thomas Brandt has examined the bilateral organization of multiple multisensory cortical areas and revealed the vestibular dominance of the non-dominant hemisphere (Dieterich et al., 2003 ). They addressed the following questions: how is one global percept of motion and orientation in space formed, and does this dominance determine the lateralization of brain function such as handedness (Brandt and Dieterich, 2015 )? A vestibular contribution to the most crucial aspects of the human sense of self and self-consciousness has recently been highlighted by neurological and neuroscientific investigations: vestibular signals contribute to the experience that the self is located within the boundaries of the body (Blanke et al., 2004 ; Lopez et al., 2008 ) and may even be involved in self-other discrimination and interactions (Lenggenhager and Lopez, 2015 ). In this Frontiers in Integrative Neuroscience Research Topic initiated by Sidney Simon, twenty-four articles highlight recent discoveries in the field of vestibular cognition, including: (1) Anatomy of the vestibulo-cortical pathways; (2) Spatial navigation and memory; (3) Spatial cognition, bodily and self-motion perception; (4) Vestibular stimulation and rehabilitation; (5) Posture and motor control; (6) Vestibular disorders and compensation; and (7) Development of vestibular function. Anatomy of the vestibulo-cortical pathways A better understanding of the vestibulo-thalamo-cortical pathways and cortical vestibular processing is needed to fully understand the reciprocal interactions between vestibular processing and cognition. Hitier et al. ( 2014 ) provide a comprehensive review of the pathways running from the vestibular apparatus to the cortex, with a focus on the vestibulo-hippocampal pathways. Ventre-Dominey ( 2014 ) proposes that two separate cortical vestibular subsystems underpin velocity and inertia processing. A better definition of the vestibular cortex is provided on the basis of clinical and neuroimaging investigations in brain-damaged patients by Brandt et al. ( 2014 ), and on the basis of electrophysiological investigations in epileptic patients by Hewett and Bartolomei ( 2013 ). Spatial navigation and memory Yoder and Taube ( 2014 ) and Smith and Zheng ( 2013 ) offer a recent overview of the vestibular contribution to spatial learning and navigation through the head direction and place cells and how vestibular information is integrated into higher navigation centers. Jacob et al. ( 2014 ) provide a review and original data relating to the role of the entorhinal cortex (EC) in spatial memory. Despite the evidence that place cells in the hippocampus are adversely affected by the loss of vestibular function, there have been no data reported relating to grid cells in the EC. Here the authors present evidence that inactivation of the vestibular system in rats using tetrodotoxin injections results in a decrease in power in velocity-related theta EEG (5–12 Hz) in the EC, suggestin