Vestibular signal processing in a subject with somatosensory deafferentation: The case of sitting posture

BMC Neurology BioMed Central Research article Open Access Vestibular signal processing in a subject with somatosensory deafferentation: The case of sitting posture Jean Blouin*1, Normand Teasdale2,3 and Laurence Mouchnino1 Address: 1Laboratoire de Neurobiologie de la Cognition, CNRS and Aix Marseille Université, 3 Place Victor Hugo, 13331 Marseille, France, 2Faculté de Médecine, Division de kinésiologie, Université Laval, Québec, Canada and 3Centre de recherche du CHA et Centre d'excellence sur le vieillissement, Hôpital Saint-Sacrement, Québec Email: Jean Blouin* - ; Normand Teasdale - ; Laurence Mouchnino - * Corresponding author Published: 29 August 2007 BMC Neurology 2007, 7:25 doi:10.1186/1471-2377-7-25 Received: 20 March 2007 Accepted: 29 August 2007 This article is available from: http://www.biomedcentral.com/1471-2377/7/25 © 2007 Blouin et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: The vestibular system of the inner ear provides information about head translation/ rotation in space and about the orientation of the head with respect to the gravitoinertial vector. It also largely contributes to the control of posture through vestibulospinal pathways. Testing an individual severely deprived of somatosensory information below the nose, we investigated if equilibrium can be maintained while seated on the sole basis of this information. Results: Although she was unstable, the deafferented subject (DS) was able to remain seated with the eyes closed in the absence of feet, arm and back supports. However, with the head unconsciously rotated towards the left or right shoulder, the DS's instability markedly increased. Small electrical stimulations of the vestibular apparatus produced large body tilts in the DS contrary to control subjects who did not show clear postural responses to the stimulations. Conclusion: The results of the present experiment show that in the lack of vision and somatosensory information, vestibular signal processing allows the maintenance of an active sitting posture (i.e. without back or side rests). When head orientation changes with respect to the trunk, in the absence of vision, the lack of cervical information prevents the transformation of the headcentered vestibular information into a trunk-centered frame of reference of body motion. For the normal subjects, this latter frame of reference enables proper postural adjustments through vestibular signal processing, irrespectively of the orientation of the head with respect to the trunk. Background The control of human upright and seated postures is based on information about body orientation and motion [1,2]. Neck-muscle proprioception plays a crucial role to this process as it allows the central nervous system to create an internal estimate of body motion through visual and vestibular signals [3-7]. Supporting this view is the early seminal observation made by De Jong and colleagues [8] and Cohen [9] of extensive sensorimotor deficits resulting from injection of local anaesthetics in the neck in animals as well as in humans [8], or from sections of the dorsal roots in monkeys [9]. For instance, in humans, the interruption of afferent flow from neck muscles induces ataxia, staggering Page 1 of 8 (page number not for citation purposes) BMC Neurology 2007, 7:25 gait, hypotonia of lower and upper segments, and a sensation of falling [8]. Evidence for cervical and vestibular neural integration is found in the rostral fastigial nuclei. In these deep cerebellar nuclei, on which massive vestibular and somatosensory signals converge, body-in-space motions are represented in a body frame of reference rather than in a head-based frame of reference [5,10,11]. Testing a subject with intact afferent information of the cervical region but deprived of proprioception below the neck, Day and Cole [12] showed that, together, the cervical and vestibular signals could provide the required estimate of body-in-space orientation/motion to keep equilibrium when seated. Interestingly, this case report showed the possibility to control posture in the absence of contact information (e.g. cutaneous and pressure) of the body with the supporting surface. As discussed above, neck proprioception may have allowed this subject determination of body motion through vestibular signals even in the absence of proprioception of trunk and limbs muscles. Here we investigated if, alone, the vestibular signals, which contribute to the perception of head motion/orientation in space and which have connections with motoneurons of axial and proximal postural muscles, are sufficient to control sitting posture. This was done testing the capacity of a rare subject, with a large-fiber sensory neuropathy that resulted in a severe loss of position sense below the nose (including the cervical region), to maintain a sitting posture. The contribution of vestibular information was specifically tested using two methods. One method consisted in creating a subliminal mismatch between vestibular information and actual body motion by slowly rotating the DS's head towards either shoulder in the dark. Controlling balance through vestibular information after undetected change of head-trunk configuration should lead to increase instability as the vestibular signals will no longer inform about the veridical body-inspace displacements. The second method employed in the present experiment consisted in externally stimulating the labyrinthine apparatus (galvanic vestibular stimulation technique, GVS). GVS produces a pattern of irregularly firing vestibular afferents that resembles that of the natural response to linear or angular head acceleration [13,14]. When applied to unrestrained subjects, GVS induces body tilt toward the anode side [7,15,16]. Day and Cole [12] showed that in a subject without body proprioception but intact cervical afferent signals, GVS also induced body tilt towards the anode side, but with a much greater magnitude than in control subjects. Here we tested if similar responses to GVS would be observed when neck muscle proprioception is also severely impaired. http://www.biomedcentral.com/1471-2377/7/25 Methods Case report The deafferented subject (female, 55 years-old) suffered at the age of 31 from a loss of the large myelinated fibres from her whole body after a severe sensory polyneuropathy. Neurophysiological data of the DS have been reported elsewhere [17]. In summary, at 27 years old, the subject suffered from a first episode of acute polyneuropathy with a complete paralysis including the respiratory muscles. A diagnostic of Guillain-Barré was made. It took six months for the subject to completely recover from the syndrome. A second episode (...truncated)