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VESTIBULAR-NECK INTERACTION and TRANSFORMATION of SENSORY COORDINATES Introduction

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VESTIBULAR-NECK INTERACTION and TRANSFORMATION of SENSORY COORDINATES Introduction Journal of Vestibular Research, Vol. 7, No.4, pp. 347-367,1997 Copyright © 1997 Elsevier Science Inc. Printed in the USA. All rights reserved 0957-4271197 $17.00 + .00 ELSEVIER PIT S0957-4271(96)00176-0 Review VESTIBULAR-NECK INTERACTION AND TRANSFORMATION OF SENSORY COORDINATES T. Mergner,* W. Huber,* and W. Beckert *Neurological University Clinic, Freiburg; tSection Neurophysiology, University of Ulm, Germany Reprint address: Dr. T. Mergner, Neurologische Klinik, Neurozentrum, Universitatsklinikum, Breisacher Str. 64, 0-79106 Freiburg, Germany. Tel: +49-761-270-5313 (5306); Fax: +49-761-270-5310; E-mail: [email protected] o Abstract - The article considers findings and Introduction concepts on vestibular-proprioceptive interaction for self-motion perception and postural control If we want to use the sensory information pro­ under the form of simple describing models. It vided by the sensory systems located in our points out that vestibular-neck interaction is only heads (vestibular, visual, auditory) for postural a small fraction of an extended mechanism of co­ ordinate transformations. This links together 'the or perceptual control of upright stance, our different parts of our bodies, so that sensory infor­ brain has to take into account that the head is mation arising in one part of the body can be used movable with respect to the trunk and, hence, for perceptual or motor tasks in other parts. Par­ also relative to the support surface we are stand­ ticular emphasis is put on the problems that arise ing on. Consider, for example, the semicircular from imperfect signal transduction in the vestibu­ canals of the vestibular system and one of their lar semicircular canal systems at low stimulus fre­ targets during postural control, the leg muscles. quencies/velocities. Also, a "down-and-up-chan­ Having a fixed orientation in the head, each ca­ neling" principle is suggested, by which the body nal will indicate head velocity in specific planes support is linked via coordinate transformations defined by head anatomy. It is therefore conve­ to the internal notion of physical space provided nient, and concurs with intuition, to treat these by the vestibular system. Furthermore, the follow­ ing question is addressed: how does the brain use signals as being "coded in head coordinates," visual input to overcome the vestibular deficien­ although the cause of these signals is an acceler­ cies, at the risk of visual self-motion illusions? Fi­ ation with respect to a fixed inertial coordinate nally, a conceptual mode! of postural controi is system. On the other hand, the leg muscles used presented in which a proprioceptive feedback tn body sway, act about axes de­ that links the body to its support surface is merged fined by the position of the corresponding foot with a loop for postural stabilization in space. on its support. Therefore, their innervation can © 1997 Elsevier Science Inc. be viewed in terms of the intended rotation (or torque) about these axes and, hence, as being o Keywords - vestibular-neck interaction; "coded in foot coordinates." proprioception; visual-vestibular interaction; The way a given canal signal acts upon a postural control; coordinate transformation; human. given muscle in the act of stabilization obvi­ ously depends on canal orientation with respect to the foot and, hence, on head-on-trunk-to-foot 347 348 T. Mergner et al position. 1 A human investigator who wants to stitute an important organizational principle of understand the mechanisms of postural control, the eNS, for both perception and motor control. may interpret this dependence as the result of a The need for a coordinate transformation of coordinate transformation. This interpretation vestibular signals was anticipated by von Holst invites further abstraction: In dealing with pos­ and Mittelstaedt (1) in their classical paper on tural reflexes one may postulate (i) signals that the "Reafferenzprinzip", in which they state directly indicate position, velocity or accelera­ that, due to a subtractive interaction of vestibu­ tion with respect to an inertial frame of refer­ lar and neck afferents, control of trunk posture ence (which can only be arrived at by appropri­ by the vestibular system proceeds as if the vesti­ ate coordinate ~ransformations of primary sensory bular organs were actually located in the trunk signals), (ii) a computation of corrective signals (" .. derOrganismus sich so verhiilt, als ob der (for example, torques) therefrom, and finally "Lagesinn" normaliter im Leib siiBe ... "; p (iii) a transformation of these desired torques 475).2 Studies in decerebrate cat support the no­ into innervations coded in coordinates of the tion of the trunk posture being controlled by a participating muscle. subtractive interaction of vestibular and neck Whether functional entities corresponding afferents (2,3). Also, recordings of vestibular nu­ to these constructs exist in the real central ner­ clear neurons during lateral head and/or trunk vous system (CNS) is, as yet, an open question. tilt in the decerebrate cat (4) and during horizon­ We cannot exclude that the three separate steps tal rotations in the intact cat (5) revealed sub­ of the human mind outlined above are lumped tractive (and additive) interactions between ves­ into a dedicated network of neurons providing tibular and neck inputs. Moreover, subtractive multiple (polysynaptic) connections of every and additive interactions of vestibular and neck canal with every muscle, as would be the case afferents have also been observed in the cere­ with a technical learning network trained to re­ bral cortex of the intact cat (6,7). produce human postural behavior. However, we In the intact cat, certain head and body pos- feel that the CNS is much more structured than 'tures during natural behavior are reminiscent of technical networks, and that its hierarchical ar­ what one might expect from a subtractive vesti­ chitecture could well accommodate abstract lev­ bular-neck interaction (8), whereas experimen­ els of processing between the primary sensory tal stimulation of these inputs do not readily and motor levels, which undoubtedly would con­ reveal the expected interactions. In humans, re­ tribute to its flexibility. On the motor side, a cer­ flexes reminiscent of the cervico-spinal ones in tain type of abstraction can be recognized in the the decerebrate cat are seen only in the first tight intraspinal coupling of synergistic muscle month after birth (9,10) or following extended groups. Therefore, we conceive of the coordi­ brain lesions (11,12). In the healthy adult, by nate transformation as being performed in a glo­ contrast, for a long time only sparse evidence bal way, before a compound motor plan is for­ for a vestibular-neck interaction in postural con­ mulated to concert muscle actions. Moreover, trol was obtained (13). we know from psychophysical studies that on More recent studies on human posture con­ the perceptual leveL humans can indeed trans­ trol directly support the notion of the above out­ form their primary sensory signals into such ab­ lined coordinate transformation. With natural stract notions as 'head velocity in space' or 'trunk body sway during tilt of a platform, compensa­ velocity in space', to name only two. Accord­ tory postural reactions are essentially indepen­ ingly, in the present article, we proceed from the dent of the head-on-trunk position. In contrast, notion that coordinate transformations may con- the body sway resulting from galvanic vestibu­ lar stimulation changes direction in direct rela­ tion to the horizontal head-on-trunk and trunk- I W e here proceed from the assumption that the main source of inertial stabilization of posture is the vestibular system, although somatic graviceptors may also play a role (see 2This idea goes back to Mittelstaedt's PhD thesis of 1949 Mittelstaedt, this volume). (see Mittelstaedt, this volume). Sensory Coordinate Transformations 349 on-foot excursion (14-16). Galvanic stimulation oratories. In doing so, we will interpret a previ­ with the head in the primary position leads to a ously suggested model of this interaction from body sway towards the ear where the anode is the point of view of coordinate transformations fixed, whereas the same stimulus with the head between a hierarchy of superimposed coordi­ horizontally rotated 30° to the right side, for in­ nate systems, and we will also discuss problems stance, evokes a body sway that also is shifted arising from imperfect signal transduction by 30° towards the right. Apparently, the galvanic receptors. Moreover, in view of their impor­ vestibular stimulus, which is fixed in head coor­ tance for ego-motion perception, we will touch dinates' is transformed into space coordinates on certain aspects of the interaction of visual by means of neck afferents-much as a physi­ cues with vestibular and proprioceptive ones. cal, and hence head position dependent acceler­ Finally, we will try to link these considerations ation would be. Whereas with the physical (tilt) to the control of body posture and present a hy­ stimulus, this transformation compensates for pothesis on how to merge a proprioceptive feed­ head-on-trunk rotation and keeps the postural re­ back loop stabilizing the body relative to a piv­ action constant, it makes the reaction directly oting support with a vestibular one controlling dependent on the neck input with galvanic stim­ body posture in space. In the appendix, we give ulation. a brief outline of the mathematics describing the
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