J Neurophysiol 91: 1919–1933, 2004; 10.1152/jn.00988.2003. Review Signal Processing in the Vestibular System During Active Versus Passive Head Movements Kathleen E. Cullen and Jefferson E. Roy Aerospace Medical Research Unit, Department of Physiology, McGill University, Montreal, Quebec H3G 1Y6, Canada Submitted 14 October 2003; accepted in final form 9 January 2004 Cullen, Kathleen E. and Jefferson E. Roy. Signal processing in the Cullen and McCrea 1993; Scudder and Fuchs 1992). However, vestibular system during active versus passive head movements. J in real life, the vestibular end organs not only inform the brain Neurophysiol 91: 1919–1933, 2004; 10.1152/jn.00988.2003. In ev- about the motion of the head during passively applied move- eryday life, vestibular receptors are activated by both self-generated ments, but they are also simultaneously activated by vestibular and externally applied head movements. Traditionally, it has been stimulation arising from our own actions. To maintain postural assumed that the vestibular system reliably encodes head-in-space motion throughout our daily activities and that subsequent processing and perceptual stability and to accurately guide behavior, the by upstream cerebellar and cortical pathways is required to transform nervous system must differentiate between sensory signals that this information into the reference frames required for voluntary register changes in the external world and those signals that behaviors. However, recent studies have radically changed the way result from our own actions. For example, vestibulospinal we view the vestibular system. In particular, the results of recent reflex pathways play a critical role in controlling head and single-unit studies in head-unrestrained monkeys have shown that the body posture by stabilizing the head and body relative to space. vestibular system provides the CNS with more than an estimate of While these reflexes are crucial for compensating for externally head motion. This review first considers how head-in-space velocity is applied head perturbations, they can be counterproductive processed at the level of the vestibular afferents and vestibular nuclei when an animal decides to actively move its head and/or body during active versus passive head movements. While vestibular in- relative to space. formation appears to be similarly processed by vestibular afferents during passive and active motion, it is differentially processed at the Von Holst and Mittelstaedt (1950) originally put forth the level of the vestibular nuclei. For example, one class of neurons in hypothesis that the CNS differentiates between sensory signals vestibular nuclei, which receives direct inputs from semicircular canal that arise from our own actions and those that result from afferents, is substantially less responsive to active head movements external events by sending a parallel “efference copy” of the than to passively applied head rotations. The projection patterns of motor command to sensory areas. In turn, this anticipatory these neurons strongly suggest that they are involved in generating signal is subtracted from the incoming sensory signal to selec- head-stabilization responses as well as shaping vestibular information tively remove that portion due to the animal’s own actions. In for the computation of spatial orientation. In contrast, a second class the vestibular system, an efferent pathway to the labyrinth has of neurons in the vestibular nuclei that mediate the vestibuloocular been described that could, in theory, underlie such a mecha- reflex process vestibular information in a manner that depends prin- nism. Vestibular efferent somas are located in the periabducens cipally on the subject’s current gaze strategy rather than whether the head movement was self-generated or externally applied. The impli- region, and directly project via the VIIIth nerve to the vestib- cations of these results are then discussed in relation to the status of ular hair cells in the labyrinth (Goldberg and Ferna´ndez 1980). vestibular reflexes (i.e., the vestibuloocular, vestibulocollic, and cer- It has been proposed that the primate efferent system functions vicoocular reflexes) and implications for higher-level processing of to reduce the sensitivity of the vestibular nerve during volun- vestibular information during active head movements. tary head movements (Goldberg and Ferna´ndez 1980). More- over, in addition to direct inputs from vestibular afferents, the vestibular nuclei receive substantial projections from cortical, INTRODUCTION cerebellar, and other brain stem structures. These structures The vestibular system is classically associated with detecting could provide the vestibular nuclei with numerous extra-ves- the motion of the head-in-space to generate the reflexes that are tibular cues that could be used to dissociate between active and crucial for our daily activities, such as maintaining head and passive head rotations. body posture (see Peterson and Richmond 1988) and stabiliz- Here we review the results of recent experiments that have ing gaze during walking and running (Grossman et al. 1988, addressed the question: how does the nervous system differ- 1989). Angular head-in-space velocity is detected by vestibular entiate between actively generated versus externally applied hair cells that are located within the semicircular canals of the head movements? We focus on recent studies that have con- vestibular end organs (Goldberg and Ferna´ndez 1971). In turn, sidered how head-movement information is encoded at the this information is relayed to neurons in the vestibular nuclei level of vestibular nerve afferents and neurons to which they via the afferent fibers of the vestibular nerve. Single-unit project in the vestibular nuclei. First, the results of prior stud- experiments in head-restrained animals have shown that head- ies, which have characterized neuronal responses in head- in-space velocity is reliably encoded at each of these sequential restrained monkeys during passive whole-body rotations, are stages of processing during passive whole-body rotations (e.g., summarized. Next recent studies that have addressed the pos- Address for reprint requests and other correspondence: K. E. Cullen, Aero- The costs of publication of this article were defrayed in part by the payment space Medical Research Unit, 3655 Promenade Sir William Osler, Montreal, of page charges. The article must therefore be hereby marked ‘‘advertisement’’ Quebec H3G 1Y6, Canada (E-mail: [email protected]). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. www.jn.org 0022-3077/04 $5.00 Copyright © 2004 The American Physiological Society 1919 Review 1920 K. E. CULLEN AND J. E. ROY sible differential encoding of self-generated and passively ap- to differentiate between active and passive head movements at plied rotations of the head-in-space are examined. Finally, the the level of the vestibular afferents. functional implications of the neurophysiological findings are discussed. In particular, we consider the status of vestibular reflexes during active and passive head movements as well as VESTIBULAR NUCLEI: ENCODING PASSIVE implications for higher-level processing of vestibular informa- VERSUS ACTIVE HEAD MOTION tion. Overview VESTIBULAR AFFERENTS: ENCODING PASSIVE Does the vestibular system differentiate between active and VERSUS ACTIVE HEAD MOTION passive head movements at the level of the vestibular nuclei? Although the processing of head movements by the vestibular Passive head movements nuclei has been well characterized during passive whole-body The responses of vestibular afferents have been well char- rotations, researchers have only recently begun to systemati- acterized during passive head rotations. Vestibular afferents cally explore vestibular processing during self-generated head with more regular spontaneous firing rates closely encode movements. The processing of angular horizontal head veloc- angular head velocity over the frequency range of physiolog- ity by the vestibular nuclei has been the most extensively ical head movements 2–20 Hz (Hullar and Minor 1999) with characterized and hence is the primary focus of this review. little change of sensitivity and a phase lead that increases with The afferent fibers of the horizontal semicircular canals, which frequency. In contrast, vestibular afferents that have more encode horizontal head velocity, project primarily to neurons irregular spontaneous firing rates demonstrate a gain enhance- within the rostral medial vestibular nuclei (rMVN) and the ment and significant phase lead for frequencies above 10 Hz ventrolateral vestibular nuclei (vLVN) (Gacek and Lyon (Goldberg and Ferna´ndez 1971). It had been proposed (Minor 1974). Single-unit recording experiments in alert head-re- and Goldberg 1991) that regular afferents might make the strained monkeys have shown neurons in these nuclei can be primary contribution to vestibuloocular reflex (VOR) pathway, grouped into distinct classes based on idiosyncratic constella- which functions to stabilize the axis of gaze on the retina. In tions of discharge properties during head-restrained eye move- contrast, irregular afferents could be more useful in overcom- ment paradigms and passive whole-body rotations (Chubb et ing the load of the head and so might be involved in mediating al. 1984; Fuchs and Kimm 1975; Keller and Daniels 1975; the vestibulocollic reflex (VCR), which functions to stabilize Lisberger and Miles 1980; Miles 1974; Tomlinson and Rob- gaze