EFFECTS OF BODY TO HEAD ROTATION ON THE LABYRINTHINE RESPONSES OF RAT VESTIBULAR NEURONS M. BARRESI, a C. GRASSO, a G. LI VOLSI b AND D. MANZONI a * a Department of Translational Research and New Technologies in Medicine and Surgery, University of Pisa, I-56127 Pisa, Italy b Department of Biomedical Sciences, University of Catania, I-95125 Catania, Italy Abstract—Vestibulospinal reflexes elicited by head dis- placement in space depend on the direction of body dis- placement, because the neuronal responses to labyrinthine stimulation are tuned by neck displacement: a directional tuning takes place in the medial cerebellum and in spinal motoneurons, while a gain and a basal activity tun- ing can be observed in the reticular formation, a target struc- ture of the medial cerebellum. In the present study, we investigated whether also the response of vestibular nuclear neurons (another target of the medial cerebellum) to labyrin- thine stimulation is tuned by neck displacement and which parameters of the response are modulated by it. In urethane-anaesthetized Wistar rats, single-unit activity was recorded from the vestibular nuclei at rest and during wob- ble of the whole animal at 0.156 Hz. This stimulus tilted the animal’s head by a constant amplitude (5°), in a direction rotating at a constant velocity over the horizontal plane, either in clockwise or counter clockwise direction. The gain and the direction of neuronal responses to wobble were evaluated through Fourier analysis, in the control position (with coincident head and body axes) and following a body-to-head rotation of 5–30° over the horizontal plane, in both directions. Most of the vestibular neurons modified their response gain and/or their basal activity following body-to-head rotation, as it occurs in the reticular formation. Only few neurons modified their response direction, as occurs in the cerebellum and in spinal motoneurons. The different behaviour of cerebellar neurons and of their vestib- ular and reticular target cells, suggests that the role played by the cerebellum in the neck tuning of vestibulospinal reflexes has to be reconsidered. Ó 2013 IBRO. Published by Elsevier Ltd. All rights reserved. Key words: cerebellum, reticular formation, vestibular nuclei, vestibular reflexes, neck rotation. INTRODUCTION Vestibulospinal (VS) reflexes modify the postural tone according to head position in space (Von Holst and Mittelstaedt, 1950; Roberts, 1978). They are spatially organized, i.e. each muscle is maximally activated for a specific, ‘‘preferred’’ direction of head tilt (Wilson et al., 1986). Vestibular signals that monitor head displacement in space have to be integrated with proprioceptive neck signals related to the body-to-head position (von Holst and Mittelstaedt, 1950; Roberts, 1978), in order to elicit VS reflexes appropriate to stabilize the body position. It is well known that a linear interaction of VS and cervicospinal (CS) reflexes elicited by coplanar head and neck rotations (Lindsay et al., 1976; Ezure and Wilson, 1983; Manzoni et al., 1983), modulates the postural tone only when the position of the trunk in space changes. A similar interaction seems also to underline the perception of body motion in healthy humans (Mergner et al., 1991, 1997). In this study, however, we address another aspect of the interaction of neck and vestibular signals, which may take place when head and neck rotations are not coplanar (Mergner et al., 1997). Indeed, in order to maintain balance (Fig. 1A, B), an identical labyrinthine signal elicited by body sway (black arrows) must give rise to different postural responses (white arrows), if the head is kept in different static positions with respect to the body: in this instance, tonic neck input may allow to infer body motion from labyrinthine signal, leading to a change in the reference frame of the vestibular input from head to body. This is the reason why, during galvanic vestibular stimulation of the labyrinth, the direction of the perceived (Fitzpatrick et al., 1994) and the elicited (Lund and Broberg, 1983; Britton et al., 1993; Fitzpatrick et al., 1994) body sway changes along with the head-to-body position, in spite of the similar activation of vestibular afferents. There is an extensive literature on the neural mechanisms underlying the linear interaction of vestibular and neck reflexes elicited by co-planar head and neck rotations (Denoth et al., 1979; Boyle and Pompeiano, 1981; Kubin et al., 1981; Anastasopoulos and Mergner, 1982; Pompeiano et al., 1984; Wilson et al., 1984; Mergner et al., 1985; Kasper et al., 1988). In contrast, only few studies investigated how tonic neck input elicited by a sustained body-to-head displacement modifies the labyrinthine responses elicited by non coplanar animal tilts (Manzoni et al., 1998, 1999; Kleine et al., 2004; Shaikh et al., 2004). In particular, it has been shown that the preferred directions of the responses of the limb muscles to animal tilt rotate in the same 0306-4522/13 $36.00 Ó 2013 IBRO. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.neuroscience.2013.04.010 * Corresponding author. Address: Dipartimento Traslazionale, Uni- versita` di Pisa, Via S. Zeno 31, 56127 Pisa, Italy. Tel: +39-50- 2213466; fax: +39-50-2213527. E-mail address: manzoni@dfb.unipi.it (D. Manzoni). Abbreviations: CCW, counter clockwise; CW, clockwise; D, direction; S MAX , maximal sensitivity vector; SN, signal-to-noise; SPDH, sequential pulse density histogram; SU, side-up; VS, vestibulospinal. Neuroscience 244 (2013) 134–146 134