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Introduction the Vestibular Stimulus Turntable Journal of Vestibular Research, Vol. 1, pp. 223-239, 1990/91 0957-4271/91 $3.00 + .00 Printed in the USA. All rights reserved. Copyright © 1991 Pergamon Press pic EFFECT OF INCISIONS IN THE BRAINSTEM COMMISSURAL NETWORK ON THE SHORT-TERM VESTIBULO-OCULAR ADAPTATION OF THE CAT G. Cheron The Laboratory of Neurophysiology, Faculty of Medicine, University of Mons, 24, avenue du Champ de Mars, 7000 Mons, Belgium Reprint address: G. Cheron, The Laboratory of Neurophysiology, Faculty of Medicine, University of Mons, 24, avenue du Champ de Mars, 7000 Mons, Belgium o Abstract - This study was intended to test the combined stimulation during the training was still adaptive plasticity of the vestibulo-ocular reflex be­ operative in all lesioned cats, the adaptive plastic­ fore and after either a midsagittal or parasagittal ity was completely abolished by the lesions. These incision in the brainstem. Eye movements were results suggest that the commissural brainstem net­ measured with the electromagnetic search coil tech­ work may playa crucial role in the acquisition of nique during the vestibulo-ocular reflex (VORD) the forced VOR adaptation. in the dark, the optokinetic reflex (OKN), and the visuo-vestibular adaptive training procedure. Two o Keywords - ve-stibulo-ocular adaptation; types of visual-vestibular combined stimulation brain stem commissural incisions; cat. were applied by means of low frequency stimuli (0.05 to 0.10 Hz). In order to increase or decrease the VORD gain, the optokinetic drum was oscil­ lated either 180° out-of-phase or in-phase with Introduction the vestibular stimulus turntable. This "training" procedure was applied for 4 hours. Initial measure­ The vestibulo-ocular reflex (VOR) stabilizes ments of the VORD were normal with a mean gain retinal images during self-induced and artifi­ value of 0.92 ± 0.08. After 4 hours of "training" cially induced rotational head movement by with the out-of-phase condition (180°), VORD generating smooth eye movements that are gain reached mean values of 1.33 ± 0.11 (n = 6 cats). In the in-phase combination, the mean VORD opposite in direction and nearly equal in am­ gain decreased from 1.0 to 0.63 ± 0.02 (n = 2 cats). plitude to head movement. No significant change of VORD phase was found It is now well accepted that the VOR can in any of the cats. Midsagittal or parasagittal pon­ be adaptively modified by artificial alteration to medullary brainstem incisions were performed in of the normal visual stimulation produced 4 cats. Recovery of the VOR was tested on the during rotation of the head (for references, 2nd, 7th, and 30th day after operation. After the see reference 1). 30th day, recovery of the VORD gain stabilized at Until now, many studies have been de­ about 66070 of the initial preoperative value. At this voted to identifying the neuronal circuit re­ stage of the recovery, the optokinetic response sponsible for the adaptive visual-vestibular (OKN) of the midsagittal-Iesioned cats was practi­ cally normal: in the parasagittal-Jesioned cats, the interaction. However, the site of the short­ postoperative OKN responses were asymmetric. term and long-term vestibula-ocular motor After stabilization of recovery, lesioned cats were learning is currently a controversial issue. On trained with the same adaptation procedure. Al­ the one hand, the flocculus hypothesis sup­ though the direct effect of the visuo-vestibular ported by Ito's group (2-4) was first advanced RECEIVED 23 February 1990; REVISION RECEIVED 5 October 1990; ACCEPTED 9 October 1990. 223 224 G. Cheron on the basis of bilateral flocculectomy pre­ Methods venting any adaptation (S-6) and secondly reinforced on the basis of Purkinje cell re­ General Procedure cordings before and after adaptation (7). On the other hand, the brains tern hypothesis, put The experiments were performed on 10 forward by Mile's group (8-11) on the basis cats. Under general anaesthesia (xylidinodi­ of the fact that the changes of Purkinje cells' hydrothiazin, Rompun, Bayer 3 mg/kg and output were in the wrong direction to produce pentobarbitone, Nembutal, Abbott, 20 mg/kg) VOR adaptation. In the light of more recent and aseptic conditions, 2 devices were chron­ experiments, these two conflicting hypothesis ically implanted. A scleral search coil was im­ were reanalyzed by Lisberger (12) who sug- planted subconjunctivally on both eyes (17). in 1988 [hat ~:1ere inay bt 2, ::>1[c5 of synap- Two uansverse tubes were placed on the skull tic adaptation: a primary site in the brainstem in the horizontal plane and embedded in den­ (the flocculus target neurons) and a secondary tal acrylic cement to immobilize the head dur­ site in the floccular cortex. In this context, ing the experiments. another reconciling hypothesis based on a When an animal had recovered from the theoretical model was advanced by Galiana effects of this first surgery (about one week), (13,14). In this model, the commissural path­ it was loosely restrained in a body box to way interconnecting the 2 sides of the brain­ which the head was fixed. A week later con­ stem was put forward as a powerful putative trol records of the eye movements and the ad­ site for adaptive modulation of the VOR. aptation procedure were performed. The aim of the present article is to test ex­ In order to avoid some possible change of perimentally the effects of a commissural in­ the central parameters controlling the VOR cision on VOR adaptation behavior. This when the cat was trained with the visuo­ approach, while theoretically possible, pre­ vestibular combined stimuli before the com­ sents practical problems since the lesion may missural incision, most of the data were interfere with basic components of the VOR obtained from naive cats. Only one animal or of the OKN adapting stimulation. For ex­ (CF3) was tested both before and after the ample, the vestibular commissural pathway lesion. The others were tested either before plays an important role in the VOR integrat­ (CF2, CS/88, C9/87, C7/88, C4/88, C6/88) ing process (theoretically suggested in 1984 by or after (C16/87, C13/87, C8/87) surgery. Galiana and Outerbridge [IS]). We recently A midsagittal or a parasagittal pontomed­ demonstrated (16) that each time a brainstem ullary brainstem section was performed in 4 incision reached or went past the rostral bor­ cats. A small piece of razor blade was fixed der of the 6 nuclei, all the vestibular commis­ to a guide. The angle between the guide and o sural fibers crossing dorsally at the level of the knife was 13S • The guide was handled the medial vestibular nuclei were interrupted; using a manipulator fixed to a stereotactic the vestibular neural integrator was found to frame. The guide was tilted to be parallel to be disabled without any later recuperation. In the floor of the fourth ventricle. A suboccip­ this context, testing with the classical adapta­ ital craniotomy was performed. The vermis tion procedure could not answer correctly the was gently retracted dorsally in order to ex­ basic question raised about a commissural pose the fourth ventricle. Then, the knife was contribution to adaptation of the VOR. inserted into the brainstem (on the midline or Thus, we must produce a partial commis­ 2 mm laterally), advanced cranially and with­ sural incision, where there is a satisfactory re­ drawn. Care was taken that the guide did not covery of VOR integration; then and only touch the ventricle. Bleeding was slight. An­ then can we apply the adaptation procedure tibiotics and prednisolone were given intra­ to study whether these partially commissural muscularly during the first S postoperative fibers are necessary for VOR gain adaptation. (p.o.) day. Postoperative controls of the ves- Vestibulo-Ocular Adaptation 225 tibular and optokinetic system were performed the adaptation procedure and rotated at a on the 2nd, 7th, and 30th p.o. day. After this steady-state velocity of 30° for the OKN and recovery period, we again tested the adapt a­ OKAN testing procedures. Optokinetic re­ tive ability of these brainstem-Iesioned cats. sponses were quantified by measuring the gain of the OKN during its steady-state and the time constant of OKAN. The time con­ Recording of Eye Movements stant of OKAN was estimated by measuring the time it took for the slow-phase velocity of The eye movement measurement system OKAN to drop to 37070 of its initial value. has a bandwidth of 0 to 1000 Hz and a sensi­ Visual vestibular stimulation was per­ tivity of 0.25°. Eye movements were recorded formed by means of low frequency oscillation simultaneously on an electrostatic recorder in order to remain in the working range of (Gould ES 1000, overall Bandwidth 0 to 1 cat's optokinetic system. Two types of visual­ kHz) and on FM tape. Eye velocity signals vestibular combined stimulation were applied: were also recorded from an analog differen­ 1) 40° or 80° peak-to-peak at 0.05 Hz or 0.10 tiator (0 to 10 Hz). All data were analyzed by Hz, respectively, turntable rotation combined hand from the recorded tracings. Calibration 180° out-of-phase with 40° or 80° peak-to­ was obtained by keeping the untrained cat (in peak screen rotation (out-of-phase combina­ a body box to which the head was fixed) tion). 2) 40° peak-to-peak at 0.05 Hz turntable stockstill in space while the surrounding mag­ rotation combined in phase with 80° peak-to­ netic field was rotated sinusoidally (l Hz; ± peak screen rotation (in-phase combination). 5°) in the horizontal plane. During the cali­ As a measure of the animal's level of alert­ bration procedure, spontaneous sac,cades ness the number of quick phases was con­ were abolished by intramuscular injection of trolled throughout each adaptation period.
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