Differential effect of injections of kainic acid into the prepositus and the vestibular nuclei of the cat.

Abstract

SUMMARY1. In order adequately to control eye movements, oculomotoneurones have to be supplied with both an eye-velocity signal and an eye-position signal. However, all the command signals of the oculomotor system are velocity signals. Nowadays, there is general agreement about the existence of a brainstem network that would convert velocity command-signals into an eye-position signal. This circuit, because of its function, is called the oculomotor neural integrator. The most obvious symptom of its eventual failure is a gaze-holding deficit: in this case, saccades are followed by a centripetal post-saccadic drift. Although the oculomotor neural integrator is central in oculomotor theory, its precise location is still a matter for debate.2. Previously, microinjections of kainic acid (KA) into the region of the nucleus prepositus hypoglossi (NPH) and of the medial vestibular nucleus (MVN) were found to induce a horizontal gaze-holding failure both in the cat and in the monkey.However, the relatively large volumes (1-3 pl) and concentrations (2-4 ,ug j#ll) used in these injections made it difficult to know if the observed deficit was due to a disturbance of the NPH or of the nearby MVN. These considerations led us to inject very small amounts of kainic acid (50 nl, 0.1 jtg jtl-) either into the rostral part of the MVN or into different sites along the NPH of the cat.3. The search coil technique was used to record (1) spontaneous eye movements (2) the vestibulo-ocular reflex (VOR) induced by a constant-velocity rotation (50 deg s-1 for 40 s) and the optokinetic nystagmus (OKN) elicited by rotating an optokinetic drum at 30 deg s-1 for 40 s.4. In each injection experiment, the location of the abducens nucleus of the alert cat was mapped out by recording the antidromic field potentials evoked by the stimulation of the abducens nerve. Two micropipettes were then glued together in such a way that when the tip of the recording micropipette was in the centre of the abducens nucleus the tip of the injection micropipette was in a target area. The twin pipettes were then lowered in the brainstem until the recording micropipette reached the centre of the abducens nucleus. Kainic acid was then injected into the brainstem of the alert cat through the injection micropipette by an air pressure system. 5. Carried out according to such a protocol, KA injections into the NPH or the rostral part of the MVN consistently led to specific eye-movement changes. A unilateral injection into the NPH caused a bilateral horizontal gaze-holding failure MS 2099 E. GODAUX, P. METTENS AND G. CHERON without any spontaneous nystagmus or any significant deviation of the null-position of the gaze. A unilateral injection into the rostral MVN, for its part, induced a nystagmus whose slow phases were linear and directed to the contralateral side. No gaze-holding deficit accompanied this vestibular imbalance.6. Taken together with the data from the literature showing that the principal signal carried by the neurones of the NPH is an eye-position signal,...

How the brain keeps the eyes still

“…Vestibular nystagmus (fast unidirectional drift) is often caused by unilateral damage to the vestibular nerve or semicircular canals. Pharmacological inactivation of the MVN or PH can produce centripetal or unidirectional ocular drift (9,(14)(15)(16)(17)(18)(19). Some patients with cerebellar disease suffer from centrifugal ocular drift away from a null position, suggesting a memory state space with a saddle point, as shown in Fig.…”

“…Stimulation of the MVN or PH causes persistent changes in eye position (9)(10)(11). Electrolytic lesion (12,13) or pharmacological inactivation (9,(14)(15)(16)(17)(18)(19) of these areas causes the disorder gazeevoked nystagmus. Such experimental results indicate that these premotor neurons are part of the network that stores the memory of eye position.…”

“…After saccades to other positions, the eyes drift back toward the null position, in a disorder known as gaze-evoked nystagmus (1). Localization studies suggest that the memory of eye position is stored in a neural network that extends over several areas in the brainstem and cerebellum (2)(3)(4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19).…”

Mechanisms of Action and Targets of Nitric Oxide in the Oculomotor System

“…Depending on the target, velocity imbalance and/or integration deficit will occur, leading to well characterized abnormal eye movements (C annon and Robinson, 1987;Godaux et al, 1993;Mettens et al, 1994;Pastor et al, 1994;Godaux and Cheron, 1996), which are schematically represented in Figure 1. Each PH nucleus simultaneously receives excitatory and inhibitory signals from the contralateral and ipsilateral M V nuclei, respectively (Baker and Berthoz, 1975).…”

Three-Dimensional Eye–Head Coordination After Injection of Muscimol Into the Interstitial Nucleus of Cajal (INC)

“…The nucleus prepositus hypoglossi (NPH) was previously shown to function as the neural integrator for horizontal eye movements (Cannon and Robinson 1987;Godaux et al 1993;McFarland and Fuchs 1992). A number of studies showed that the mesencephalic interstitial nucleus of Cajal (INC) is the neural integrator for vertical and torsional components of eye movements (Crawford 1994;Crawford and Vilis 1993;Fukushima 1987;Fukushima et al 1990;Helmchen et al 1998;King et al 1981;Ranalli et al 1988).…”