Dynamic Coding of Vertical Facilitated Vergence by Premotor Saccadic Burst Neurons

Abstract

Van Horn MR, Cullen KE. Dynamic coding of vertical facilitated vergence by premotor saccadic burst neurons. J Neurophysiol 100: 1967-1982. First published July 23, 2008 doi:10.1152/jn.90580.2008. To redirect our gaze in three-dimensional space we frequently combine saccades and vergence. These eye movements, known as disconjugate saccades, are characterized by eyes rotating by different amounts, with markedly different dynamics, and occur whenever gaze is shifted between near and far objects. How the brain ensures the precise control of binocular positioning remains controversial. It has been proposed that the traditionally assumed "conjugate" saccadic premotor pathway does not encode conjugate commands but rather encodes monocular commands for the right or left eye during saccades. Here, we directly test this proposal by recording from the premotor neurons of the horizontal saccade generator during a dissociation task that required a vergence but no horizontal conjugate saccadic command. Specifically, saccadic burst neurons (SBNs) in the paramedian pontine reticular formation were recorded while rhesus monkeys made vertical saccades made between near and far targets. During this task, we first show that peak vergence velocities were enhanced to saccade-like speeds (e.g., Ͼ150 vs. Ͻ100°/s during saccade-free movements for comparable changes in vergence angle). We then quantified the discharge dynamics of SBNs during these movements and found that the majority of the neurons preferentially encode the velocity of the ipsilateral eye. Notably, a given neuron typically encoded the movement of the same eye during horizontal saccades that were made in depth. Taken together, our findings demonstrate that the brain stem saccadic burst generator encodes integrated conjugate and vergence commands, thus providing strong evidence for the proposal that the classic saccadic premotor pathway controls gaze in three-dimensional space. I N T R O D U C T I O NTo quickly and accurately redirect our gaze between near and far targets, we typically combine saccadic and vergence eye movements. During such eye movements, termed disconjugate saccades, the eyes rotate by different angles and with different trajectories to precisely realign the two visual axes on the new target of interest. Traditionally, disconjugate saccades were thought to be controlled by linear summation of premotor commands from two distinct neural control pathways that separately encode the conjugate and vergence components of eye motion: 1) a conjugate saccadic subsystem, which commands a rapid but yoked movement of the two eyes in a given direction; and 2) a separate vergence subsystem, which rotates the eyes in opposite directions to ensure accurate binocular positioning (Hering 1977; Mays 1984Mays , 1998. Accordingly, the premotor circuitry involved in generating horizontal saccades (e.g., the saccadic burst neurons [SBNs] of the paramedian pontine reticular formation [PPRF]) was generally assumed to provide the command to drive the horizontal conjugate compone...

Comment le cerveau contrôle-t-il les mouvements des yeux ? Les neurones moteurs et prémoteurs du tronc cérébral

“…En ré sumé , l'approche de King et Zhou [57,59,60,65,66], ainsi que de l'é quipe de Cullen [61][62][63][64][68][69][70] et de Chen et al, est innovante. Les neurones pré moteurs supposé s coder des commandes binoculaires pourraient, en fait, coder un signal monoculaire, tandis que les motoneurones supposé s coder une commande monoculaire pourraient, en ré alité , coder un signal binoculaire (Fig.…”

“…Une telle hypothè se se fonda sur les dé couvertes neurophysiologiques des mê mes auteurs, et furent corroboré es et é tendues par Cullen et al [61][62][63][64][68][69][70]. Par ailleurs, le modè le suggé ra l'existence d'une voie directe entre l'inté grateur neuronal et les neurones toniques de convergence (NTC), ce qui à ce jour et à notre connaissance n'a pas é té confirmé au plan neuroanatomique.…”

“…La dé couverte de King et Zhou fut confirmé e et é tendue ulté rieurement par le laboratoire de Cullen [61][62][63][64]. Sylvestre et al [61] examinè rent le rô le de neurones phasiques-toniques situé s dans le NPH et le NVM (rappelons que ces noyaux font partie de la circuiterie saccadique pré motrice) dans la gé né ration des saccades conjugué es, mais aussi des saccades disconjugué es et de la fixation.…”

“…De maniè re importante, la majorité des NPS codaient pré fé rentiellement les caracté ristiques dynamiques d'un oeil individuel pendant les saccades disconjugué es. Dans une autre é tude, Van Horn et Cullen [62] testè rent à nouveau si la circuiterie pré motrice saccadique code, non pas des commandes conjugué es, mais des commandes monoculaires pour l'un ou l'autre oeil. Ils enregistrè rent chez le singe les NPS du gé né rateur saccadique du tronc cé ré bral (NPE et NPI inclus).…”

“…Là encore, la majorité des NPS codent pré fé rentiellement la vitesse de l'oeil ipsilaté ral. Au total, il ressort de ces é tudes [61][62][63] la preuve que les commandes des neurones pré moteurs de la circuiterie, dite saccadique, du tronc cé ré bral sont suffisantes pour assurer des dé placements du regard dans l'espace 3D.…”