Neurophysiology of visually guided eye movements: critical review and alternative viewpoint

Abstract

In this article, we perform a critical examination of assumptions that led to the assimilation of measurements of the movement of a rigid body in the physical world to parameters encoded within brain activity. In many neurophysiological studies of goal-directed eye movements, equivalence has indeed been made between the kinematics of the eyes or of a targeted object and the associated neuronal processes. Such a way of proceeding brings up the reduction encountered in projective geometry when a multidimensional object is being projected onto a one-dimensional segment. The measurement of a movement indeed consists of generation of a series of numerical values from which magnitudes such as amplitude, duration, and their ratio (speed) are calculated. By contrast, movement generation consists of activation of multiple parallel channels in the brain. Yet, for many years, kinematic parameters were supposed to be encoded in brain activity, even though the neuronal image of most physical events is distributed both spatially and temporally. After explaining why the "neuronalization" of such parameters is questionable for elucidating the neural processes underlying the execution of saccadic and pursuit eye movements, we propose an alternative to the framework that has dominated the last five decades. A viewpoint is presented in which these processes follow principles that are defined by intrinsic properties of the brain (population coding, multiplicity of transmission delays, synchrony of firing, connectivity). We propose reconsideration of the time course of saccadic and pursuit eye movements as the restoration of equilibria between neural populations that exert opposing motor tendencies.

Keywords: equilibrium; model; pursuit; saccade; symmetry.

Fig. 1.

Visual fixation as equilibrium. A saccade may not be launched if the visuo-oculomotor system is within a mode where opposite commands (presumably issued by the left and right superior colliculi) counterbalance each other. The initiation of a slow eye movement could involve the same symmetry breaking, although with different groups of neurons (see text).

Fig. 2.

Nystagmus observed after injection of a small amount of muscimol (0.6 µl) in the left nucleus of the optic tract (NOT). The eye drifts horizontally toward the contralesional side until a saccade is made toward the left. The unilateral suppression of NOT signals causes an imbalance of visual input to the nucleus prepositus hypoglossi, which itself affects the balance of tonic input onto the abducens motor neurons. Exp. 1 and Exp. 2 refer to two experimental sessions made on different days.

Fig. 3.

Typical oculomotor behavior of a monkey tracking a visual target moving horizontally with a constant speed. The horizontal eye position is plotted as a function of time after target motion onset for 3 trials recorded during the first (Beginning, left) and last (End, right) training sessions. The time course of horizontal target position is illustrated by the dashed line. The selected trials were recorded in 5 monkeys (from top to bottom, monkeys A, B, C, M, and G) when the target moved in the upper right quadrant with a constant speed (20°/s). During the other randomly interleaved trials, the target moved similarly, horizontally and away from the vertical meridian, but in the lower right, the lower left, or the upper left quadrant. Additional methodological information can be found in Bourrelly et al. (2016).