Abstract
Saccades are rapid eye movements that redirect gaze. Their magnitudes and directions are tightly controlled by the oculomotor system, which is capable of generating conjugate, monocular, convergent and divergent saccades. Recent studies suggest a mainly monocular control of saccades in mammals, although the development of binocular control and the interaction of different functional populations is less well understood. For zebrafish, a well-established model in sensorimotor research, the nature of binocular control in this key oculomotor behavior is unknown. Here, we use the optokinetic response and calcium imaging to characterize how the developing zebrafish oculomotor system encodes the diverse repertoire of saccades. We find that neurons with phasic saccade-associated activity (putative burst neurons) are most frequent in dorsal regions of the hindbrain and show elements of both monocular and binocular encoding, revealing a mix of the response types originally hypothesized by Helmholtz and Hering. Additionally, we observed a certain degree of behavior-specific recruitment in individual neurons. Surprisingly, calcium activity is only weakly tuned to saccade size. Instead, saccade size is apparently controlled by a push–pull mechanism of opposing burst neuron populations. Our study reveals the basic layout of a developing vertebrate saccade system and provides a perspective into the evolution of the oculomotor system.
Highlights
Saccades are rapid eye movements that redirect gaze
We identified putative burst neurons in the hindbrain and found that neural recruitment was biased towards certain saccade types for each neuron, suggesting a certain level of binocular and monocular saccade-type specificity across putative burst neuron populations, which is neither in line with Helmholtz’s nor Hering’s hypotheses
In this study we investigated the monocular and binocular encoding of horizontal saccades within the hindbrain using calcium imaging in semi-restrained zebrafish larvae during optokinetic behavior (Fig. 2a)
Summary
Saccades are rapid eye movements that redirect gaze. Their magnitudes and directions are tightly controlled by the oculomotor system, which is capable of generating conjugate, monocular, convergent and divergent saccades. The ability of the oculomotor system to generate two such behaviorally distinct states, one characterized by bilaterally coupled gaze interspersed with fast reorienting conjugate eye movements (saccades), the other by uniocular independence, provides hints towards the underlying circuits, which are not yet fully understood. The majority of saccades are conjugate, and it is difficult to determine whether they are executed via a single neural command sent to both eyes (argued by Ewald Hering and known as “Hering’s Law of equal innervation”), or via two individual commands defined by separate systems but performed synchronously (suggested by Hermann von Helmholtz) This debate has provided a framework for much of the research into conjugate and vergence eye movements in monkey (reviewed in[5,6,7]). Debowy and Baker[17] found that the adult goldfish velocity-to-position neural integrator for horizontal eye movements contained both monocular and conjugate neurons
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