A distributed saccade-associated network encodes high velocity conjugate and monocular eye movements in the zebrafish hindbrain

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.

Dimensionality reduction reveals separate translation and rotation populations in the zebrafish hindbrain

“…Previous studies 18, 42, 53 looking at eye position and velocity encoding have focused on more ventral areas of the hindbrain, and thus, mostly non-overlapping with areas imaged in the present study. In a recent study 20 , the authors reported neurons active during saccadic eye movements located in rhombomeres 5 and 6; these neurons may partly overlap with our recorded region (see Discussion). The clusters defined here did not clearly overlap with any of the annotated hindbrain nuclei (MPI2, Z-brain), except for some overlap with the facial motor nucleus, and some overlap of ROIs in the green (vergence) cluster with the medial octavolateralis nucleus, and more prominently with the vagal sensory lobe and vagus motor nucleus (MPI2 atlas).…”

“…Monocular and binocular encoding of saccades 20 and eye velocity 18 has recently been described in zebrafish larvae. Although in the latter study a spatial gradient of binocular/monocular activity was described, we did not find such a clear spatial organization (data not shown).…”

“…Evidence for the two hypotheses has remained inconclusive: in the monkey brain, some studies have identified separate areas for conjugate and vergent eye movements 13,14 , while others have pointed to monocular encoding of eye movements [15][16][17] . Similarly, studies in teleost fish find both monocular and binocular encoding of eye position and velocity in all areas of the oculomotor system that have so far been surveyed [18][19][20] .…”

Emergence of time persistence in a data-driven neural network model

“…It is therefore important to develop quantitative, yet interpretable approaches to tackle the functions carried out by large neural populations. The present work is an attempt to do so in the specific context of the anterior rhombencephalic turning region (ARTR), a circuit in the zebrafish larva that shows slow (∼ 10 sec) endogenous alternations between left and right active states driving the gaze orientation and chaining of leftward/rightward swim bouts (Ahrens et al, 2013; Dunn et al, 2016; Wolf et al, 2017; Ramirez & Aksay, 2021; Leyden et al, 2021).…”

“…The present work is an attempt to do so in the specific context of the anterior rhombencephalic turning region (ARTR), a circuit in the zebrafish larva that drives the saccadic dynamics and orchestrates the chaining of leftward/rightward swim bouts ( Ahrens et al, 2013; Dunn et al, 2016; Wolf et al, 2017; Ramirez and Aksay, 2021; Leyden et al, 2021 ). The ARTR spontaneous activity exhibits temporal persistence, i.e.…”