Functional architecture underlying binocular coordination of eye position and velocity in the larval zebrafish hindbrain

Abstract

BackgroundThe oculomotor integrator (OI) in the vertebrate hindbrain transforms eye velocity input into persistent position coding output, which plays a crucial role in retinal image stability. For a mechanistic understanding of the integrator function and eye position control, knowledge about the tuning of the OI and other oculomotor nuclei is needed. Zebrafish are increasingly used to study integrator function and sensorimotor circuits, yet the precise neuronal tuning to motor variables remains uncharacterized.ResultsHere, we recorded cellular calcium signals while evoking monocular and binocular optokinetic eye movements at different slow-phase eye velocities. Our analysis reveals the anatomical distributions of motoneurons and internuclear neurons in the nucleus abducens as well as those of oculomotor neurons in caudally adjacent hindbrain volumes. Each neuron is tuned to eye position and/or velocity to variable extents and is only activated after surpassing particular eye position and velocity thresholds. While the abducens (rhombomeres 5/6) mainly codes for eye position, in rhombomeres 7/8, a velocity-to-position coding gradient exists along the rostro-caudal axis, which likely corresponds to the oculomotor structures storing velocity and position, and is in agreement with a feedforward mechanism of persistent activity generation. Position encoding neurons are recruited at eye position thresholds distributed across the behaviourally relevant dynamic range, while velocity-encoding neurons have more centred firing thresholds for velocity. In the abducens, neurons coding exclusively for one eye intermingle with neurons coding for both eyes. Many of these binocular neurons are preferentially active during conjugate eye movements and less active during monocular eye movements. This differential recruitment during monocular versus conjugate tasks represents a functional diversification in the final common motor pathway.ConclusionsWe localized and functionally characterized the repertoire of oculomotor neurons in the zebrafish hindbrain. Our findings provide evidence for a mixed but task-specific binocular code and suggest that generation of persistent activity is organized along the rostro-caudal axis in the hindbrain.

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

“…A rich diversity of functional saccade-associated populations are present in the hindbrain and interact in order to generate a wider range of behaviors. Together with the tuning properties of position and low velocity encoding neurons 16 , our findings advance the understanding of larval zebrafish oculomotor behavior at cellular resolution, and suggest coding strategies which may prove to be conserved in other vertebrates.…”

“…Calcium signals of oculomotor neurons are difficult to analyze during nystagmus, since the time points of eye position and eye velocity changes are highly correlated. Therefore, to disambiguate eye velocity and eye position related neural activity 16 , we paused stimulus motion for 5–7 s after automatic detection of a saccade and then switched its direction for both eyes (Fig. 2 d).…”

“…Imaging was carried out at a frequency of 2 Hz, a magnification of 1.5x, and at a wavelength of 920 nm for a duration of 2550 frames. For anatomical registration, we used the same registration framework described in Brysch, Leyden and Arrenberg 16 . Since the Mauthner neurons did not express the calcium indicator in our transgenic line, the gap in expression in rhombomere 4 corresponding to their somata was instead used as the registration landmark.…”

Ramp-to-Threshold Dynamics in a Hindbrain Population Controls the Timing of Spontaneous Saccades

“…This greater sparsity could be related to differences cooperativity in the calcium sensor employed. Second, in comparison to mapping work involving optokinetic behavior (Brysch, Leyden, & Arrenberg, 2019;Portugues et al, 2014), the current mapping provides information on activity associated with the preparation for and initiation of spontaneous saccadic movements. Third, in relation to a mapping effort involving phototactic behavior (Wolf et al, 2017), we observed some similarities in the distribution of position signals (e.g.…”

The tectum/superior colliculus as the vertebrate solution for spatial sensory integration and action

“…Finally, there is a group of tectal neurons tuned to prey-like objects in the frontal visual field, and ablation of these neurons reduces the occurrence of predatory pursuit and tracking 42 . The circuits responsible for the eye movements themselves have been described 187 , but the ways in which tectal information is relayed to the nuclei involved in ocular movements have yet to be fully elucidated.…”