Recruitment orders underlying binocular coordination of eye position and velocity in the larval zebrafish hindbrain

Abstract

24Background: 25 The oculomotor integrator (OI) in the vertebrate hindbrain transforms eye velocity input into 26 persistent position coding output, which plays a crucial role in retinal image stability. For a 27 mechanistic understanding of the integrator function and eye position control, knowledge 28 about the tuning of the OI and other oculomotor nuclei is needed. Zebrafish are increasingly 29 used to study integrator function and sensorimotor circuits, yet the precise neuronal tuning 30 to motor variables remains uncharacterized. 31 32 Results: 33 Here, we recorded cellular calcium signals while evoking monocular and binocular optokinetic 34 eye movements at different slow-phase eye velocities. Our analysis reveals the anatomical 35 distributions of motoneurons and internuclear neurons in the nucleus abducens as well as 36 those of oculomotor neurons in caudally adjacent hindbrain volumes. Each neuron is tuned 37 to eye position and/or velocity to variable extents and is only activated after surpassing 38 particular eye position and velocity thresholds. While the abducens (rhombomeres 5/6) 39 mainly codes for eye position, in rhombomeres 7/8 a velocity-to-position coding gradient 40 exists along the rostro-caudal axis, which likely corresponds to the velocity and position 41 storage mechanisms. Position encoding neurons are recruited at eye position thresholds 42 distributed across the behavioral dynamic range, while velocity encoding neurons have more 43 centered firing thresholds for velocity. In the abducens, neurons coding exclusively for one 44 eye intermingle with neurons coding for both eyes. Many of these binocular neurons are 45 preferentially active during conjugate eye movements, which represents a functional 46 diversification in the final common motor pathway. 47 3Conclusions: 48 We localized and functionally characterized the repertoire of oculomotor neurons in the 49 zebrafish hindbrain. Our findings provide evidence for a mixed but task-specific binocular 50 code and suggest that generation of persistent activity is organized along the rostro-caudal 51 axis in the hindbrain.The oculomotor system is responsible for moving the eyes in vertebrates and is highly 71 conserved across species. Zebrafish are increasingly used to improve our understanding of 72 the oculomotor population code and eye movement control [1]- [6]. 73 The oculomotor system for horizontal eye movements consists of multiple elements (Fig. 1a). 74 It is responsible for generating and maintaining stable eye positions as well as eye movements 75 during saccades, optokinetic and vestibulo-ocular reflexes (OKR, VOR), and other behaviours. 76 The lateral and medial rectus (LR, MR), which represent the extraocular eye muscles 77 responsible for horizontal eye movements, are controlled by motoneurons (MN) in the 78 nucleus abducens (ABN) and the oculomotor nucleus (OMN), respectively. The OMN MNs are 79 activated by internuclear neurons (INN) residing in the contralateral ABN. The ABN receives 80 input from...

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

“…All data generated or analysed during this study are included in this published article and its supplementary information files. Data and analysis algorithms used in this study have been uploaded to the public repository G-Node GIN and can be accessed via 10.12751/g-node.6521de [76]. Additional materials (e.g.…”