Extraocular motoneuron pools develop along a dorsoventral axis in zebrafish, Danio rerio

Abstract

Both spatial and temporal cues determine the fate of immature neurons. A major challenge at the interface of developmental and systems neuroscience is to relate this spatiotemporal trajectory of maturation to circuit‐level functional organization. This study examined the development of two extraocular motor nuclei (nIII and nIV), structures in which a motoneuron's identity, or choice of muscle partner, defines its behavioral role. We used retro‐orbital dye fills, in combination with fluorescent markers for motoneuron location and birthdate, to probe spatial and temporal organization of the oculomotor (nIII) and trochlear (nIV) nuclei in the larval zebrafish. We describe a dorsoventral organization of the four nIII motoneuron pools, in which inferior and medial rectus motoneurons occupy dorsal nIII, while inferior oblique and superior rectus motoneurons occupy distinct divisions of ventral nIII. Dorsal nIII motoneurons are, moreover, born before motoneurons of ventral nIII and nIV. The order of neurogenesis can therefore account for the dorsoventral organization of nIII and may play a primary role in determining motoneuron identity. We propose that the temporal development of extraocular motoneurons plays a key role in assembling a functional oculomotor circuit. J. Comp. Neurol. 525:65–78, 2017. © 2016 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

Ontogenetic Development of Vestibulo-Ocular Reflexes in Amphibians

“…Within the anuran oculomotor nucleus, situated immediately rostral to the midbrain-hindbrain boundary, individual eye muscle-specific populations (MR, SR, IR, IO motoneurons) are arranged in a partially segregated manner (Matesz and Székely, 1977). This spatial organization is reminiscent of the birth date-related pattern recently described for zebrafish oculomotor and trochlear motoneurons (Greaney et al, 2016). In contrast to the midbrain origin of oculomotor motoneurons, trochlear and abducens motoneurons in anurans originate from rostral r1 and from r5, respectively (Straka et al, 1998, 2006).…”

Key Features of Structural and Functional Organization of Zebrafish Facial Motor Neurons Are Resilient to Disruption of Neuronal Migration

“…In larval zebrafish, spinal cord [20,21] and hindbrain [4,21–23] motor and interneurons are organized topographically by age along the dorsoventral axis, and the dorsoventral location of the soma correlates with key functional properties such as recruitment order and axon morphology [4,21,24]. This led us to use transgenic expression of the photo convertible protein Dendra2 to determine if facial motor neurons were organized according to relative age, and if this age topography was still established in caudal migration mutants.…”

Temporal transcription factors determine circuit membership by permanently altering motor neuron-to-muscle synaptic partnerships

“…The class of molecules termed temporal transcription factors are poised to be key upstream regulators of the decisions that determine circuit membership. This is because in many systems there is a strong association between the birth time of a neuron and its ultimate circuit membership, and because temporal transcription factors have been postulated to control entire time-linked developmental programs (Bhansali et al, 2014;Deguchi et al, 2011;Eerdunfu et al, 2017;Greaney et al, 2017;Jefferis et al, 2001;Kulkarni et al, 2016;McLean et al, 2007;McLean and Fetcho, 2009;Morrow et al, 2008;Osterhout et al, 2014;Petrovic and Hummel, 2008;Pujol-Martí et al, 2012;Tripodi et al, 201;Doe 2017, Li et al 2013, Suzuki et al 2013, EIliott et al, 2008, Alsio et al, 2013, Allan and Thor, 2015. If temporal transcription factors control entire time-linked developmental programs, this would include all of the decisions that a neuron makes during development to establish circuit membership.…”