A structural and functional ground plan for neurons in the hindbrain of zebrafish

Abstract

The vertebrate hindbrain contains various sensory-motor networks controlling movements of the eyes, jaw, head, and body. Here we show that stripes of neurons with shared neurotransmitter phenotype that extend throughout the hindbrain of young zebrafish reflect a broad underlying structural and functional patterning. The neurotransmitter stripes contain cell types with shared gross morphologies and transcription factor markers. Neurons within a stripe are stacked systematically by extent and location of axonal projections, input resistance, and age, and are recruited along the axis of the stripe during behavior. The implication of this pattern is that the many networks in hindbrain are constructed from a series of neuronal components organized into stripes that are ordered from top to bottom according to a neuron's age, structural and functional properties, and behavioral roles. This simple organization probably forms a foundation for the construction of the networks underlying the many behaviors produced by the hindbrain.interneuron | locomotion | recruitment | topography T he hindbrain contains a diverse set of sensory-motor networks that control movements required for vision, respiration, mastication, and locomotion in all vertebrates (1, 2). Most often these different networks are studied separately from one another, perhaps because the behaviors are distinct, and the regional differentiation of hindbrain suggests that its several networks might have little in common. Thus, we have strong data for the hindbrain control of eye movements, respiration, and locomotion (3-10), but fewer unifying principles of structural and functional organization that apply across the different networks.Structurally, the hindbrain is divided into segments, called rhombomeres, which differ in the expression of homeotic genes, in the morphological differentiation of neurons, and in their sensory inputs and motor outputs (2, 11). Though there are clear distinctions among rhombomeres, there are indications from previous developmental work using in situ staining for transcription factors and backfilling of hindbrain neurons that there may be structural patterns that cross rhombomere boundaries (12-16). Prior work has also revealed parallels in the development of hindbrain and spinal cord, with the hindbrain sharing features of the now-classic transcription factor code that directs development in spinal cord (17)(18)(19)(20)(21)(22). Though these studies did not explore function because they were performed during early development, they raised the possibility of a broader structuralfunctional patterning that spans rhomobomeres and may underlie the organization of circuits for different behaviors.Here we show that there is indeed a broad structural and functional patterning of neurons in the hindbrain of young zebrafish. The work was initially prompted by a striking patterning observed in earlier work in which we used in situ staining for markers of neurotransmitter phenotype to reveal putative glycinergic, GABAergic, and glutamatergic ...

Visually guided gradation of prey capture movements in larval zebrafish

“…Before doing so, it is worth considering the role of development. The high acuity ventro-temporal region of the retina in 5-7day old larvae is the last to differentiate (Schmitt and Dowling, 1999), as are the networks in the brainstem and spinal cord responsible for the slower locomotor maneuvers used during prey capture (Kimura et al, 2006;Kinkhabwala et al, 2011;McLean et al, 2007;Satou et al, 2012). The sequential emergence of reticulospinal and spinal populations generates a topographic arrangement of cell bodies and their respective dendrites/axons in the neuropil.…”

“…We found that larval zebrafish can systematically bias the speed, intensity and directionality of their movements based on visual cues. Given the known retinotopic organization of the optic tectum (Baier et al, 1996;Niell and Smith, 2005;Stuermer, 1988) and the topographic organization of reticulospinal and spinal networks according to movement strength (Kimura et al, 2006;Kinkhabwala et al, 2011;Koyama et al, 2011;McLean et al, 2007), our observations provide predictions about the interactions between visual, oculomotor and axial networks during prey capture. These findings should help future studies of the neural control of visually guided behaviors in zebrafish.…”

Generation of Multiple Classes of V0 Neurons in Zebrafish Spinal Cord: Progenitor Heterogeneity and Temporal Control of Neuronal Diversity

“…Microinjection of Tol2-based plasmid DNA was performed as described previously (Kawakami, 2004;Urasaki et al, 2006 (Miyasaka et al, 2009;Kani et al, 2010;Kinkhabwala et al, 2011;Koyama et al, 2011) Stochastic labeling of V0 neurons with GFP. For stochastic expression of GFP in V0 neurons, gad1b:lDl-GFP, or huC:lDl-GFP was injected into one to four cell stage embryos of Tg[dbx1b:Cre] stable transgenic fish.…”

Three-dimensional motion tracking reveals a diving component to visual and auditory escape swims in zebrafish larvae

“…Spinal motor circuits are directly controlled by a diverse population of 'descending' neurons in the brain, including reticulospinal neurons (Bretzner and Brownstone, 2013), which have been studied extensively in zebrafish (Kinkhabwala et al, 2011;Stobb et al, 2012). It is likely that specific subsets of descending neurons control vertical swimming direction by coordinating activity of dorsal and ventral muscles to alter the body's pitch angle (upward or downward), while lateral body bends provide propulsion.…”