In the absence of visual information, larval zebrafish (Danio rerio) use their mechanosensory lateral line to perform rheotaxis by using flow velocity gradients as navigational cues. Imagine you are a very small fish in the ocean being carried along in a uniform flow in darkness. How do you sense that you are in a flow at all? From your frame of reference you would be stationary. Even so, fish — even very small ones — consistently orientate themselves against the current. So how do they detect the current to begin with? Florian Engert and colleagues show that larval zebra fishes use their mechanosensory lateral line to detect tiny vortices in the water flow, as well as how these vortices evolve with time. This enables them to deduce flow direction. When flying or swimming, animals must adjust their own movement to compensate for displacements induced by the flow of the surrounding air or water1. These flow-induced displacements can most easily be detected as visual whole-field motion with respect to the animal’s frame of reference2. Despite this, many aquatic animals consistently orient and swim against oncoming flows (a behaviour known as rheotaxis) even in the absence of visual cues3,4. How animals achieve this task, and its underlying sensory basis, is still unknown. Here we show that, in the absence of visual information, larval zebrafish (Danio rerio) perform rheotaxis by using flow velocity gradients as navigational cues. We present behavioural data that support a novel algorithm based on such local velocity gradients that fish use to avoid getting dragged by flowing water. Specifically, we show that fish use their mechanosensory lateral line to first sense the curl (or vorticity) of the local velocity vector field to detect the presence of flow and, second, to measure its temporal change after swim bouts to deduce flow direction. These results reveal an elegant navigational strategy based on the sensing of flow velocity gradients and provide a comprehensive behavioural algorithm, also applicable for robotic design, that generalizes to a wide range of animal behaviours in moving fluids.

/pdf/a-novel-mechanism-for-mechanosensory-based-rheotaxis-in-3adfmcecmy.pdf

A novel mechanism for mechanosensory-based rheotaxis in larval zebrafish

The Gems of the Past: A Brief History of Lateral Line Research in the Context of the Hearing Sciences.- Morphological Diversity, Development, and Evolution of the Mechanosensory Lateral Line System.- The Hydrodynamic of Flow Stimuli.- The Biophysics of the Fish Lateral Line.- Sensory Ecology and Neuroethology of the Lateral Line.- Information Encoding and Processing by the Peripheral Lateral Line System.- The Central Nervous Organization of the Lateral Line System.- Central Processing of Lateral Line Information.- Functional Overlap and Nonoverlap Between Lateral Line and Auditory Systems.- The Hearing Loss, Protection, and Regeneration in the Larval Zebrafish Lateral Line.

The lateral line system

The rhythmic firing behavior of spinal motoneurons is a function of their electrical properties and synaptic inputs. However, the relative contribution of endogenous versus network-based rhythmogenic mechanisms to locomotion is unclear. To address this issue, we have recorded from identified motoneurons and compared their current-evoked firing patterns to network-driven ones in the larval zebrafish ( Danio rerio ). Zebrafish axial motoneurons are recruited topographically from the bottom of the spinal cord up. Here, we have explored differences in the morphology of axial motoneurons, their electrical properties, and their synaptic drive, to reveal how they match the topographic pattern of recruitment. More ventrally located “secondary” motoneurons generate bursts of action potentials in response to constant current steps, demonstrating a strong inherent rhythmogenesis. The membrane potential oscillations underlying bursting behavior occur in the normal frequency range of swimming. In contrast, more dorsal secondaries chatter in response to current, while the most dorsally distributed “primary” motoneurons all fire tonically. We find that systematic variations in excitability and endogenous rhythmicity are inversely related to the level of oscillatory synaptic drive within the entire axial motor pool. Specifically, bursting cells exhibit the least amount of drive, while tonic cells exhibit the most. Our data suggest that increases in swimming frequency are accomplished by the recruitment of axial motoneurons that progressively rely on instructive synaptic drive to shape their oscillatory activity appropriately. Thus, within the zebrafish spinal cord, there are differences in the relative contribution of endogenous versus network-based rhythms to locomotion and these vary predictably according to order of recruitment.

https://www.jneurosci.org/content/jneuro/32/32/10925.full.pdf

A Gradient in Endogenous Rhythmicity and Oscillatory Drive Matches Recruitment Order in an Axial Motor Pool

Zebrafish are a unique cell to behavior model for studying the basic biology of human inherited neurological conditions. Conserved vertebrate genetics and optical transparency provide in vivo access to the developing nervous system as well as high-throughput approaches for drug screens. Here we review zebrafish modeling for two broad groups of inherited conditions that each share genetic and molecular pathways and overlap phenotypically: neurodevelopmental disorders such as Autism Spectrum Disorders (ASD), Intellectual Disability (ID) and Schizophrenia (SCZ), and neurodegenerative diseases, such as Cerebellar Ataxia (CATX), Hereditary Spastic Paraplegia (HSP) and Charcot-Marie Tooth Disease (CMT). We also conduct a small meta-analysis of zebrafish orthologs of high confidence neurodevelopmental disorder and neurodegenerative disease genes by looking at duplication rates and relative protein sizes. In the past zebrafish genetic models of these neurodevelopmental disorders and neurodegenerative diseases have provided insight into cellular, circuit and behavioral level mechanisms contributing to these conditions. Moving forward, advances in genetic manipulation, live imaging of neuronal activity and automated high-throughput molecular screening promise to help delineate the mechanistic relationships between different types of neurological conditions and accelerate discovery of therapeutic strategies.

/pdf/function-over-form-modeling-groups-of-inherited-neurological-4wl871lr7x.pdf

Function Over Form: Modeling Groups of Inherited Neurological Conditions in Zebrafish

Aquatic animals of all major phyla have developed sensory systems to perceive water movements, so-called hydrodynamic sensory systems. These water movements, or hydrodynamic stimuli, arise from a variety of sources. Some sources of hydrodynamic stimuli are biotic, such as predators, prey, and conspecifics, some are abiotic, such as wind, gravity that induces currents, and others. We have only relatively recently begun to take a closer look at these hydrodynamic stimuli with regard to the question how they may have formed the hydrodynamic sensory systems of aquatic animals during evolution. Hydrodynamic stimuli are measured with several different techniques, some of which are invasive, meaning that a sensor is inserted into the flow, some are noninvasive, such as optical and acoustical techniques. The laser-based technique of particle image velocimetry (PIV) has proven especially helpful. It is an optical technique that measures flow velocities not only in a single point, but simultaneously in hundreds or thousands of points in a selected layer of the fluid, and with more advanced modifications of the technique, even in a limited volume. Furthermore, the laser-based technique of laser Doppler velocimetry has contributed much to our understanding. In this chapter, naturally occurring hydrodynamic stimuli measured with these and other techniques are discussed, along with the advantages and shortcomings of the different experimental approaches.

Flow Sensing in Air and Water

Spatially distributed sensory information is topographically mapped in the brain by point-to-point correspondence of connections between peripheral receptors and central target neurons. In fishes, for example, the axonal projections from the mechanosensory lateral line organize a somatotopic neural map. The lateral line provides hydrodynamic information for intricate behaviors such as navigation and prey detection. It also mediates fast startle reactions triggered by the Mauthner cell. However, it is not known how the lateralis neural map is built to subserve these contrasting behaviors. Here we reveal that birth order diversifies lateralis afferent neurons in the zebrafish. We demonstrate that early- and late-born lateralis afferents diverge along the main axes of the hindbrain to synapse with hundreds of second-order targets. However, early-born afferents projecting from primary neuromasts also assemble a separate map by converging on the lateral dendrite of the Mauthner cell, whereas projections from secondary neuromasts never make physical contact with the Mauthner cell. We also show that neuronal diversity and map topology occur normally in animals permanently deprived of mechanosensory activity. We conclude that neuronal birth order correlates with the assembly of neural submaps, whose combination is likely to govern appropriate behavioral reactions to the sensory context.

https://www.jneurosci.org/content/jneuro/32/9/2976.full.pdf

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

Establishing topographical maps of the external world is an important but still poorly understood feature of the vertebrate sensory system. To study the selective innervation of hindbrain regions by sensory afferents in the zebrafish embryo, we mapped the fine-grained topographical representation of sensory projections at the central level by specific photoconversion of sensory neurons. Sensory ganglia located anteriorly project more medially than do ganglia located posteriorly, and this relates to the order of sensory ganglion differentiation. By single-plane illumination microscopy (SPIM) in vivo imaging, we show that (1) the sequence of arrival of cranial ganglion inputs predicts the topography of central projections, and (2) delaminated neuroblasts differentiate in close contact with the neural tube, and they never loose contact with the neural ectoderm. Afferent entrance points are established by plasma membrane interactions between primary differentiated peripheral sensory neurons and neural tube border cells with the cooperation of neural crest cells. These first contacts remain during ensuing morphological growth to establish pioneer axons. Neural crest cells and repulsive slit1/robo2 signals then guide axons from later-differentiating neurons toward the neural tube. Thus, this study proposes a new model by which the topographical representation of cranial sensory ganglia is established by entrance order, with the entry points determined by cell contact between the sensory ganglion cell bodies and the hindbrain.

/pdf/the-order-and-place-of-neuronal-differentiation-establish-972vui1hjb.pdf

The Order and Place of Neuronal Differentiation Establish the Topography of Sensory Projections and the Entry Points within the Hindbrain

Reconstructing the lineage of cells is central to understanding how the wide diversity of cell types develops. Here, we provide the neurosensory lineage reconstruction of a complex sensory organ, the inner ear, by imaging zebrafish embryos in vivo over an extended timespan, combining cell tracing and cell fate marker expression over time. We deliver the first dynamic map of early neuronal and sensory progenitor pools in the whole otic vesicle. It highlights the remodeling of the neuronal progenitor domain upon neuroblast delamination, and reveals that the order and place of neuroblasts' delamination from the otic epithelium prefigure their position within the SAG. Sensory and non-sensory domains harbor different proliferative activity contributing distinctly to the overall growth of the structure. Therefore, the otic vesicle case exemplifies a generic morphogenetic process where spatial and temporal cues regulate cell fate and functional organization of the rudiment of the definitive organ.

Distribution of neurosensory progenitor pools during inner ear morphogenesis unveiled by cell lineage reconstruction

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Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

The Order and Place of Neuronal Differentiation Establish the Topography of Sensory Projections and the Entry Points within the Hindbrain

Distribution of neurosensory progenitor pools during inner ear morphogenesis unveiled by cell lineage reconstruction