The development of the hindbrain afferent projections in the axolotl: Evidence for timing as a specific mechanism of afferent fiber sorting

Fritzsch, Bernd; Gregory, Darin R.; Rosa‐Molinar, Eduardo

doi:10.1016/j.zool.2005.08.003

Cited by 29 publications

(47 citation statements)

References 36 publications

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“…Secondary neuromasts, by contrast, only project late-born neurons that do not converge on the Mauthner. A potentially equivalent relationship between developmental timing and neuronal projection patterns has been reported for the segregation of afferent projections for the otic, lateralis and ampullary organs in the axolotl (Fritzsch et al, 2005). In this case, however, the relationship is between organs rather than within each organ.…”

Section: Discussionmentioning

confidence: 55%

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

Pujol-Martí¹,

Zecca²,

Baudoin³

et al. 2012

J. Neurosci.

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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.

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Section: Discussionmentioning

confidence: 55%

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

Pujol-Martí¹,

Zecca²,

Baudoin³

et al. 2012

J. Neurosci.

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“…An important question arising from this work is whether the degree of predetermination that we have observed peripherally also extends to the central projections (39). If afferent neurons use a molecular code to distinguish between hair-cell polarities, does this same code function in the hindbrain to organize polarity-specific sensory pathways (40)?…”

Section: Discussionmentioning

confidence: 94%

Activity-independent specification of synaptic targets in the posterior lateral line of the larval zebrafish

Nagiel

Patel

Andor-Ardó

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

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The development of functional neural circuits requires that connections between neurons be established in a precise manner. The mechanisms by which complex nervous systems perform this daunting task remain largely unknown. In the posterior lateral line of larval zebrafish, each afferent neuron forms synaptic contacts with hair cells of a common hair-bundle polarity. We investigated whether afferent neurons distinguish hair-cell polarities by analyzing differences in the synaptic signaling between oppositely polarized hair cells. By examining two mutant zebrafish lines with defects in mechanoelectrical transduction, and by blocking transduction during the development of wild-type fish, we found that afferent neurons could form specific synapses in the absence of stimulus-evoked patterns of synaptic release. Asking next whether this specificity arises through intrinsically generated patterns of synaptic release, we found that the polarity preference persisted in two mutant lines lacking essential synaptic proteins. These results indicate that lateral-line afferent neurons do not require synaptic activity to distinguish hair-cell polarities and suggest that molecular labels of hair-cell polarity guide prepatterned afferents to form the appropriate synapses.calcium channel ͉ hair cell ͉ neuromast ͉ planar cell polarity ͉ protocadherin A n essential feature of neural development is the establishment of specific synaptic connections. To form the appropriate contacts, each growing axon must respond to guidance cues, find its target region, and then establish synapses with specific target cells (1, 2). The first two of these steps-axonal guidance and target recognition-rely predominantly on molecular signposts that attract or repulse growth cones in a manner independent of neuronal activity (3, 4). How neurons decide to form stable synapses with particular target cells, however, remains unclear. Activity serves an important role in regulating the growth of axonal arbors and in selectively stabilizing synapses (5-8). In several vertebrate systems, axons form synapses diffusely within the target region and then undergo activitydependent pruning to eliminate inappropriate synapses (9-14). Hebb's postulate, by which correlated activity between synaptic partners strengthens connections (15,16), offers an attractive model to explain this phenomenon (17). Nevertheless, the evidence for an activity-dependent process must be reconciled with data suggesting that normal brain architecture can form in the absence of synaptic transmission (18)(19)(20). In this case, synaptic specificity could derive from a combinatorial code of cell-surface molecules such as cadherins (21) or members of the immunoglobin superfamily (22). These fundamental uncertainties highlight the need for in vivo studies in an experimentally tractable vertebrate system.The posterior lateral line of zebrafish permits a detailed analysis of the role of activity in establishing synaptic specificity. The larval posterior lateral line consists of superficial clusters ...

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“…1 a). Developmental segregation of afferents from the different inner ear or lateral line end organs generates precise projections into modality-specific, evolutionarily conserved central target regions [Rubel and Fritzsch, 2002;Fritzsch et al, 2005;Maklad et al, 2010]. Thus, vestibular afferents terminate on specific central neuronal populations, primarily within the differ-ent vestibular subnuclei ( fig.…”

Section: Evolving An Ear and Connecting It To The Hindbrainmentioning

confidence: 99%

“…The specific connections from vestibular afferents to central vestibular neurons might be genetically preprogrammed [Fritzsch et al, 2005;Maklad et al, 2010] or determined retrogradely by the prior established connectivity of vestibular projection neurons with extraocular motoneuron targets [Glover, 2003;Straka, 2010]. Indeed, developmental studies in the chicken embryo show that as soon as synaptic contacts between vestibulo-ocular neurons and extraocular motoneurons are made, there is functional specificity within the VOR circuit spanning from afferents to projection neurons to motoneurons [Glover, 2003;Glover et al, unpubl.…”

Section: Regionalizing Vestibular Projection Neurons To Define the Flmentioning

confidence: 99%

Connecting Ears to Eye Muscles: Evolution of a ‘Simple' Reflex Arc

2014

Self Cite

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Developmental and evolutionary data from vertebrates are beginning to elucidate the origin of the sensorimotor pathway that links gravity and motion detection to image-stabilizing eye movements - the vestibulo-ocular reflex (VOR). Conserved transcription factors coordinate the development of the vertebrate ear into three functional sensory compartments (graviception/translational linear acceleration, angular acceleration and sound perception). These sensory components connect to specific populations of vestibular and auditory projection neurons in the dorsal hindbrain through undetermined molecular mechanisms. In contrast, a molecular basis for the patterning of the vestibular projection neurons is beginning to emerge. These are organized through the actions of rostrocaudally and dorsoventrally restricted transcription factors into a ‘hodological mosaic' within which coherent and largely segregated subgroups are specified to project to different targets in the spinal cord and brain stem. A specific set of these regionally diverse vestibular projection neurons functions as the central element that transforms vestibular sensory signals generated by active and passive head and body movements into motor output through the extraocular muscles. The large dynamic range of motion-related sensory signals requires an organization of VOR pathways as parallel, frequency-tuned, hierarchical connections from the sensory periphery to the motor output. We suggest that eyes, ears and functional connections subserving the VOR are vertebrate novelties that evolved into a functionally coherent motor control system in an almost stereotypic organization across vertebrate taxa.

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The development of the hindbrain afferent projections in the axolotl: Evidence for timing as a specific mechanism of afferent fiber sorting

Cited by 29 publications

References 36 publications

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

Activity-independent specification of synaptic targets in the posterior lateral line of the larval zebrafish

Connecting Ears to Eye Muscles: Evolution of a ‘Simple' Reflex Arc

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