4.7 Article

Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

Journal

JOURNAL OF NEUROSCIENCE
Volume 32, Issue 9, Pages 2976-2987

Publisher

SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.5157-11.2012

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Funding

  1. Agencia de Gestio d'Ajuts Universitaris i de Recerca (AGAUR) [2009-SGR-305]
  2. European Research Council [ERC-2007-StG SENSORINEURAL]
  3. Fondation pour la Recherche Medicale of France
  4. Intra-European Marie Curie Fellowship
  5. AGAUR
  6. National BioResource Project
  7. Ministry of Education, Culture, Sports, Science and Technology of Japan
  8. Grants-in-Aid for Scientific Research [22700349] Funding Source: KAKEN

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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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