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      Primary sensory map formations reflect unique needs and molecular cues specific to each sensory system

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          Abstract

          Interaction with the world around us requires extracting meaningful signals to guide behavior. Each of the six mammalian senses (olfaction, vision, somatosensation, hearing, balance, and taste) has a unique primary map that extracts sense-specific information. Sensory systems in the periphery and their target neurons in the central nervous system develop independently and must develop specific connections for proper sensory processing. In addition, the regulation of sensory map formation is independent of and prior to central target neuronal development in several maps. This review provides an overview of the current level of understanding of primary map formation of the six mammalian senses. Cell cycle exit, combined with incompletely understood molecules and their regulation, provides chemoaffinity-mediated primary maps that are further refined by activity. The interplay between cell cycle exit, molecular guidance, and activity-mediated refinement is the basis of dominance stripes after redundant organ transplantations in the visual and balance system. A more advanced level of understanding of primary map formation could benefit ongoing restoration attempts of impaired senses by guiding proper functional connection formations of restored sensory organs with their central nervous system targets.

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          Most cited references172

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          A place theory of sound localization.

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            Neuropilin-1 Conveys Semaphorin and VEGF Signaling during Neural and Cardiovascular Development

            Neuropilin-1 (Npn-1) is a receptor that binds multiple ligands from structurally distinct families, including secreted semaphorins (Sema) and vascular endothelial growth factors (VEGF). We generated npn-1 knockin mice, which express an altered ligand binding site variant of Npn-1, and npn-1 conditional null mice to establish the cell-type- and ligand specificity of Npn-1 function in the developing cardiovascular and nervous systems. Our results show that VEGF-Npn-1 signaling in endothelial cells is required for angiogenesis. In striking contrast, Sema-Npn-1 signaling is not essential for general vascular development but is required for axonal pathfinding by several populations of neurons in the CNS and PNS. Remarkably, both Sema-Npn-1 signaling and VEGF-Npn-1 signaling are critical for heart development. Therefore, Npn-1 is a multifunctional receptor that mediates the activities of structurally distinct ligands during development of the heart, vasculature, and nervous system.
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              Mechanisms underlying development of visual maps and receptive fields.

              Patterns of synaptic connections in the visual system are remarkably precise. These connections dictate the receptive field properties of individual visual neurons and ultimately determine the quality of visual perception. Spontaneous neural activity is necessary for the development of various receptive field properties and visual feature maps. In recent years, attention has shifted to understanding the mechanisms by which spontaneous activity in the developing retina, lateral geniculate nucleus, and visual cortex instruct the axonal and dendritic refinements that give rise to orderly connections in the visual system. Axon guidance cues and a growing list of other molecules, including immune system factors, have also recently been implicated in visual circuit wiring. A major goal now is to determine how these molecules cooperate with spontaneous and visually evoked activity to give rise to the circuits underlying precise receptive field tuning and orderly visual maps.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal AnalysisRole: Project AdministrationRole: ValidationRole: VisualizationRole: Writing – Original Draft Preparation
                Role: ResourcesRole: ValidationRole: VisualizationRole: Writing – Review & Editing
                Role: ConceptualizationRole: ValidationRole: Writing – Review & Editing
                Journal
                F1000Res
                F1000Res
                F1000Research
                F1000Research
                F1000 Research Limited (London, UK )
                2046-1402
                27 March 2019
                2019
                : 8
                : F1000 Faculty Rev-345
                Affiliations
                [1 ]Department of Biology, University of Iowa, Iowa City, USA
                [2 ]Institute of Biotechnology of the Czech Academy of Sciences, Vestec, Czech Republic
                Author notes

                No competing interests were disclosed.

                Author information
                https://orcid.org/0000-0002-4882-8398
                Article
                10.12688/f1000research.17717.1
                6439788
                30984379
                696d6fbb-993f-4bfc-85dd-f358efdce198
                Copyright: © 2019 Fritzsch B et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 21 March 2019
                Funding
                Funded by: Czech Acamady of Sciences
                Award ID: 86652036
                Funded by: Czech Science Fooundation
                Award ID: 17-04719S
                Funded by: NIH/NIDCD
                Award ID: R03DC015333
                Funded by: NIH/NIA
                Award ID: R01AG060504
                The authors were supported by the Czech Science Foundation (17-04719S to GP), the European Regional Development Fund (BIOCEVCZ.1.05/1.1.00/02.0109), the institutional support of the Czech Academy of Sciences (RVO: 86652036), and the National Institutes of Health (R01 AG060504 to BF and R03 DC015333 to KE).
                The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Review
                Articles

                primary sensory maps,retinotopic map,olfactory map,cochleotopic map,vestibular map,taste map

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