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Molecular mechanisms of tiling and self-avoidance in neural development.

Cameron S, Rao Y - Mol Brain (2010)

Bottom Line: Dscams and Turtle (Tutl), two Ig superfamily proteins, have been shown to mediate contact-dependent homotypic interactions in tiling and self-avoidance.By contrast, the Activin pathway regulates axonal tiling in a contact-independent manner.These cell surface signals may directly or indirectly regulate the activity of the Tricornered kinase pathway and/or other intracellular signaling pathways to prevent the overlap between same-type neuronal arbors in the sensory or synaptic input field.

View Article: PubMed Central - HTML - PubMed

Affiliation: McGill Centre for Research in Neuroscience, McGill University Health Centre, 1650 Cedar Avenue, Montreal, Quebec H3G 1A4, Canada.

ABSTRACT
Recent studies have begun to unravel the molecular basis of tiling and self-avoidance, two important cellular mechanisms that shape neuronal circuitry during development in both invertebrates and vertebrates. Dscams and Turtle (Tutl), two Ig superfamily proteins, have been shown to mediate contact-dependent homotypic interactions in tiling and self-avoidance. By contrast, the Activin pathway regulates axonal tiling in a contact-independent manner. These cell surface signals may directly or indirectly regulate the activity of the Tricornered kinase pathway and/or other intracellular signaling pathways to prevent the overlap between same-type neuronal arbors in the sensory or synaptic input field.

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Examples of tiling and self-avoidance in vertebrates and invertebrates. A, A simplified diagram showing the tiling of vertebrate retinal ganglion neurons, based on results in [4]. B, Axonal tiling contributes to the organized columnar projection pattern of R7 and R8 photoreceptor neurons and L1 lamina neurons in the medulla of the Drosophila visual system. While L1 neurons arborize at both M1 and M5 sub-layers, R7 and R8 axons terminate at M6 and M3 sub-layers, respectively. Genetic dissection of neuronal circuit formation in the fly visual system has contributed significantly to our understanding of neuronal positioning, axon guidance and neuronal target selection (e.g. [53-57]). C, A schematic diagram showing the non-overlapping coverage of the receptive field by sister branches from a Pv mechanosensory neuron in leech, based on results in [14]. D, A simplified diagram showing self-avoidance in a Drosophila class IV da neuron, where sister branches tend to avoid each other.
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Figure 1: Examples of tiling and self-avoidance in vertebrates and invertebrates. A, A simplified diagram showing the tiling of vertebrate retinal ganglion neurons, based on results in [4]. B, Axonal tiling contributes to the organized columnar projection pattern of R7 and R8 photoreceptor neurons and L1 lamina neurons in the medulla of the Drosophila visual system. While L1 neurons arborize at both M1 and M5 sub-layers, R7 and R8 axons terminate at M6 and M3 sub-layers, respectively. Genetic dissection of neuronal circuit formation in the fly visual system has contributed significantly to our understanding of neuronal positioning, axon guidance and neuronal target selection (e.g. [53-57]). C, A schematic diagram showing the non-overlapping coverage of the receptive field by sister branches from a Pv mechanosensory neuron in leech, based on results in [14]. D, A simplified diagram showing self-avoidance in a Drosophila class IV da neuron, where sister branches tend to avoid each other.

Mentions: Tiling involves the recognition between certain same-type or functionally equivalent neurons, which allows the neurites from same-type neurons to completely cover the sensory or synaptic input field with no or minimal overlap. Tiling is likely required for providing an anatomical basis for parallel detection of same-type sensory information in the receptive field and thus allows the spatial discrimination of sensory information. The phenomenon of tiling was first discovered in the cat retina by Boycott and colleagues in 1981 [4] (Fig. 1A). Their work demonstrates that certain same-type retinal ganglion neurons (i.e. ON-brisk-transient cells and OFF-brisk-transient cells) are organized in a mosaic pattern in the retina, and so the receptive field is covered completely but non-redundantly with each subtype of α-ganglion neurons. Later studies showed that many of ~50 types of mammalian retinal neurons displayed some degree of tiling pattern, which appears to be essential for unambiguously processing visual information from the external world [5]. Tiling has also been observed in the Drosophila visual system [6] (Fig. 1B), and many other neuronal systems in both vertebrates and invertebrates [4,7-13].


Molecular mechanisms of tiling and self-avoidance in neural development.

Cameron S, Rao Y - Mol Brain (2010)

Examples of tiling and self-avoidance in vertebrates and invertebrates. A, A simplified diagram showing the tiling of vertebrate retinal ganglion neurons, based on results in [4]. B, Axonal tiling contributes to the organized columnar projection pattern of R7 and R8 photoreceptor neurons and L1 lamina neurons in the medulla of the Drosophila visual system. While L1 neurons arborize at both M1 and M5 sub-layers, R7 and R8 axons terminate at M6 and M3 sub-layers, respectively. Genetic dissection of neuronal circuit formation in the fly visual system has contributed significantly to our understanding of neuronal positioning, axon guidance and neuronal target selection (e.g. [53-57]). C, A schematic diagram showing the non-overlapping coverage of the receptive field by sister branches from a Pv mechanosensory neuron in leech, based on results in [14]. D, A simplified diagram showing self-avoidance in a Drosophila class IV da neuron, where sister branches tend to avoid each other.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2959082&req=5

Figure 1: Examples of tiling and self-avoidance in vertebrates and invertebrates. A, A simplified diagram showing the tiling of vertebrate retinal ganglion neurons, based on results in [4]. B, Axonal tiling contributes to the organized columnar projection pattern of R7 and R8 photoreceptor neurons and L1 lamina neurons in the medulla of the Drosophila visual system. While L1 neurons arborize at both M1 and M5 sub-layers, R7 and R8 axons terminate at M6 and M3 sub-layers, respectively. Genetic dissection of neuronal circuit formation in the fly visual system has contributed significantly to our understanding of neuronal positioning, axon guidance and neuronal target selection (e.g. [53-57]). C, A schematic diagram showing the non-overlapping coverage of the receptive field by sister branches from a Pv mechanosensory neuron in leech, based on results in [14]. D, A simplified diagram showing self-avoidance in a Drosophila class IV da neuron, where sister branches tend to avoid each other.
Mentions: Tiling involves the recognition between certain same-type or functionally equivalent neurons, which allows the neurites from same-type neurons to completely cover the sensory or synaptic input field with no or minimal overlap. Tiling is likely required for providing an anatomical basis for parallel detection of same-type sensory information in the receptive field and thus allows the spatial discrimination of sensory information. The phenomenon of tiling was first discovered in the cat retina by Boycott and colleagues in 1981 [4] (Fig. 1A). Their work demonstrates that certain same-type retinal ganglion neurons (i.e. ON-brisk-transient cells and OFF-brisk-transient cells) are organized in a mosaic pattern in the retina, and so the receptive field is covered completely but non-redundantly with each subtype of α-ganglion neurons. Later studies showed that many of ~50 types of mammalian retinal neurons displayed some degree of tiling pattern, which appears to be essential for unambiguously processing visual information from the external world [5]. Tiling has also been observed in the Drosophila visual system [6] (Fig. 1B), and many other neuronal systems in both vertebrates and invertebrates [4,7-13].

Bottom Line: Dscams and Turtle (Tutl), two Ig superfamily proteins, have been shown to mediate contact-dependent homotypic interactions in tiling and self-avoidance.By contrast, the Activin pathway regulates axonal tiling in a contact-independent manner.These cell surface signals may directly or indirectly regulate the activity of the Tricornered kinase pathway and/or other intracellular signaling pathways to prevent the overlap between same-type neuronal arbors in the sensory or synaptic input field.

View Article: PubMed Central - HTML - PubMed

Affiliation: McGill Centre for Research in Neuroscience, McGill University Health Centre, 1650 Cedar Avenue, Montreal, Quebec H3G 1A4, Canada.

ABSTRACT
Recent studies have begun to unravel the molecular basis of tiling and self-avoidance, two important cellular mechanisms that shape neuronal circuitry during development in both invertebrates and vertebrates. Dscams and Turtle (Tutl), two Ig superfamily proteins, have been shown to mediate contact-dependent homotypic interactions in tiling and self-avoidance. By contrast, the Activin pathway regulates axonal tiling in a contact-independent manner. These cell surface signals may directly or indirectly regulate the activity of the Tricornered kinase pathway and/or other intracellular signaling pathways to prevent the overlap between same-type neuronal arbors in the sensory or synaptic input field.

Show MeSH
Related in: MedlinePlus