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Genetic transformation of structural and functional circuitry rewires the Drosophila brain.

Sen S, Cao D, Choudhary R, Biagini S, Wang JW, Reichert H, VijayRaghavan K - Elife (2014)

Bottom Line: However, the extent to which individual factors can contribute to this is poorly understood.Loss of orthodenticle from this neuroblast affects molecular properties, neuroanatomical features, and functional inputs of progeny neurons, such that an entire central complex lineage transforms into a functional olfactory projection neuron lineage.This ability to change functional macrocircuitry of the brain through changes in gene expression in a single neuroblast reveals a surprising capacity for novel circuit formation in the brain and provides a paradigm for large-scale evolutionary modification of circuitry.

View Article: PubMed Central - PubMed

Affiliation: Department of Developmental Biology and Genetics, National Centre for Biological Sciences, Tata Institute for Fundamental Research, Bangalore, India.

ABSTRACT
Acquisition of distinct neuronal identities during development is critical for the assembly of diverse functional neural circuits in the brain. In both vertebrates and invertebrates, intrinsic determinants are thought to act in neural progenitors to specify their identity and the identity of their neuronal progeny. However, the extent to which individual factors can contribute to this is poorly understood. We investigate the role of orthodenticle in the specification of an identified neuroblast (neuronal progenitor) lineage in the Drosophila brain. Loss of orthodenticle from this neuroblast affects molecular properties, neuroanatomical features, and functional inputs of progeny neurons, such that an entire central complex lineage transforms into a functional olfactory projection neuron lineage. This ability to change functional macrocircuitry of the brain through changes in gene expression in a single neuroblast reveals a surprising capacity for novel circuit formation in the brain and provides a paradigm for large-scale evolutionary modification of circuitry.

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Expressing full-length otd in the otd−/− LALv1 lineage rescues the transformation phenotype.(A–D) is a MARCM labelled otd−/− LALv1 lineage that also expresses UAS-otd. The cell bodies of the otd−/− LALv1 lineage shown in A (magenta dotted lines) express the transgenic UAS-otd, shown in B (magenta dotted lines). The neuroanatomy of this rescued lineage resembles that of the WT LALv1 lineage, which skirts around the antennal lobe (yellow dotted lines) and innervates the lateral accessory lobe (white arrowheads). Genotype: FRT19A,otdYH13or oc2/FRT19A,Tub-Gal80,hsFLP; Tub-Gal4,UAS-mCD8::GFP/UAS-otd).DOI:http://dx.doi.org/10.7554/eLife.04407.009
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fig4s2: Expressing full-length otd in the otd−/− LALv1 lineage rescues the transformation phenotype.(A–D) is a MARCM labelled otd−/− LALv1 lineage that also expresses UAS-otd. The cell bodies of the otd−/− LALv1 lineage shown in A (magenta dotted lines) express the transgenic UAS-otd, shown in B (magenta dotted lines). The neuroanatomy of this rescued lineage resembles that of the WT LALv1 lineage, which skirts around the antennal lobe (yellow dotted lines) and innervates the lateral accessory lobe (white arrowheads). Genotype: FRT19A,otdYH13or oc2/FRT19A,Tub-Gal80,hsFLP; Tub-Gal4,UAS-mCD8::GFP/UAS-otd).DOI:http://dx.doi.org/10.7554/eLife.04407.009

Mentions: In order to investigate the neuroanatomy of the otd−/− LALv1 lineage further, we utilized the ubiquitously expressed Tub-Gal4 driver to label neuroblast clones and recovered 19 WT and 37 otd−/− neuroblast MARCM clones in the LALv1 lineage. While the wild-type neurons displayed all the features of the LALv1 lineage described above (Figure 4—figure supplement 1A), the otd−/− LALv1 neuroblast clones had dramatic changes in its neuroanatomy (Figure 4—figure supplement 1B–D). Mutant neurons no longer innervated the central complex or lateral accessory lobe neuropiles; instead they innervated the antennal lobe neuropile (asterisk in Figure 4—figure supplement 1B–D) and sent projections via the medial antennal lobe tract towards the protocerebrum (arrowhead in Figure 4—figure supplement 1B–D). These changes in dendritic and axonal innervation patterns were reversed by targeted expression of the full-length otd coding sequence in mutant neuroblast clones using the Tub-Gal4 (Figure 4—figure supplement 2).


Genetic transformation of structural and functional circuitry rewires the Drosophila brain.

Sen S, Cao D, Choudhary R, Biagini S, Wang JW, Reichert H, VijayRaghavan K - Elife (2014)

Expressing full-length otd in the otd−/− LALv1 lineage rescues the transformation phenotype.(A–D) is a MARCM labelled otd−/− LALv1 lineage that also expresses UAS-otd. The cell bodies of the otd−/− LALv1 lineage shown in A (magenta dotted lines) express the transgenic UAS-otd, shown in B (magenta dotted lines). The neuroanatomy of this rescued lineage resembles that of the WT LALv1 lineage, which skirts around the antennal lobe (yellow dotted lines) and innervates the lateral accessory lobe (white arrowheads). Genotype: FRT19A,otdYH13or oc2/FRT19A,Tub-Gal80,hsFLP; Tub-Gal4,UAS-mCD8::GFP/UAS-otd).DOI:http://dx.doi.org/10.7554/eLife.04407.009
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4307181&req=5

fig4s2: Expressing full-length otd in the otd−/− LALv1 lineage rescues the transformation phenotype.(A–D) is a MARCM labelled otd−/− LALv1 lineage that also expresses UAS-otd. The cell bodies of the otd−/− LALv1 lineage shown in A (magenta dotted lines) express the transgenic UAS-otd, shown in B (magenta dotted lines). The neuroanatomy of this rescued lineage resembles that of the WT LALv1 lineage, which skirts around the antennal lobe (yellow dotted lines) and innervates the lateral accessory lobe (white arrowheads). Genotype: FRT19A,otdYH13or oc2/FRT19A,Tub-Gal80,hsFLP; Tub-Gal4,UAS-mCD8::GFP/UAS-otd).DOI:http://dx.doi.org/10.7554/eLife.04407.009
Mentions: In order to investigate the neuroanatomy of the otd−/− LALv1 lineage further, we utilized the ubiquitously expressed Tub-Gal4 driver to label neuroblast clones and recovered 19 WT and 37 otd−/− neuroblast MARCM clones in the LALv1 lineage. While the wild-type neurons displayed all the features of the LALv1 lineage described above (Figure 4—figure supplement 1A), the otd−/− LALv1 neuroblast clones had dramatic changes in its neuroanatomy (Figure 4—figure supplement 1B–D). Mutant neurons no longer innervated the central complex or lateral accessory lobe neuropiles; instead they innervated the antennal lobe neuropile (asterisk in Figure 4—figure supplement 1B–D) and sent projections via the medial antennal lobe tract towards the protocerebrum (arrowhead in Figure 4—figure supplement 1B–D). These changes in dendritic and axonal innervation patterns were reversed by targeted expression of the full-length otd coding sequence in mutant neuroblast clones using the Tub-Gal4 (Figure 4—figure supplement 2).

Bottom Line: However, the extent to which individual factors can contribute to this is poorly understood.Loss of orthodenticle from this neuroblast affects molecular properties, neuroanatomical features, and functional inputs of progeny neurons, such that an entire central complex lineage transforms into a functional olfactory projection neuron lineage.This ability to change functional macrocircuitry of the brain through changes in gene expression in a single neuroblast reveals a surprising capacity for novel circuit formation in the brain and provides a paradigm for large-scale evolutionary modification of circuitry.

View Article: PubMed Central - PubMed

Affiliation: Department of Developmental Biology and Genetics, National Centre for Biological Sciences, Tata Institute for Fundamental Research, Bangalore, India.

ABSTRACT
Acquisition of distinct neuronal identities during development is critical for the assembly of diverse functional neural circuits in the brain. In both vertebrates and invertebrates, intrinsic determinants are thought to act in neural progenitors to specify their identity and the identity of their neuronal progeny. However, the extent to which individual factors can contribute to this is poorly understood. We investigate the role of orthodenticle in the specification of an identified neuroblast (neuronal progenitor) lineage in the Drosophila brain. Loss of orthodenticle from this neuroblast affects molecular properties, neuroanatomical features, and functional inputs of progeny neurons, such that an entire central complex lineage transforms into a functional olfactory projection neuron lineage. This ability to change functional macrocircuitry of the brain through changes in gene expression in a single neuroblast reveals a surprising capacity for novel circuit formation in the brain and provides a paradigm for large-scale evolutionary modification of circuitry.

Show MeSH
Related in: MedlinePlus