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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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Loss of otd from the LALv1 neuroblast lineage, transforms it into an antennal lobe PN lineage.(A and B) are Tubulin-Gal4 labelled adult, wild-type clones of the LALv1 lineage. (A) shows the anterior sections and (B) shows more posterior sections of the same clone. (A) The cell bodies of LALv1 lie ventral to the antennal lobe (AL) and express the transcription factor otd (inset in A). The axon tract of this lineage skirts around the AL (magenta arrows in A and B) and innervates the lateral accessory lobe (LAL, magenta dotted lines in A) and the central complex (CC, magenta dotted lines in B). Note that there are no innervation from this lineage in the AL. (C and D) are tubulin labelled adult, otd  clones of the LALv1 NB lineage. (C) shows the anterior sections, and (D) shows more posterior sections of the same clone. The otd−/− LALv1 lineage innervates the AL (magenta dotted lines in C and D) and sends its axon tracts towards the protocerebrum (magenta arrows in D).DOI:http://dx.doi.org/10.7554/eLife.04407.008
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fig4s1: Loss of otd from the LALv1 neuroblast lineage, transforms it into an antennal lobe PN lineage.(A and B) are Tubulin-Gal4 labelled adult, wild-type clones of the LALv1 lineage. (A) shows the anterior sections and (B) shows more posterior sections of the same clone. (A) The cell bodies of LALv1 lie ventral to the antennal lobe (AL) and express the transcription factor otd (inset in A). The axon tract of this lineage skirts around the AL (magenta arrows in A and B) and innervates the lateral accessory lobe (LAL, magenta dotted lines in A) and the central complex (CC, magenta dotted lines in B). Note that there are no innervation from this lineage in the AL. (C and D) are tubulin labelled adult, otd clones of the LALv1 NB lineage. (C) shows the anterior sections, and (D) shows more posterior sections of the same clone. The otd−/− LALv1 lineage innervates the AL (magenta dotted lines in C and D) and sends its axon tracts towards the protocerebrum (magenta arrows in D).DOI:http://dx.doi.org/10.7554/eLife.04407.008

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)

Loss of otd from the LALv1 neuroblast lineage, transforms it into an antennal lobe PN lineage.(A and B) are Tubulin-Gal4 labelled adult, wild-type clones of the LALv1 lineage. (A) shows the anterior sections and (B) shows more posterior sections of the same clone. (A) The cell bodies of LALv1 lie ventral to the antennal lobe (AL) and express the transcription factor otd (inset in A). The axon tract of this lineage skirts around the AL (magenta arrows in A and B) and innervates the lateral accessory lobe (LAL, magenta dotted lines in A) and the central complex (CC, magenta dotted lines in B). Note that there are no innervation from this lineage in the AL. (C and D) are tubulin labelled adult, otd  clones of the LALv1 NB lineage. (C) shows the anterior sections, and (D) shows more posterior sections of the same clone. The otd−/− LALv1 lineage innervates the AL (magenta dotted lines in C and D) and sends its axon tracts towards the protocerebrum (magenta arrows in D).DOI:http://dx.doi.org/10.7554/eLife.04407.008
© Copyright Policy
Related In: Results  -  Collection

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

fig4s1: Loss of otd from the LALv1 neuroblast lineage, transforms it into an antennal lobe PN lineage.(A and B) are Tubulin-Gal4 labelled adult, wild-type clones of the LALv1 lineage. (A) shows the anterior sections and (B) shows more posterior sections of the same clone. (A) The cell bodies of LALv1 lie ventral to the antennal lobe (AL) and express the transcription factor otd (inset in A). The axon tract of this lineage skirts around the AL (magenta arrows in A and B) and innervates the lateral accessory lobe (LAL, magenta dotted lines in A) and the central complex (CC, magenta dotted lines in B). Note that there are no innervation from this lineage in the AL. (C and D) are tubulin labelled adult, otd clones of the LALv1 NB lineage. (C) shows the anterior sections, and (D) shows more posterior sections of the same clone. The otd−/− LALv1 lineage innervates the AL (magenta dotted lines in C and D) and sends its axon tracts towards the protocerebrum (magenta arrows in D).DOI:http://dx.doi.org/10.7554/eLife.04407.008
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