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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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Overexpression of Otd in the ALad1 lineage results in a partial reciprocal transformation.(A–C) ALad1 neuroblast clone misexpressing Otd. (B and C) are the anterior and lateral views of the 3D reconstructions of the clone in A. Few of the Otd misexpressing cells (yellow asterisk in A) retain the wild type neuroanatomy of the ALad1 lineage (magenta cells in the reconstructions)—they have innervations in the AL glomeruli (yellow arrowheads in A–C) and project via the antennal-cerebral tract (yellow arrowhead in C). Most of the Otd misexpressing ALad1 neurons are seen ventral to the AL (magenta asterisk in A; green cells in the reconstructions in B and C). They do not innervate the AL and instead project towards the LAL (white arrowheads in A–C). Genotype in A–C: FRT19A/FRT19A,Tub-Gal80,hsFLP; Tub-Gal4,UAS-mCD8::GFP/UAS-otd. Midline is represented by a yellow line. Scale bar is 50 µm.DOI:http://dx.doi.org/10.7554/eLife.04407.016
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fig8: Overexpression of Otd in the ALad1 lineage results in a partial reciprocal transformation.(A–C) ALad1 neuroblast clone misexpressing Otd. (B and C) are the anterior and lateral views of the 3D reconstructions of the clone in A. Few of the Otd misexpressing cells (yellow asterisk in A) retain the wild type neuroanatomy of the ALad1 lineage (magenta cells in the reconstructions)—they have innervations in the AL glomeruli (yellow arrowheads in A–C) and project via the antennal-cerebral tract (yellow arrowhead in C). Most of the Otd misexpressing ALad1 neurons are seen ventral to the AL (magenta asterisk in A; green cells in the reconstructions in B and C). They do not innervate the AL and instead project towards the LAL (white arrowheads in A–C). Genotype in A–C: FRT19A/FRT19A,Tub-Gal80,hsFLP; Tub-Gal4,UAS-mCD8::GFP/UAS-otd. Midline is represented by a yellow line. Scale bar is 50 µm.DOI:http://dx.doi.org/10.7554/eLife.04407.016

Mentions: We next asked whether otd gain-of-function in the antennal lobe lineage, ALad1, might result in a reciprocal anatomical transformation of this lineage into one resembling the wild-type central complex lineage, LALv1. We used the MARCM system to misexpress the full-length otd coding sequence in the antennal lobe neuroblast clones using a Tub-Gal4 driver. In all Otd misexpression clones of the antennal lobe lineage (15/15), we found a partial transformation of this lineage towards the central complex identity (Figure 8). All 15 clones comprised a few cells that retained neuroanatomical features of the wild-type antennal lobe lineage such as antero-dorsal cell body position, innervation of the antennal lobe, and axonal projections via the medial antennal lobe tract (yellow asterisk and arrowhead in Figure 8A–C). However, most of the cells in the clones displayed neuroanatomical features of the central complex lineage. These cell bodies were positioned ventral to the adult antennal lobe, they projected their axons via the loVM and LEp tracts and they innervated the lateral accessory lobe (magenta asterisk and white arrowheads in Figure 8A–C). Thus, otd gain-of-function was able to cause a partial, albeit incomplete transformation, of the antennal lobe lineage into a central complex-like lineage.10.7554/eLife.04407.016Figure 8.Overexpression of Otd in the ALad1 lineage results in a partial reciprocal transformation.


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)

Overexpression of Otd in the ALad1 lineage results in a partial reciprocal transformation.(A–C) ALad1 neuroblast clone misexpressing Otd. (B and C) are the anterior and lateral views of the 3D reconstructions of the clone in A. Few of the Otd misexpressing cells (yellow asterisk in A) retain the wild type neuroanatomy of the ALad1 lineage (magenta cells in the reconstructions)—they have innervations in the AL glomeruli (yellow arrowheads in A–C) and project via the antennal-cerebral tract (yellow arrowhead in C). Most of the Otd misexpressing ALad1 neurons are seen ventral to the AL (magenta asterisk in A; green cells in the reconstructions in B and C). They do not innervate the AL and instead project towards the LAL (white arrowheads in A–C). Genotype in A–C: FRT19A/FRT19A,Tub-Gal80,hsFLP; Tub-Gal4,UAS-mCD8::GFP/UAS-otd. Midline is represented by a yellow line. Scale bar is 50 µm.DOI:http://dx.doi.org/10.7554/eLife.04407.016
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4307181&req=5

fig8: Overexpression of Otd in the ALad1 lineage results in a partial reciprocal transformation.(A–C) ALad1 neuroblast clone misexpressing Otd. (B and C) are the anterior and lateral views of the 3D reconstructions of the clone in A. Few of the Otd misexpressing cells (yellow asterisk in A) retain the wild type neuroanatomy of the ALad1 lineage (magenta cells in the reconstructions)—they have innervations in the AL glomeruli (yellow arrowheads in A–C) and project via the antennal-cerebral tract (yellow arrowhead in C). Most of the Otd misexpressing ALad1 neurons are seen ventral to the AL (magenta asterisk in A; green cells in the reconstructions in B and C). They do not innervate the AL and instead project towards the LAL (white arrowheads in A–C). Genotype in A–C: FRT19A/FRT19A,Tub-Gal80,hsFLP; Tub-Gal4,UAS-mCD8::GFP/UAS-otd. Midline is represented by a yellow line. Scale bar is 50 µm.DOI:http://dx.doi.org/10.7554/eLife.04407.016
Mentions: We next asked whether otd gain-of-function in the antennal lobe lineage, ALad1, might result in a reciprocal anatomical transformation of this lineage into one resembling the wild-type central complex lineage, LALv1. We used the MARCM system to misexpress the full-length otd coding sequence in the antennal lobe neuroblast clones using a Tub-Gal4 driver. In all Otd misexpression clones of the antennal lobe lineage (15/15), we found a partial transformation of this lineage towards the central complex identity (Figure 8). All 15 clones comprised a few cells that retained neuroanatomical features of the wild-type antennal lobe lineage such as antero-dorsal cell body position, innervation of the antennal lobe, and axonal projections via the medial antennal lobe tract (yellow asterisk and arrowhead in Figure 8A–C). However, most of the cells in the clones displayed neuroanatomical features of the central complex lineage. These cell bodies were positioned ventral to the adult antennal lobe, they projected their axons via the loVM and LEp tracts and they innervated the lateral accessory lobe (magenta asterisk and white arrowheads in Figure 8A–C). Thus, otd gain-of-function was able to cause a partial, albeit incomplete transformation, of the antennal lobe lineage into a central complex-like lineage.10.7554/eLife.04407.016Figure 8.Overexpression of Otd in the ALad1 lineage results in a partial reciprocal transformation.

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