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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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WT (A) and otd-/- (B) ALv1 lineage. Note the position of the cell body (yellow dotted lines), the lateral point of entry of axon tract into the antennal lobe (indicated by the asterisk), the use of the mediolateral antennal lobe tract (indicated by the arrow) and the predominant innervation of the lateral horn of both the WT (A) and the otd-/- ALv1 lineage (B). Midline is represented by the yellow line. Genotype in A: FRT19A/FRT19A,Tub-Gal80,hsFLP; GH146-Gal4,UAS-mCD8::GFP/+. Genotype in B: FRT19A, oc2/FRT19A,Tub-Gal80,hsFLP; GH146-Gal4,UAS-mCD8::GFP/+.
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fig13: WT (A) and otd-/- (B) ALv1 lineage. Note the position of the cell body (yellow dotted lines), the lateral point of entry of axon tract into the antennal lobe (indicated by the asterisk), the use of the mediolateral antennal lobe tract (indicated by the arrow) and the predominant innervation of the lateral horn of both the WT (A) and the otd-/- ALv1 lineage (B). Midline is represented by the yellow line. Genotype in A: FRT19A/FRT19A,Tub-Gal80,hsFLP; GH146-Gal4,UAS-mCD8::GFP/+. Genotype in B: FRT19A, oc2/FRT19A,Tub-Gal80,hsFLP; GH146-Gal4,UAS-mCD8::GFP/+.

Mentions: We thank the reviewers for pointing out this potential complication. The GH146 driver labels only about 6-10 cells of the ALv1 lineage. These neurons are indeed antennal lobe projection interneurons, however, their neuroanatomy is very different from the otd-/- LALv1 lineage. The entry point of the axons of these two lineages into the antennal lobe is diametrically opposite to each other; while the otd-/- LALv1 lineage enters the lobe medially, ALv1 (as well as the otd-/- ALv1) enters it laterally (see asterisks in Author response image 1A,B). Most strikingly, their axons exit the lobe towards the protocerebrum using different tracts; while the otd-/- LALv1 lineage uses the medial antennal lobe tract, the ALv1 (as well as the otd-/- ALv1) use the mediolateral antennal lobe tract (see arrow in Author response 1A,B). Both these tracts are visible in Figure 5 A-C. Finally, while the otd-/- LALv1 lineage first innervates the calyx of the mushroom body and then the lateral horn, the GH146-labelled neurons of ALv1 (as well as the otd-/- ALv1) largely innervate only the lateral horn (see Author response image 1A,B). We have brought out these points in the main text as well. Please see paragraph 3 under the subheading, ‘Determining the lineage identity of the transformed neurons’ (also see Author response image 1).


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)

WT (A) and otd-/- (B) ALv1 lineage. Note the position of the cell body (yellow dotted lines), the lateral point of entry of axon tract into the antennal lobe (indicated by the asterisk), the use of the mediolateral antennal lobe tract (indicated by the arrow) and the predominant innervation of the lateral horn of both the WT (A) and the otd-/- ALv1 lineage (B). Midline is represented by the yellow line. Genotype in A: FRT19A/FRT19A,Tub-Gal80,hsFLP; GH146-Gal4,UAS-mCD8::GFP/+. Genotype in B: FRT19A, oc2/FRT19A,Tub-Gal80,hsFLP; GH146-Gal4,UAS-mCD8::GFP/+.
© Copyright Policy
Related In: Results  -  Collection

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

fig13: WT (A) and otd-/- (B) ALv1 lineage. Note the position of the cell body (yellow dotted lines), the lateral point of entry of axon tract into the antennal lobe (indicated by the asterisk), the use of the mediolateral antennal lobe tract (indicated by the arrow) and the predominant innervation of the lateral horn of both the WT (A) and the otd-/- ALv1 lineage (B). Midline is represented by the yellow line. Genotype in A: FRT19A/FRT19A,Tub-Gal80,hsFLP; GH146-Gal4,UAS-mCD8::GFP/+. Genotype in B: FRT19A, oc2/FRT19A,Tub-Gal80,hsFLP; GH146-Gal4,UAS-mCD8::GFP/+.
Mentions: We thank the reviewers for pointing out this potential complication. The GH146 driver labels only about 6-10 cells of the ALv1 lineage. These neurons are indeed antennal lobe projection interneurons, however, their neuroanatomy is very different from the otd-/- LALv1 lineage. The entry point of the axons of these two lineages into the antennal lobe is diametrically opposite to each other; while the otd-/- LALv1 lineage enters the lobe medially, ALv1 (as well as the otd-/- ALv1) enters it laterally (see asterisks in Author response image 1A,B). Most strikingly, their axons exit the lobe towards the protocerebrum using different tracts; while the otd-/- LALv1 lineage uses the medial antennal lobe tract, the ALv1 (as well as the otd-/- ALv1) use the mediolateral antennal lobe tract (see arrow in Author response 1A,B). Both these tracts are visible in Figure 5 A-C. Finally, while the otd-/- LALv1 lineage first innervates the calyx of the mushroom body and then the lateral horn, the GH146-labelled neurons of ALv1 (as well as the otd-/- ALv1) largely innervate only the lateral horn (see Author response image 1A,B). We have brought out these points in the main text as well. Please see paragraph 3 under the subheading, ‘Determining the lineage identity of the transformed neurons’ (also see Author response image 1).

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