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The wiring diagram of a glomerular olfactory system.

Berck ME, Khandelwal A, Claus L, Hernandez-Nunez L, Si G, Tabone CJ, Li F, Truman JW, Fetter RD, Louis M, Samuel AD, Cardona A - Elife (2016)

Bottom Line: We found a canonical circuit with uniglomerular projection neurons (uPNs) relaying gain-controlled ORN activity to the mushroom body and the lateral horn.A second, parallel circuit with multiglomerular projection neurons (mPNs) and hierarchically connected local neurons (LNs) selectively integrates multiple ORN signals already at the first synapse.This complete wiring diagram will support experimental and theoretical studies towards bridging the gap between circuits and behavior.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, Harvard University, Cambridge, United States.

ABSTRACT
The sense of smell enables animals to react to long-distance cues according to learned and innate valences. Here, we have mapped with electron microscopy the complete wiring diagram of the Drosophila larval antennal lobe, an olfactory neuropil similar to the vertebrate olfactory bulb. We found a canonical circuit with uniglomerular projection neurons (uPNs) relaying gain-controlled ORN activity to the mushroom body and the lateral horn. A second, parallel circuit with multiglomerular projection neurons (mPNs) and hierarchically connected local neurons (LNs) selectively integrates multiple ORN signals already at the first synapse. LN-LN synaptic connections putatively implement a bistable gain control mechanism that either computes odor saliency through panglomerular inhibition, or allows some glomeruli to respond to faint aversive odors in the presence of strong appetitive odors. This complete wiring diagram will support experimental and theoretical studies towards bridging the gap between circuits and behavior.

No MeSH data available.


Related in: MedlinePlus

Neurotransmitters of Keystone LN and Picky LNs.Genetic driver lines specific for Keystone LN (GAL4 line GMR27F08) and Picky LNs (split-GAL4 lines JRC_SS04499, JRC_SS04500, JRC_SS04260) driving GFP expression specifically in these neurons were labeled with anti-GABA and anti-vGlut (A–U), and also anti-Chat (all negative; not shown). Keystone presents immunoreactivity to anti-GABA (textbf A–C), and at least 4 of the 5 Picky LNs are positive to anti-vGlut and negative to anti-GABA (D–U). These neurons derive from the BAla2 lineage (Das et al., 2013). JRC_SS04260 drives expression specifically and uniquely a Picky LN, likely Picky LN 4, which presents anti-vGLut immunoreactivity (P–R). Left unlettered panels show the homologous identified EM-reconstructed neurons, with Broad LNs in grey for reference. Asterisks mark the location of cell bodies when there is not labeling, such as in panels I, O and U. Broad LNs and Choosy LNs are GABAergic (see Thum et al., 2011 at Figure 2 D–G for Broad LNs and L–O for Choosy LNs).DOI:http://dx.doi.org/10.7554/eLife.14859.008
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fig2s1: Neurotransmitters of Keystone LN and Picky LNs.Genetic driver lines specific for Keystone LN (GAL4 line GMR27F08) and Picky LNs (split-GAL4 lines JRC_SS04499, JRC_SS04500, JRC_SS04260) driving GFP expression specifically in these neurons were labeled with anti-GABA and anti-vGlut (A–U), and also anti-Chat (all negative; not shown). Keystone presents immunoreactivity to anti-GABA (textbf A–C), and at least 4 of the 5 Picky LNs are positive to anti-vGlut and negative to anti-GABA (D–U). These neurons derive from the BAla2 lineage (Das et al., 2013). JRC_SS04260 drives expression specifically and uniquely a Picky LN, likely Picky LN 4, which presents anti-vGLut immunoreactivity (P–R). Left unlettered panels show the homologous identified EM-reconstructed neurons, with Broad LNs in grey for reference. Asterisks mark the location of cell bodies when there is not labeling, such as in panels I, O and U. Broad LNs and Choosy LNs are GABAergic (see Thum et al., 2011 at Figure 2 D–G for Broad LNs and L–O for Choosy LNs).DOI:http://dx.doi.org/10.7554/eLife.14859.008

Mentions: The 14 pairs of LNs originate in 5 different lineages (Figure 1—figure supplement 3). We assigned the same name to neurons of the same lineage, and numbered each when there is more than one per lineage. LNs connect to other neuron classes stereotypically in the two antennal lobes (Figure 2). We selected names reminiscent of either their circuit role or anatomical feature, including 'Broad' to refer to panglomerular arbors; 'Picky' and 'Choosy' for LNs of two different lineages (and different neurotransmitter; see below) with arbors innervating select subsets of glomeruli; 'Keystone' for a single pair that mediate interactions between LNs of different circuits; and 'Ventral LN' for a single pair of LNs with ventral cell bodies. We also determined the neurotransmitters of LNs that were previously unknown (Figure 2—figure supplement 1). We introduce the properties of each LN type below with the olfactory circuits that they participate in.10.7554/eLife.14859.007Figure 2.Percentage of synapses of LNs from/onto specific cell types.


The wiring diagram of a glomerular olfactory system.

Berck ME, Khandelwal A, Claus L, Hernandez-Nunez L, Si G, Tabone CJ, Li F, Truman JW, Fetter RD, Louis M, Samuel AD, Cardona A - Elife (2016)

Neurotransmitters of Keystone LN and Picky LNs.Genetic driver lines specific for Keystone LN (GAL4 line GMR27F08) and Picky LNs (split-GAL4 lines JRC_SS04499, JRC_SS04500, JRC_SS04260) driving GFP expression specifically in these neurons were labeled with anti-GABA and anti-vGlut (A–U), and also anti-Chat (all negative; not shown). Keystone presents immunoreactivity to anti-GABA (textbf A–C), and at least 4 of the 5 Picky LNs are positive to anti-vGlut and negative to anti-GABA (D–U). These neurons derive from the BAla2 lineage (Das et al., 2013). JRC_SS04260 drives expression specifically and uniquely a Picky LN, likely Picky LN 4, which presents anti-vGLut immunoreactivity (P–R). Left unlettered panels show the homologous identified EM-reconstructed neurons, with Broad LNs in grey for reference. Asterisks mark the location of cell bodies when there is not labeling, such as in panels I, O and U. Broad LNs and Choosy LNs are GABAergic (see Thum et al., 2011 at Figure 2 D–G for Broad LNs and L–O for Choosy LNs).DOI:http://dx.doi.org/10.7554/eLife.14859.008
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fig2s1: Neurotransmitters of Keystone LN and Picky LNs.Genetic driver lines specific for Keystone LN (GAL4 line GMR27F08) and Picky LNs (split-GAL4 lines JRC_SS04499, JRC_SS04500, JRC_SS04260) driving GFP expression specifically in these neurons were labeled with anti-GABA and anti-vGlut (A–U), and also anti-Chat (all negative; not shown). Keystone presents immunoreactivity to anti-GABA (textbf A–C), and at least 4 of the 5 Picky LNs are positive to anti-vGlut and negative to anti-GABA (D–U). These neurons derive from the BAla2 lineage (Das et al., 2013). JRC_SS04260 drives expression specifically and uniquely a Picky LN, likely Picky LN 4, which presents anti-vGLut immunoreactivity (P–R). Left unlettered panels show the homologous identified EM-reconstructed neurons, with Broad LNs in grey for reference. Asterisks mark the location of cell bodies when there is not labeling, such as in panels I, O and U. Broad LNs and Choosy LNs are GABAergic (see Thum et al., 2011 at Figure 2 D–G for Broad LNs and L–O for Choosy LNs).DOI:http://dx.doi.org/10.7554/eLife.14859.008
Mentions: The 14 pairs of LNs originate in 5 different lineages (Figure 1—figure supplement 3). We assigned the same name to neurons of the same lineage, and numbered each when there is more than one per lineage. LNs connect to other neuron classes stereotypically in the two antennal lobes (Figure 2). We selected names reminiscent of either their circuit role or anatomical feature, including 'Broad' to refer to panglomerular arbors; 'Picky' and 'Choosy' for LNs of two different lineages (and different neurotransmitter; see below) with arbors innervating select subsets of glomeruli; 'Keystone' for a single pair that mediate interactions between LNs of different circuits; and 'Ventral LN' for a single pair of LNs with ventral cell bodies. We also determined the neurotransmitters of LNs that were previously unknown (Figure 2—figure supplement 1). We introduce the properties of each LN type below with the olfactory circuits that they participate in.10.7554/eLife.14859.007Figure 2.Percentage of synapses of LNs from/onto specific cell types.

Bottom Line: We found a canonical circuit with uniglomerular projection neurons (uPNs) relaying gain-controlled ORN activity to the mushroom body and the lateral horn.A second, parallel circuit with multiglomerular projection neurons (mPNs) and hierarchically connected local neurons (LNs) selectively integrates multiple ORN signals already at the first synapse.This complete wiring diagram will support experimental and theoretical studies towards bridging the gap between circuits and behavior.

View Article: PubMed Central - PubMed

Affiliation: Department of Physics, Harvard University, Cambridge, United States.

ABSTRACT
The sense of smell enables animals to react to long-distance cues according to learned and innate valences. Here, we have mapped with electron microscopy the complete wiring diagram of the Drosophila larval antennal lobe, an olfactory neuropil similar to the vertebrate olfactory bulb. We found a canonical circuit with uniglomerular projection neurons (uPNs) relaying gain-controlled ORN activity to the mushroom body and the lateral horn. A second, parallel circuit with multiglomerular projection neurons (mPNs) and hierarchically connected local neurons (LNs) selectively integrates multiple ORN signals already at the first synapse. LN-LN synaptic connections putatively implement a bistable gain control mechanism that either computes odor saliency through panglomerular inhibition, or allows some glomeruli to respond to faint aversive odors in the presence of strong appetitive odors. This complete wiring diagram will support experimental and theoretical studies towards bridging the gap between circuits and behavior.

No MeSH data available.


Related in: MedlinePlus