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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

Six SEZ neurons receive specific inputs from some ORNs and from some antennal lobe LNs.Left, EM-reconstruction of the 6 SEZ neurons (vine, cypress, clamp, spruce and ginkgo 1 and 2), with their axons labeled green and their dendrites blue. Presynaptic sites in red and postsynaptic sites in cyan. Middle, 3 of these SEZ neurons project to the same unidentified region of the SEZ. Spruce projects to a more posterior area. Lateral view, anterior to the left. Right, table of percent of postsynaptic sites of a column neuron contributed by a row neuron, illustrating how some ORNs and LNs specifically target these SEZ neurons. We show only connections with at least two synapses, consistently found among homologous identified neurons in both the left and right antennal lobes. Percentages between 0 and 0.5 are removed. Notice how Picky LNs 2, 3 and 4 synapse strongly onto SEZ neurons.DOI:http://dx.doi.org/10.7554/eLife.14859.013
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fig4s1: Six SEZ neurons receive specific inputs from some ORNs and from some antennal lobe LNs.Left, EM-reconstruction of the 6 SEZ neurons (vine, cypress, clamp, spruce and ginkgo 1 and 2), with their axons labeled green and their dendrites blue. Presynaptic sites in red and postsynaptic sites in cyan. Middle, 3 of these SEZ neurons project to the same unidentified region of the SEZ. Spruce projects to a more posterior area. Lateral view, anterior to the left. Right, table of percent of postsynaptic sites of a column neuron contributed by a row neuron, illustrating how some ORNs and LNs specifically target these SEZ neurons. We show only connections with at least two synapses, consistently found among homologous identified neurons in both the left and right antennal lobes. Percentages between 0 and 0.5 are removed. Notice how Picky LNs 2, 3 and 4 synapse strongly onto SEZ neurons.DOI:http://dx.doi.org/10.7554/eLife.14859.013

Mentions: Parallel to the uniglomerular readout by the 21 uPNs, we found 14 multiglomerular PNs (mPNs; Figure 4a). Each mPN receives unique and stereotyped inputs from multiple ORNs (Figure 4c) or at least from one ORN and multiple unidentified non-ORN sensory neurons in the SEZ (Figure 4a). The mPNs originate in multiple neuronal lineages and project to multiple brain regions; most commonly the lateral horn (LH) but also regions surrounding the MB calyx. Of the 14 mPNs, three project to the calyx itself (mPNs b-upper, b-lower and C2) and another (mPN cobra) to the MB vertical lobe (Figure 4a). In addition to the 14 mPNs that project to the brain, we identified an extra 6 oligoglomerular neurons that project to the SEZ (SEZ neurons; Figure 1c; Figure 4—figure supplement 1). A class of mPNs has been described in the adult fly (Liang et al., 2013) but their projection pattern does not match any of the larval mPNs. In strong contrast to uPNs, mPNs are very diverse in their lineage of origin, their pattern of inputs, and the brain areas they target. A small subset of mPNs has been identified via light microscopy before (Thum et al., 2011; Das et al., 2013).10.7554/eLife.14859.012Figure 4.The multiglomerular circuit consists of 14 mPNs that project to the brain and 5 Picky LNs, each an identified neuron.


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)

Six SEZ neurons receive specific inputs from some ORNs and from some antennal lobe LNs.Left, EM-reconstruction of the 6 SEZ neurons (vine, cypress, clamp, spruce and ginkgo 1 and 2), with their axons labeled green and their dendrites blue. Presynaptic sites in red and postsynaptic sites in cyan. Middle, 3 of these SEZ neurons project to the same unidentified region of the SEZ. Spruce projects to a more posterior area. Lateral view, anterior to the left. Right, table of percent of postsynaptic sites of a column neuron contributed by a row neuron, illustrating how some ORNs and LNs specifically target these SEZ neurons. We show only connections with at least two synapses, consistently found among homologous identified neurons in both the left and right antennal lobes. Percentages between 0 and 0.5 are removed. Notice how Picky LNs 2, 3 and 4 synapse strongly onto SEZ neurons.DOI:http://dx.doi.org/10.7554/eLife.14859.013
© Copyright Policy
Related In: Results  -  Collection

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fig4s1: Six SEZ neurons receive specific inputs from some ORNs and from some antennal lobe LNs.Left, EM-reconstruction of the 6 SEZ neurons (vine, cypress, clamp, spruce and ginkgo 1 and 2), with their axons labeled green and their dendrites blue. Presynaptic sites in red and postsynaptic sites in cyan. Middle, 3 of these SEZ neurons project to the same unidentified region of the SEZ. Spruce projects to a more posterior area. Lateral view, anterior to the left. Right, table of percent of postsynaptic sites of a column neuron contributed by a row neuron, illustrating how some ORNs and LNs specifically target these SEZ neurons. We show only connections with at least two synapses, consistently found among homologous identified neurons in both the left and right antennal lobes. Percentages between 0 and 0.5 are removed. Notice how Picky LNs 2, 3 and 4 synapse strongly onto SEZ neurons.DOI:http://dx.doi.org/10.7554/eLife.14859.013
Mentions: Parallel to the uniglomerular readout by the 21 uPNs, we found 14 multiglomerular PNs (mPNs; Figure 4a). Each mPN receives unique and stereotyped inputs from multiple ORNs (Figure 4c) or at least from one ORN and multiple unidentified non-ORN sensory neurons in the SEZ (Figure 4a). The mPNs originate in multiple neuronal lineages and project to multiple brain regions; most commonly the lateral horn (LH) but also regions surrounding the MB calyx. Of the 14 mPNs, three project to the calyx itself (mPNs b-upper, b-lower and C2) and another (mPN cobra) to the MB vertical lobe (Figure 4a). In addition to the 14 mPNs that project to the brain, we identified an extra 6 oligoglomerular neurons that project to the SEZ (SEZ neurons; Figure 1c; Figure 4—figure supplement 1). A class of mPNs has been described in the adult fly (Liang et al., 2013) but their projection pattern does not match any of the larval mPNs. In strong contrast to uPNs, mPNs are very diverse in their lineage of origin, their pattern of inputs, and the brain areas they target. A small subset of mPNs has been identified via light microscopy before (Thum et al., 2011; Das et al., 2013).10.7554/eLife.14859.012Figure 4.The multiglomerular circuit consists of 14 mPNs that project to the brain and 5 Picky LNs, each an identified neuron.

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