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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

Distribution of postsynaptic sites on the uPN dendrites.We show 5 examples, plotting the distance (along the cable) of individual postsynaptic sites (colored dots) to the axon initial segment of each uPN. The same type of presynaptic neuron presents the same color across all plots. Notice how Choosy LN inputs (red, framed in a red box) onto uPNs are generally more proximal to the axon initial segment than other inhibitory inputs such as from Broad LNs; particularly noticeable for 42a PN (top row) and 94 & 94b PN (bottom row). No noticeable difference exists between Broad LN Duet and Trio. Notice that the left 49a PN presents an arbor with two main dendrites, with one being further than the other from the axon initial segment, explaining the split in the distribution of distances of postsynaptic sites. While 67b PN (third row) does not receive inputs from Choosy LNs, the Picky LN 3 (light green), which specifically targets 67b PN and no other uPN, provides proximal inputs. Presynaptic neurons are ordered with the largest contributor at the bottom of each plot.DOI:http://dx.doi.org/10.7554/eLife.14859.011
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fig3s2: Distribution of postsynaptic sites on the uPN dendrites.We show 5 examples, plotting the distance (along the cable) of individual postsynaptic sites (colored dots) to the axon initial segment of each uPN. The same type of presynaptic neuron presents the same color across all plots. Notice how Choosy LN inputs (red, framed in a red box) onto uPNs are generally more proximal to the axon initial segment than other inhibitory inputs such as from Broad LNs; particularly noticeable for 42a PN (top row) and 94 & 94b PN (bottom row). No noticeable difference exists between Broad LN Duet and Trio. Notice that the left 49a PN presents an arbor with two main dendrites, with one being further than the other from the axon initial segment, explaining the split in the distribution of distances of postsynaptic sites. While 67b PN (third row) does not receive inputs from Choosy LNs, the Picky LN 3 (light green), which specifically targets 67b PN and no other uPN, provides proximal inputs. Presynaptic neurons are ordered with the largest contributor at the bottom of each plot.DOI:http://dx.doi.org/10.7554/eLife.14859.011

Mentions: Another GABAergic cell type, that we call the Choosy LNs (two neurons; Figures 1c, 3c, Figure 1—figure supplement 3), contributes exclusively to postsynaptic inhibition for most glomeruli. Unlike the Broad LNs, Choosy LNs have a clear axon innervating most glomeruli, while their dendrites collect inputs from only a small subset of glomeruli (Figure 3c; Figure 1—figure supplement 3; Figure 3—figure supplement 1). Therefore some glomeruli can drive postsynaptic inhibition of most glomeruli. Additionally, the inputs from Choosy LNs tend to be more proximal to the axon initial segment of the uPNs (Gouwens and Wilson, 2009) unlike those of Broad LNs which are more uniformly distributed throughout the uPN dendritic arbor (Figure 3—figure supplement 2). In the adult, ORNs tend to synapse at the most distal PN dendritic terminals, allowing for some LN inhibition to occur via synapses more proximal to the axon initial segment (Rybak et al., 2016). This pattern of spatially structured inputs suggests that different inhibitory LN types may exert different effects on uPN dendritic integration.


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)

Distribution of postsynaptic sites on the uPN dendrites.We show 5 examples, plotting the distance (along the cable) of individual postsynaptic sites (colored dots) to the axon initial segment of each uPN. The same type of presynaptic neuron presents the same color across all plots. Notice how Choosy LN inputs (red, framed in a red box) onto uPNs are generally more proximal to the axon initial segment than other inhibitory inputs such as from Broad LNs; particularly noticeable for 42a PN (top row) and 94 & 94b PN (bottom row). No noticeable difference exists between Broad LN Duet and Trio. Notice that the left 49a PN presents an arbor with two main dendrites, with one being further than the other from the axon initial segment, explaining the split in the distribution of distances of postsynaptic sites. While 67b PN (third row) does not receive inputs from Choosy LNs, the Picky LN 3 (light green), which specifically targets 67b PN and no other uPN, provides proximal inputs. Presynaptic neurons are ordered with the largest contributor at the bottom of each plot.DOI:http://dx.doi.org/10.7554/eLife.14859.011
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4930330&req=5

fig3s2: Distribution of postsynaptic sites on the uPN dendrites.We show 5 examples, plotting the distance (along the cable) of individual postsynaptic sites (colored dots) to the axon initial segment of each uPN. The same type of presynaptic neuron presents the same color across all plots. Notice how Choosy LN inputs (red, framed in a red box) onto uPNs are generally more proximal to the axon initial segment than other inhibitory inputs such as from Broad LNs; particularly noticeable for 42a PN (top row) and 94 & 94b PN (bottom row). No noticeable difference exists between Broad LN Duet and Trio. Notice that the left 49a PN presents an arbor with two main dendrites, with one being further than the other from the axon initial segment, explaining the split in the distribution of distances of postsynaptic sites. While 67b PN (third row) does not receive inputs from Choosy LNs, the Picky LN 3 (light green), which specifically targets 67b PN and no other uPN, provides proximal inputs. Presynaptic neurons are ordered with the largest contributor at the bottom of each plot.DOI:http://dx.doi.org/10.7554/eLife.14859.011
Mentions: Another GABAergic cell type, that we call the Choosy LNs (two neurons; Figures 1c, 3c, Figure 1—figure supplement 3), contributes exclusively to postsynaptic inhibition for most glomeruli. Unlike the Broad LNs, Choosy LNs have a clear axon innervating most glomeruli, while their dendrites collect inputs from only a small subset of glomeruli (Figure 3c; Figure 1—figure supplement 3; Figure 3—figure supplement 1). Therefore some glomeruli can drive postsynaptic inhibition of most glomeruli. Additionally, the inputs from Choosy LNs tend to be more proximal to the axon initial segment of the uPNs (Gouwens and Wilson, 2009) unlike those of Broad LNs which are more uniformly distributed throughout the uPN dendritic arbor (Figure 3—figure supplement 2). In the adult, ORNs tend to synapse at the most distal PN dendritic terminals, allowing for some LN inhibition to occur via synapses more proximal to the axon initial segment (Rybak et al., 2016). This pattern of spatially structured inputs suggests that different inhibitory LN types may exert different effects on uPN dendritic integration.

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