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Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Nature. Author manuscript; available in PMC Feb 19, 2010.
Published in final edited form as:
PMCID: PMC2824883
NIHMSID: NIHMS175732

Lateral presynaptic inhibition mediates gain control in an olfactory circuit

SUMMARY

Olfactory signals are transduced by a large family of odorant receptor proteins, each of which corresponds to a unique glomerulus in the first olfactory relay of the brain. Cross-talk between glomeruli has been proposed to be important in olfactory processing, but it is not clear how these interactions shape the odor responses of second-order neurons. In the Drosophila antennal lobe (a region analogous to the vertebrate olfactory bulb), we selectively remove most inter-glomerular input to identified second-order olfactory neurons. We find this broadens the odor tuning of these neurons, implying that inter-glomerular inhibition dominates over inter-glomerular excitation. The strength of this inhibitory signal scales with total feedforward input to the entire antennal lobe, and has similar tuning in different glomeruli. A substantial portion of this inter-glomerular inhibition acts at a presynaptic locus, and our results imply this is mediated by both GABAA and GABAB receptors on the same nerve terminal.

A sensory stimulus generally triggers activity in multiple neural processing channels, each of which carries information about some feature of that stimulus. The concept of a processing channel has a particularly clear anatomical basis in the first relay of the olfactory system, which is typically divided into glomerular compartments. Each glomerulus receives input from many first-order olfactory receptor neurons (ORNs), all of which express the same odorant receptor. Each second-order neuron receives direct ORN input from a single glomerulus, and thus all the first- and second-order neurons corresponding to a glomerulus constitute a discrete processing channel. An odorant typically triggers activity in multiple glomeruli, and local interneurons that interconnect glomeruli provide a substrate for cross-talk between channels.

The Drosophila antennal lobe is a favored model for investigating olfactory processing because it contains only ~50 glomeruli1, each of which corresponds to an identified type of ORN and an identified type of postsynaptic projection neuron (PN)25. Several recent studies of the Drosophila antennal lobe have produced divergent views of the relative importance of inter-glomerular connections. One model proposes that PN odor responses are almost completely determined by feedforward excitation6, 7. This model ascribes little importance to cross-talk between glomerular processing channels. An alternative model proposes that inter-glomerular connections make an important contribution to shaping PN odor responses812. However, this has not been demonstrated by showing a change in PN odor responses when lateral inputs to that PN are removed. (We use the word “lateral” as a synonym for “inter-glomerular”.)

In principle, several features of olfactory processing in the Drosophila antennal lobe could reflect either intra- or inter-glomerular events. For example, most PNs are more broadly tuned to odors than their presynaptic ORNs8, 10. This could reflect a purely intra-glomerular nonlinear process, such as short-term synaptic depression at ORN-PN connections. Alternatively, it could be due to the fact that lateral excitatory connections exist between glomeruli7, 11, 12. It is also unclear whether inhibitory epochs in PN odor responses810 reflect inter- or intra-glomerular events. Many GABAergic interneurons form connections between glomeruli9, 13, 14, but several recent studies have failed to observe any inter-glomerular inhibition7, 11, 12. These studies removed all the direct ORN inputs to an identified PN, and asked whether lateral input could be evoked in that PN by olfactory stimulation of other ORN types. In all cases, lateral inputs to PNs were excitatory. This raises the possibility that inter-glomerular inhibition might not exist, and inhibitory PN odor responses might merely reflect intra-glomerular feedback1517. This is an important issue because intra- and inter-glomerular inhibition have different consequences for how olfactory representations are transformed in this circuit.

In this study, we addressed three questions: Do inter-glomerular interactions make a substantial contribution to PN odor responses? Do these interactions include lateral inhibition? If so, how does this occur, and why has it been difficult to observe?

Removing lateral input to PNs

We began by investigating what happens to PN odor responses when most lateral input to that PN is removed. We took advantage of the fact that the fly has two olfactory organs. About 90% of ORNs are contained in the antennae, with 10% in the maxillary palp (Fig. 1a). Palp ORNs express odorant receptors not expressed in the antennae, and project to palp glomeruli that are distinct from glomeruli targeted by antennal ORNs3, 4. Antennal and palp glomeruli are interconnected by local interneurons. Acute removal of the antennae eliminates 90% of the input to the antennal lobe, and thus most excitatory drive to local interneurons (Fig. 1b). If lateral connections are mainly excitatory7, 11, 12, then removing the antennae should decrease the odor responses of palp PNs.

Figure 1
Removing lateral input disinhibits PNs

We performed this experiment in two different palp glomeruli (VM7 and VC1). Surprisingly, removing the antennae increased most of the odor responses of these PNs (Fig. 1c,d; Supplementary Figs. 2,3). No odor responses were decreased. This implies that most of our odors normally evoke lateral inhibitory input to these glomeruli, and this outweighs the effect of lateral excitatory input.

We examined the input-output function of each glomerulus by plotting the strength of each PN odor response versus the strength of the cognate ORN response to the same odor. These input-output functions were nonlinear (Fig. 1d), which is typical for most glomeruli10. When we removed most lateral input to PNs, the nonlinearity persisted (Fig. 1d), and PNs became even more broadly tuned (Fig. 1e). This argues that broad PN tuning8, 10 results mainly from purely intra-glomerular mechanisms. These could include short-term synaptic depression at ORN-PN connections, and/or an intrinsic ceiling on PN firing rates. Lateral excitation should tend to broaden PN tuning even more, but lateral inhibition evidently counteracts this.

One clue to the significance of lateral inputs is that in the intact antennal lobe circuit, PN responses cannot be predicted purely on the basis of feedforward excitatory inputs10. Two odors can elicit similar responses in an ORN, but divergent responses in a postsynaptic PN. For example, pentyl acetate and 4-methyl phenol evoke similar activity in VM7 ORNs, but not in VM7 PNs (Fig. 1c), implying that these odors recruit different lateral inputs to this glomerulus. After antennae were removed, these odors evoked similar responses in VM7 PNs (Fig. 1c). Overall, removing the antenna increased the correlation between the ranked odor preferences of ORNs and their cognate PNs (Spearman’s ρ increased from 0.82 to 0.88 for VM7, from 0.89 to 0.94 for VC1; p < 0.02 for each comparison, Mann-Whitney U-test).

Lateral inhibition suppresses ORN input

Several recent studies have failed to observe lateral inhibition in the Drosophila antennal lobe7, 11, 12. These studies silenced all direct ORN inputs to a PN, and focused on lateral input to that PN evoked by stimulating ORNs presynaptic to other glomeruli. We reasoned that some lateral inhibition might target ORN axon terminals; if so, this would only be observed when the direct ORN inputs to a PN are active. GABAergic inhibition at ORN axon terminals has been described previously in the olfactory bulb1521, and synapses from GABAergic interneurons onto ORN axon terminals have been found in an insect antennal lobe22.

To test the idea that some lateral inhibition is presynaptic, we asked how lateral input to glomerulus VM7 depends on the activity of VM7 ORNs. Each VM7 ORN fires spontaneously at ~10 spikes/s, and consequently these PNs are bombarded by spontaneous spike-driven EPSPs (Supplementary Fig. 4a). When we silenced VM7 ORNs by removing the maxillary palps, large spontaneous EPSPs disappeared in these PNs (Fig. 2a). In this experimental configuration, stimulating the antennae with odorants depolarized VM7 PNs (Fig. 2a), which is consistent with previous reports that lateral input is excitatory when direct ORN inputs are silent7, 11, 12. Next, we asked whether preserving spontaneous activity in VM7 ORNs would allow us to observe lateral inhibition. To prevent odor-evoked activity in VM7 ORNs, we covered the maxillary palps with a plastic shield. We inferred that the shield did not prevent spontaneous activity in VM7 ORNs because we observed normal spontaneous EPSPs in VM7 PNs (Fig. 2b). The shield was clearly an effective barrier to odors because it blocked the normal strong excitatory response to ethyl butyrate in VM7 PNs (Fig. 2b, Supplementary Fig. 4). Rather, when the palps were shielded, stimulating the antennae with odorants suppressed spontaneous EPSPs in VM7 PNs (Fig. 2b,c). This was accompanied by hyperpolarization of the membrane potential, which would reflect (at least in part) the removal of ongoing depolarization produced by EPSP bombardment.

Figure 2
Lateral inhibition suppresses spontaneous EPSCs and scales with total ORN input

For all 20 odors in our panel, lateral input depolarized VM7 PNs when their cognate ORNs were absent (as in Fig. 2a), and hyperpolarized these PNs when their ORNs were spontaneously active (as in Fig. 2b). This argues that a substantial component of lateral inhibition acts at a presynaptic locus. This does not mean that all lateral inhibition is presynaptic; indeed there is evidence for an additional postsynaptic component (Supplementary Fig. 5).

Inhibition scales with total ORN input

When palp ORNs were shielded, different odors evoked different amounts of inhibition in glomerulus VM7 (Fig. 2c, black traces). We hypothesized that this odor tuning could explain why antennal removal disinhibits some VM7 PN odor responses more than others (Fig. 1c,d). To test this, we measured the amount of inhibition evoked by each odor in the shielded-palps experiment, and compared this to the change in PN spiking responses to that odor after antennal removal. These two measures were well-correlated (Fig. 2d, n = 20 odors, Pearson’s r2 = 0.65, p < 0.0001), which argues that these two experimental paradigms measure the same underlying phenomenon.

The odor tuning of lateral input must reflect the connectivity of the local interneurons that mediate this inhibition. Many individual GABAergic interneurons innervate all glomeruli9, 12, 13, suggesting that lateral inhibition to each glomerulus might reflect pooled input from all ORNs. If so, then the size of lateral input to a glomerulus should correlate with the total ORN activity evoked by that odor. We estimated total ORN activity by summing the spiking responses of each antennal ORN type23, and found that this measure predicted the strength of lateral inhibition evoked by each odor in the shielded-palps experiment (Fig. 2e, n = 14 odors, Pearson’s r2 = 0.73, p < 0.0005).

If lateral inhibition to all glomeruli scales with total ORN activity, then lateral inhibitory input to each glomerulus would show the same odor tuning. We have already shown that the odor tuning of lateral input to VM7 is a good predictor of which odor responses were most disinhibited in VM7 PNs after antennal removal (Fig. 2d). As expected, it also partially predicted which odor responses were most disinhibited in a different palp glomerulus, VC1 (Fig. 2f, n = 20 odors, Pearson’s r2 = 0.32, p < 0.01). However, this correlation was weaker than the correlation with disinhibition in VM7. This leaves open the possibility that there may be some differences in the odor tuning of lateral inhibitory input to different glomeruli (see Discussion).

GABA mediates presynaptic inhibition

Our results suggest that much of the lateral inhibition in this circuit acts by suppressing ORN-PN synaptic transmission. To test this, we monitored ORN-PN synaptic strength in one glomerulus while recruiting lateral input to that glomerulus (Fig. 3a). We recorded from an identified PN while electrically stimulating the ipsilateral antennal nerve to evoke excitatory postsynaptic currents (EPSCs). Next, we used an odor to stimulate ORNs in the remaining intact antenna (and the maxillary palps). Because most glomeruli receive bilateral ORN input2, olfactory stimulation of the contralateral antenna drives activity in ipsilateral glomeruli. Finally, we prevented odors from recruiting direct ORN input to the recorded PN by mutating the odorant receptor gene normally expressed by its ORNs.

Figure 3
Lateral GABAergic suppression of ORN-PN synapses

As predicted, olfactory stimulation of the contralateral antenna inhibited EPSCs evoked by ipsilateral nerve stimulation (Fig. 3b,c). We could mimic this inhibition by iontophoresing GABA into the antennal lobe neuropil (Fig. 3d–f). A GABAB receptor antagonist blocked the late phase of this inhibition, but had only a modest effect on the early phase (Fig. 3c,f). Adding a GABAA antagonist to the GABAB antagonist blocked the residual early portion of the inhibition (Fig. 3c,f). The GABAA antagonist alone had no effect (Fig. 3c,f). Taken together, these results suggest that both GABAA and GABAB receptors are present on the same ORN axon terminals, and either GABAA or GABAB receptors alone are sufficient to mediate substantial inhibition of EPSCs just after GABA release. The late phase of inhibition evidently involves only GABAB receptors.

Presynaptic inhibition is generally associated with a change in the way a synapse responds to paired electrical pulses24. We found that both the GABAA and GABAB components of EPSC inhibition are associated with an increase in the paired-pulse ratio (Supplementary Fig. 7). This implies that the independent actions of both GABAA and GABAB receptors are at least partially presynaptic. As a further test of this model, we genetically abolished GABAB signaling selectively in presynaptic ORNs. We used an ORN-specific promoter25 to drive expression of pertussis toxin26, a selective inhibitor of some types of G-proteins. In these flies, GABA still inhibited ORN-PN EPSCs, but now this inhibition had a briefer duration than in wild-type flies (Fig. 4a,b). Unlike in wild-type flies, this inhibition was completely resistant to the GABAB antagonist and completely blocked by the GABAA antagonist (compare Fig. 4c to Fig. 3f). As a negative control, we confirmed that this phenotype requires both the ORN-specific promoter and the toxin transgene (Supplementary Fig. 8). This demonstrates that GABAB receptors inhibit ORN-PN synapses at a purely presynaptic locus.

Figure 4
Genetic evidence that GABAB receptors inhibit ORN-PN synapses at a presynaptic locus

If activation of either GABAA or GABAB receptors is sufficient to mediate strong lateral inhibition, then blockade of both receptors should be required to mimic the removal of lateral input. To test this, we again recorded from palp PNs in glomerulus VM7. Normally, the odor pentyl acetate weakly excites VM7 ORNs and inhibits VM7 PNs. When most lateral input is removed (by removing the antennae), this odor strongly excites these PNs (Fig. 1c). We could not mimic this disinhibition by applying either a GABAA or a GABAB receptor antagonist alone. However, the two antagonists together produced strong disinhibition that resembled the effect of removing the antennae (Fig. 5).

Figure 5
GABA receptor antagonists mimic removal of lateral input to a PN

Discussion

Many previous studies have shown that odors can inhibit spiking in olfactory bulb mitral cells and antennal lobe projection neurons (see refs. 2732 for early examples), but in principle this inhibition could be purely intra-glomerular1517. Experiments in vitro have revealed several types of inter-glomerular circuits3335, but some of these circuits are evidently not recruited by olfactory stimuli15. Here we have directly demonstrated an important role for inhibitory interactions between olfactory glomeruli in vivo.

Our results argue that a substantial component of inter-glomerular inhibition occurs at a presynaptic locus. Previous studies in other species have shown that GABA can inhibit release from ORN axon terminals1521. Our results imply that in Drosophila this is mediated by both GABAA and GABAB receptors. This arrangement is unusual but not unique; for example, there are several instances of GABAA and GABAB inhibition at the same presynaptic site in other neural circuits3639. Ionotropic and metabotropic receptors act with different kinetics, and so this arrangement might ensure that inhibition spans a broad time window. Although both receptor types were co-active during most of the odor response, we noticed that GABAA receptors were required for the a brief early phase of inhibition after odor onset (Fig. 5), while GABAB receptors were required for the long, late phase (Fig. 3 and Fig. 5).

We have shown that lateral inhibitory input to a glomerulus roughly scales with total ORN activity. This would imply that the odor tuning of GABAergic input to each glomerulus is approximately similar. However, the effects of lateral input may nevertheless be somewhat glomerulus-specific. Even if the odor tuning of GABA release were identical in all glomeruli, the efficacy of presynaptic inhibition will vary with presynaptic membrane potential40, 41. As a result, the same inhibitory signal should be more effective in some glomeruli than in others. Also, in some glomeruli, lateral inhibition might be outweighed by lateral excitation. This would explain why other studies have found that some PNs can be excited by odors that do not excite their cognate ORNs8, 10, 42.

In sum, we propose that this form of gain control represents a flexible balance between sensitivity and efficiency. When total ORN input is weak, lateral inhibition is minimal, and ORN-PN synapses are strong. When an odorant recruits vigorous ORN input to many glomeruli, GABAergic interneurons inhibit ORN neurotransmitter release. This should prevent a stimulus from saturating the dynamic range of many PN types simultaneously. Because this mechanism suppresses responses that are strong and redundant, it may tend to decrease cross-correlations between the output of different glomeruli, and thus promote a more efficient neural code for odors.

Methods Summary

In vivo whole-cell patch clamp recordings from PNs and extracellular recordings from ORNs were performed essentially as previously described811, 42. Antagonists (CGP54626 50 µM and picrotoxin 5 µM) were added to the saline which perfused the brain. Pertussis toxin was expressed under control of the Or83b-Gal4 driver. All data in Results are mean values, averaged across experiments, ± s.e.m. (except for raw electrophysiological traces and rasters). The odor stimulus period was 500 ms (shown as black bar in Figures).

Supplementary Material

Supplementary material

Acknowledgments

We are grateful to K. Ito, L. Luo, G. Roman, D.P. Smith, L.M. Stevens, and L.B. Vosshall for gifts of fly stocks. We thank G. Laurent, A.W. Liu, and members of the Wilson lab for helpful conversations. This work was funded by a grant from the NIDCD, the Pew, McKnight, Sloan, and Beckman Foundations (to R.I.W.). S.R.O. was partially supported by a NSF fellowship.

Footnotes

Full Methods are available in the online version of the paper at www.nature.com/nature.

Supplementary Information is linked to the online version of the paper at www.nature.com/nature. A figure summarizing the main result of this paper is available in Supplementary Information.

Author Contributions. S.R.O. performed the experiments and analyzed the data. S.R.O. and R.I.W. designed the experiments and wrote the paper.

Author Information. Reprints and permissions are available at www.nature.com/reprints.

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