The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx
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Evaluation Summary:
The authors show that a widely arborizing inhibitory interneuron AL reduces the variability of olfactory responses in at Drosophila Kenyon postsynapses in the mushroom body calyx, which receive inputs from the projection neurons (PNs) in the antennal lobe. The data support a model in which APL neurons, which also receive inputs from PNs, mediate scaled GABAergic feedback to normalize of postsynaptic responses in the calyx. The conclusions, based on detailed analysis of one odorant are mostly well supported by the data.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Abstract
To identify and memorize discrete but similar environmental inputs, the brain needs to distinguish between subtle differences of activity patterns in defined neuronal populations. The Kenyon cells (KCs) of the Drosophila adult mushroom body (MB) respond sparsely to complex olfactory input, a property that is thought to support stimuli discrimination in the MB. To understand how this property emerges, we investigated the role of the inhibitory anterior paired lateral (APL) neuron in the input circuit of the MB, the calyx. Within the calyx, presynaptic boutons of projection neurons (PNs) form large synaptic microglomeruli (MGs) with dendrites of postsynaptic KCs. Combining electron microscopy (EM) data analysis and in vivo calcium imaging, we show that APL, via inhibitory and reciprocal synapses targeting both PN boutons and KC dendrites, normalizes odour-evoked representations in MGs of the calyx. APL response scales with the PN input strength and is regionalized around PN input distribution. Our data indicate that the formation of a sparse code by the KCs requires APL-driven normalization of their MG postsynaptic responses. This work provides experimental insights on how inhibition shapes sensory information representation in a higher brain centre, thereby supporting stimuli discrimination and allowing for efficient associative memory formation.
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Evaluation Summary:
The authors show that a widely arborizing inhibitory interneuron AL reduces the variability of olfactory responses in at Drosophila Kenyon postsynapses in the mushroom body calyx, which receive inputs from the projection neurons (PNs) in the antennal lobe. The data support a model in which APL neurons, which also receive inputs from PNs, mediate scaled GABAergic feedback to normalize of postsynaptic responses in the calyx. The conclusions, based on detailed analysis of one odorant are mostly well supported by the data.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
Prisco et al. detail how the GABAergic APL neuron normalizes olfactory input to the Drosophila mushroom body, reporting that the APL neuron normalizes olfactory responses in Kenyon cells via scaled inhibition. Silencing APL neurons increases variability in the magnitude of KC olfactory responses. Furthermore, APL provides localized feedback in the MB calyx that may shape the patterns of KC responses locally. This is straightforward manuscript describing a high-quality data set that lays out clear conclusions about the role of GABAergic feedback in shaping olfactory responses in a brain region that is critical for olfactory learning. The conclusions of the paper are well supported by the data for the most paper, though a few additional analysis and experiments would help to clarify the role of the APL neuron …
Reviewer #1 (Public Review):
Prisco et al. detail how the GABAergic APL neuron normalizes olfactory input to the Drosophila mushroom body, reporting that the APL neuron normalizes olfactory responses in Kenyon cells via scaled inhibition. Silencing APL neurons increases variability in the magnitude of KC olfactory responses. Furthermore, APL provides localized feedback in the MB calyx that may shape the patterns of KC responses locally. This is straightforward manuscript describing a high-quality data set that lays out clear conclusions about the role of GABAergic feedback in shaping olfactory responses in a brain region that is critical for olfactory learning. The conclusions of the paper are well supported by the data for the most paper, though a few additional analysis and experiments would help to clarify the role of the APL neuron in modulating KC responses across the calyx.
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Reviewer #2 (Public Review):
The principal neurons of the fly mushroom body, the Kenyon cells, receive input at their dendrites in the calyx: excitatory input from projection neurons and inhibitory input from APL. The anatomical and physiological interaction between these two inputs in the calyx has not yet been examined in detail, and the authors do so here. The study confirms and extends previous findings showing that APL normalizes KC activity by reducing the difference in amplitude in KC activity for odors of different strength, by showing that these effects also extend to KC post-synaptic claws (as opposed to acting only on KC spiking), and by directly comparing the activity of KCs, PNs and APL for different odors. Although the conclusion would be more robust if a larger range of odors was tested and some aspects of the …
Reviewer #2 (Public Review):
The principal neurons of the fly mushroom body, the Kenyon cells, receive input at their dendrites in the calyx: excitatory input from projection neurons and inhibitory input from APL. The anatomical and physiological interaction between these two inputs in the calyx has not yet been examined in detail, and the authors do so here. The study confirms and extends previous findings showing that APL normalizes KC activity by reducing the difference in amplitude in KC activity for odors of different strength, by showing that these effects also extend to KC post-synaptic claws (as opposed to acting only on KC spiking), and by directly comparing the activity of KCs, PNs and APL for different odors. Although the conclusion would be more robust if a larger range of odors was tested and some aspects of the quantification methods could be clarified, the data are well-controlled and persuasive. A particular strength is the use of targeted GCaMP indicators to confine their analysis to pre-synaptic and post-synaptic compartments. The findings improve our understanding of the integration of excitatory and inhibitory inputs in Kenyon cells.
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