The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx

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 propert...

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Main Authors: Luigi Prisco, Stephan Hubertus Deimel, Hanna Yeliseyeva, André Fiala, Gaia Tavosanis
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2021-12-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/74172
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author Luigi Prisco
Stephan Hubertus Deimel
Hanna Yeliseyeva
André Fiala
Gaia Tavosanis
author_facet Luigi Prisco
Stephan Hubertus Deimel
Hanna Yeliseyeva
André Fiala
Gaia Tavosanis
author_sort Luigi Prisco
collection DOAJ
description 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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spelling doaj.art-fa87f2ac90604ac6bf8114096d72cd9a2022-12-22T04:28:58ZengeLife Sciences Publications LtdeLife2050-084X2021-12-011010.7554/eLife.74172The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyxLuigi Prisco0https://orcid.org/0000-0002-5896-9346Stephan Hubertus Deimel1https://orcid.org/0000-0002-4678-4926Hanna Yeliseyeva2André Fiala3https://orcid.org/0000-0002-9745-5145Gaia Tavosanis4https://orcid.org/0000-0002-8679-5515Dynamics of neuronal circuits, German Center for Neurodegenerative Diseases (DZNE), Bonn, GermanyDepartment of Molecular Neurobiology of Behavior, University of Göttingen, Göttingen, GermanyDynamics of neuronal circuits, German Center for Neurodegenerative Diseases (DZNE), Bonn, GermanyDepartment of Molecular Neurobiology of Behavior, University of Göttingen, Göttingen, GermanyDynamics of neuronal circuits, German Center for Neurodegenerative Diseases (DZNE), Bonn, Germany; LIMES, Rheinische Friedrich Wilhelms Universität Bonn, Bonn, GermanyTo 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.https://elifesciences.org/articles/74172mushroom bodyAPLmicroglomerulussparse codinginhibitionpattern separation
spellingShingle Luigi Prisco
Stephan Hubertus Deimel
Hanna Yeliseyeva
André Fiala
Gaia Tavosanis
The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx
eLife
mushroom body
APL
microglomerulus
sparse coding
inhibition
pattern separation
title The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx
title_full The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx
title_fullStr The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx
title_full_unstemmed The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx
title_short The anterior paired lateral neuron normalizes odour-evoked activity in the Drosophila mushroom body calyx
title_sort anterior paired lateral neuron normalizes odour evoked activity in the drosophila mushroom body calyx
topic mushroom body
APL
microglomerulus
sparse coding
inhibition
pattern separation
url https://elifesciences.org/articles/74172
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