The cellular architecture of memory modules in Drosophila supports stochastic input integration

The ability to associate neutral stimuli with valence information and to store these associations as memories forms the basis for decision making. To determine the underlying computational principles, we build a realistic computational model of a central decision module within the Drosophila mushroo...

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Main Authors: Omar A Hafez, Benjamin Escribano, Rouven L Ziegler, Jan J Hirtz, Ernst Niebur, Jan Pielage
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2023-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/77578
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author Omar A Hafez
Benjamin Escribano
Rouven L Ziegler
Jan J Hirtz
Ernst Niebur
Jan Pielage
author_facet Omar A Hafez
Benjamin Escribano
Rouven L Ziegler
Jan J Hirtz
Ernst Niebur
Jan Pielage
author_sort Omar A Hafez
collection DOAJ
description The ability to associate neutral stimuli with valence information and to store these associations as memories forms the basis for decision making. To determine the underlying computational principles, we build a realistic computational model of a central decision module within the Drosophila mushroom body (MB), the fly’s center for learning and memory. Our model combines the electron microscopy-based architecture of one MB output neuron (MBON-α3), the synaptic connectivity of its 948 presynaptic Kenyon cells (KCs), and its membrane properties obtained from patch-clamp recordings. We show that this neuron is electrotonically compact and that synaptic input corresponding to simulated odor input robustly drives its spiking behavior. Therefore, sparse innervation by KCs can efficiently control and modulate MBON activity in response to learning with minimal requirements on the specificity of synaptic localization. This architecture allows efficient storage of large numbers of memories using the flexible stochastic connectivity of the circuit.
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spelling doaj.art-53875d7a61d54b76b954c5a163ef0f4d2023-04-03T15:44:52ZengeLife Sciences Publications LtdeLife2050-084X2023-03-011210.7554/eLife.77578The cellular architecture of memory modules in Drosophila supports stochastic input integrationOmar A Hafez0https://orcid.org/0000-0002-7846-9226Benjamin Escribano1https://orcid.org/0000-0002-1432-5952Rouven L Ziegler2https://orcid.org/0000-0002-3050-7692Jan J Hirtz3https://orcid.org/0000-0002-4486-3057Ernst Niebur4https://orcid.org/0000-0002-2815-9262Jan Pielage5https://orcid.org/0000-0002-5115-5884Zanvyl Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, United StatesDivision of Neurobiology and Zoology, Department of Biology, University of Kaiserslautern, Kaiserslautern, GermanyDivision of Neurobiology and Zoology, Department of Biology, University of Kaiserslautern, Kaiserslautern, GermanyPhysiology of Neuronal Networks Group, Department of Biology, University of Kaiserslautern, Kaiserslautern, GermanyZanvyl Krieger Mind/Brain Institute, Johns Hopkins University, Baltimore, United States; Solomon Snyder Department of Neuroscience, Johns Hopkins University, Baltimore, United StatesDivision of Neurobiology and Zoology, Department of Biology, University of Kaiserslautern, Kaiserslautern, GermanyThe ability to associate neutral stimuli with valence information and to store these associations as memories forms the basis for decision making. To determine the underlying computational principles, we build a realistic computational model of a central decision module within the Drosophila mushroom body (MB), the fly’s center for learning and memory. Our model combines the electron microscopy-based architecture of one MB output neuron (MBON-α3), the synaptic connectivity of its 948 presynaptic Kenyon cells (KCs), and its membrane properties obtained from patch-clamp recordings. We show that this neuron is electrotonically compact and that synaptic input corresponding to simulated odor input robustly drives its spiking behavior. Therefore, sparse innervation by KCs can efficiently control and modulate MBON activity in response to learning with minimal requirements on the specificity of synaptic localization. This architecture allows efficient storage of large numbers of memories using the flexible stochastic connectivity of the circuit.https://elifesciences.org/articles/77578mushroom body output neurondendritic signal processingdecision makinglong term memoryneuronal output tuningshort term memory
spellingShingle Omar A Hafez
Benjamin Escribano
Rouven L Ziegler
Jan J Hirtz
Ernst Niebur
Jan Pielage
The cellular architecture of memory modules in Drosophila supports stochastic input integration
eLife
mushroom body output neuron
dendritic signal processing
decision making
long term memory
neuronal output tuning
short term memory
title The cellular architecture of memory modules in Drosophila supports stochastic input integration
title_full The cellular architecture of memory modules in Drosophila supports stochastic input integration
title_fullStr The cellular architecture of memory modules in Drosophila supports stochastic input integration
title_full_unstemmed The cellular architecture of memory modules in Drosophila supports stochastic input integration
title_short The cellular architecture of memory modules in Drosophila supports stochastic input integration
title_sort cellular architecture of memory modules in drosophila supports stochastic input integration
topic mushroom body output neuron
dendritic signal processing
decision making
long term memory
neuronal output tuning
short term memory
url https://elifesciences.org/articles/77578
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