Minimal circuit motifs for second-order conditioning in the insect mushroom body

In well-established first-order conditioning experiments, the concurrence of a sensory cue with reinforcement forms an association, allowing the cue to predict future reinforcement. In the insect mushroom body, a brain region central to learning and memory, such associations are encoded in the synap...

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Main Authors: Anna-Maria Jürgensen, Felix Johannes Schmitt, Martin Paul Nawrot
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-01-01
Series:Frontiers in Physiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fphys.2023.1326307/full
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author Anna-Maria Jürgensen
Felix Johannes Schmitt
Martin Paul Nawrot
author_facet Anna-Maria Jürgensen
Felix Johannes Schmitt
Martin Paul Nawrot
author_sort Anna-Maria Jürgensen
collection DOAJ
description In well-established first-order conditioning experiments, the concurrence of a sensory cue with reinforcement forms an association, allowing the cue to predict future reinforcement. In the insect mushroom body, a brain region central to learning and memory, such associations are encoded in the synapses between its intrinsic and output neurons. This process is mediated by the activity of dopaminergic neurons that encode reinforcement signals. In second-order conditioning, a new sensory cue is paired with an already established one that presumably activates dopaminergic neurons due to its predictive power of the reinforcement. We explored minimal circuit motifs in the mushroom body for their ability to support second-order conditioning using mechanistic models. We found that dopaminergic neurons can either be activated directly by the mushroom body’s intrinsic neurons or via feedback from the output neurons via several pathways. We demonstrated that the circuit motifs differ in their computational efficiency and robustness. Beyond previous research, we suggest an additional motif that relies on feedforward input of the mushroom body intrinsic neurons to dopaminergic neurons as a promising candidate for experimental evaluation. It differentiates well between trained and novel stimuli, demonstrating robust performance across a range of model parameters.
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spelling doaj.art-e74fb55701994ac99cd1fe88390441a22024-01-10T04:11:58ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2024-01-011410.3389/fphys.2023.13263071326307Minimal circuit motifs for second-order conditioning in the insect mushroom bodyAnna-Maria JürgensenFelix Johannes SchmittMartin Paul NawrotIn well-established first-order conditioning experiments, the concurrence of a sensory cue with reinforcement forms an association, allowing the cue to predict future reinforcement. In the insect mushroom body, a brain region central to learning and memory, such associations are encoded in the synapses between its intrinsic and output neurons. This process is mediated by the activity of dopaminergic neurons that encode reinforcement signals. In second-order conditioning, a new sensory cue is paired with an already established one that presumably activates dopaminergic neurons due to its predictive power of the reinforcement. We explored minimal circuit motifs in the mushroom body for their ability to support second-order conditioning using mechanistic models. We found that dopaminergic neurons can either be activated directly by the mushroom body’s intrinsic neurons or via feedback from the output neurons via several pathways. We demonstrated that the circuit motifs differ in their computational efficiency and robustness. Beyond previous research, we suggest an additional motif that relies on feedforward input of the mushroom body intrinsic neurons to dopaminergic neurons as a promising candidate for experimental evaluation. It differentiates well between trained and novel stimuli, demonstrating robust performance across a range of model parameters.https://www.frontiersin.org/articles/10.3389/fphys.2023.1326307/fullassociative leaningmushroom bodysecond-order conditioningclassical conditioningmechanistic modellearning and memory
spellingShingle Anna-Maria Jürgensen
Felix Johannes Schmitt
Martin Paul Nawrot
Minimal circuit motifs for second-order conditioning in the insect mushroom body
Frontiers in Physiology
associative leaning
mushroom body
second-order conditioning
classical conditioning
mechanistic model
learning and memory
title Minimal circuit motifs for second-order conditioning in the insect mushroom body
title_full Minimal circuit motifs for second-order conditioning in the insect mushroom body
title_fullStr Minimal circuit motifs for second-order conditioning in the insect mushroom body
title_full_unstemmed Minimal circuit motifs for second-order conditioning in the insect mushroom body
title_short Minimal circuit motifs for second-order conditioning in the insect mushroom body
title_sort minimal circuit motifs for second order conditioning in the insect mushroom body
topic associative leaning
mushroom body
second-order conditioning
classical conditioning
mechanistic model
learning and memory
url https://www.frontiersin.org/articles/10.3389/fphys.2023.1326307/full
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