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Dendritic integration of sensory and reward information facilitates learning


Schoenfeld, Gwendolin; Kollmorgen, Sepp; Lewis, Christopher; Bethge, Philipp; Reuss, Anna Maria; Aguzzi, Adriano; Mante, Valerio; Helmchen, Fritjof (2021). Dendritic integration of sensory and reward information facilitates learning. bioRxiv 2021.12.28, Cold Spring Harbor Laboratory.

Abstract

Learning goal-directed behaviours requires integration of separate information streams representing context, relevant stimuli and reward. Dendrites of pyramidal neurons are suitable sites for such integration, but it remains elusive how their responses adapt when an animal learns a new task. Here, we identify two distinct classes of dendritic responses that represent either contextual/sensory information or reward information and that differ in their task- and learning-related dynamics. Using longitudinal calcium imaging of apical dendritic tufts of L5 pyramidal neurons in mouse barrel cortex, we tracked dendritic activity across learning and analyzed both local dendritic branch signals and global apical tuft activity. During texture discrimination learning, sensory representations (including contextual and touch information) strengthened and converged on the reward-predicting tactile stimulus when mice became experts. In contrast, reward-associated responses were particularly strong in the naïve condition and became less pronounced upon learning. When we blocked the representation of unexpected reward in naïve animals with optogenetic inhibition, animals failed to learn until we released the block and learning proceeded normally. Our results suggest that reward signals in dendrites are essential for adjusting neuronal integration of converging inputs to facilitate adaptive behaviour.

Abstract

Learning goal-directed behaviours requires integration of separate information streams representing context, relevant stimuli and reward. Dendrites of pyramidal neurons are suitable sites for such integration, but it remains elusive how their responses adapt when an animal learns a new task. Here, we identify two distinct classes of dendritic responses that represent either contextual/sensory information or reward information and that differ in their task- and learning-related dynamics. Using longitudinal calcium imaging of apical dendritic tufts of L5 pyramidal neurons in mouse barrel cortex, we tracked dendritic activity across learning and analyzed both local dendritic branch signals and global apical tuft activity. During texture discrimination learning, sensory representations (including contextual and touch information) strengthened and converged on the reward-predicting tactile stimulus when mice became experts. In contrast, reward-associated responses were particularly strong in the naïve condition and became less pronounced upon learning. When we blocked the representation of unexpected reward in naïve animals with optogenetic inhibition, animals failed to learn until we released the block and learning proceeded normally. Our results suggest that reward signals in dendrites are essential for adjusting neuronal integration of converging inputs to facilitate adaptive behaviour.

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Additional indexing

Item Type:Working Paper
Communities & Collections:07 Faculty of Science > Institute of Neuroinformatics
04 Faculty of Medicine > University Hospital Zurich > Institute of Neuropathology
08 Research Priority Programs > Adaptive Brain Circuits in Development and Learning (AdaBD)
Dewey Decimal Classification:570 Life sciences; biology
610 Medicine & health
Language:English
Date:2021
Deposited On:16 Mar 2022 13:33
Last Modified:22 Sep 2023 13:13
Series Name:bioRxiv
ISSN:2164-7844
OA Status:Green
Free access at:Publisher DOI. An embargo period may apply.
Publisher DOI:https://doi.org/10.1101/2021.12.28.474360
  • Content: Published Version
  • Licence: Creative Commons: Attribution 4.0 International (CC BY 4.0)