Learning enhances behaviorally relevant representations in apical dendrites

Learning alters cortical representations and improves perception. Apical tuft dendrites in cortical layer 1, which are unique in their connectivity and biophysical properties, may be a key site of learning-induced plasticity. We used both two-photon and SCAPE microscopy to longitudinally track tuft-...

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Main Authors: Sam E Benezra, Kripa B Patel, Citlali Perez Campos, Elizabeth MC Hillman, Randy M Bruno
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
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Online Access:https://elifesciences.org/articles/98349
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author Sam E Benezra
Kripa B Patel
Citlali Perez Campos
Elizabeth MC Hillman
Randy M Bruno
author_facet Sam E Benezra
Kripa B Patel
Citlali Perez Campos
Elizabeth MC Hillman
Randy M Bruno
author_sort Sam E Benezra
collection DOAJ
description Learning alters cortical representations and improves perception. Apical tuft dendrites in cortical layer 1, which are unique in their connectivity and biophysical properties, may be a key site of learning-induced plasticity. We used both two-photon and SCAPE microscopy to longitudinally track tuft-wide calcium spikes in apical dendrites of layer 5 pyramidal neurons in barrel cortex as mice learned a tactile behavior. Mice were trained to discriminate two orthogonal directions of whisker stimulation. Reinforcement learning, but not repeated stimulus exposure, enhanced tuft selectivity for both directions equally, even though only one was associated with reward. Selective tufts emerged from initially unresponsive or low-selectivity populations. Animal movement and choice did not account for changes in stimulus selectivity. Enhanced selectivity persisted even after rewards were removed and animals ceased performing the task. We conclude that learning produces long-lasting realignment of apical dendrite tuft responses to behaviorally relevant dimensions of a task.
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spelling doaj-art-05905ff63cb749ad88fd36b2272ce9312025-01-17T17:03:30ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.98349Learning enhances behaviorally relevant representations in apical dendritesSam E Benezra0Kripa B Patel1Citlali Perez Campos2Elizabeth MC Hillman3https://orcid.org/0000-0001-5511-1451Randy M Bruno4https://orcid.org/0000-0002-5122-4632Department of Neuroscience, Columbia University, New York, United States; Kavli Institute for Brain Science, Columbia University, New York, United StatesKavli Institute for Brain Science, Columbia University, New York, United States; Departments of Biomedical Engineering and Radiology, Columbia University, New York, United StatesKavli Institute for Brain Science, Columbia University, New York, United States; Departments of Biomedical Engineering and Radiology, Columbia University, New York, United StatesDepartment of Neuroscience, Columbia University, New York, United States; Kavli Institute for Brain Science, Columbia University, New York, United States; Departments of Biomedical Engineering and Radiology, Columbia University, New York, United StatesDepartment of Neuroscience, Columbia University, New York, United States; Kavli Institute for Brain Science, Columbia University, New York, United States; Zuckerman Mind Brain Behavior Institute, Columbia University, New York, United States; Department of Physiology, Anatomy & Genetics, University of Oxford, Oxford, United KingdomLearning alters cortical representations and improves perception. Apical tuft dendrites in cortical layer 1, which are unique in their connectivity and biophysical properties, may be a key site of learning-induced plasticity. We used both two-photon and SCAPE microscopy to longitudinally track tuft-wide calcium spikes in apical dendrites of layer 5 pyramidal neurons in barrel cortex as mice learned a tactile behavior. Mice were trained to discriminate two orthogonal directions of whisker stimulation. Reinforcement learning, but not repeated stimulus exposure, enhanced tuft selectivity for both directions equally, even though only one was associated with reward. Selective tufts emerged from initially unresponsive or low-selectivity populations. Animal movement and choice did not account for changes in stimulus selectivity. Enhanced selectivity persisted even after rewards were removed and animals ceased performing the task. We conclude that learning produces long-lasting realignment of apical dendrite tuft responses to behaviorally relevant dimensions of a task.https://elifesciences.org/articles/98349apical dendritelayer 1learningmemoryplasticityreward
spellingShingle Sam E Benezra
Kripa B Patel
Citlali Perez Campos
Elizabeth MC Hillman
Randy M Bruno
Learning enhances behaviorally relevant representations in apical dendrites
eLife
apical dendrite
layer 1
learning
memory
plasticity
reward
title Learning enhances behaviorally relevant representations in apical dendrites
title_full Learning enhances behaviorally relevant representations in apical dendrites
title_fullStr Learning enhances behaviorally relevant representations in apical dendrites
title_full_unstemmed Learning enhances behaviorally relevant representations in apical dendrites
title_short Learning enhances behaviorally relevant representations in apical dendrites
title_sort learning enhances behaviorally relevant representations in apical dendrites
topic apical dendrite
layer 1
learning
memory
plasticity
reward
url https://elifesciences.org/articles/98349
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AT citlaliperezcampos learningenhancesbehaviorallyrelevantrepresentationsinapicaldendrites
AT elizabethmchillman learningenhancesbehaviorallyrelevantrepresentationsinapicaldendrites
AT randymbruno learningenhancesbehaviorallyrelevantrepresentationsinapicaldendrites