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Cover ArticleResearch Articles, Systems/Circuits

Quantitative Fluorescence Analysis Reveals Dendrite-Specific Thalamocortical Plasticity in L5 Pyramidal Neurons during Learning

Ajit Ray, Joseph A. Christian, Matthew B. Mosso, Eunsol Park, Waja Wegner, Katrin I. Willig and Alison L. Barth
Journal of Neuroscience 25 January 2023, 43 (4) 584-600; DOI: https://doi.org/10.1523/JNEUROSCI.1372-22.2022
Ajit Ray
1Department of Biological Sciences, Carnegie Mellon University, Pittsburgh Pennsylvania 15213
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Joseph A. Christian
1Department of Biological Sciences, Carnegie Mellon University, Pittsburgh Pennsylvania 15213
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Matthew B. Mosso
1Department of Biological Sciences, Carnegie Mellon University, Pittsburgh Pennsylvania 15213
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Eunsol Park
1Department of Biological Sciences, Carnegie Mellon University, Pittsburgh Pennsylvania 15213
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Waja Wegner
2Optical Nanoscopy in Neuroscience, Center for Nanoscale Microscopy and Molecular Physiology of the Brain, University Medical Center Göttingen, 37099 Göttingen, Germany
3Max Planck Institute for Multidisciplinary Sciences, 37077 Göttingen, Germany
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Katrin I. Willig
2Optical Nanoscopy in Neuroscience, Center for Nanoscale Microscopy and Molecular Physiology of the Brain, University Medical Center Göttingen, 37099 Göttingen, Germany
3Max Planck Institute for Multidisciplinary Sciences, 37077 Göttingen, Germany
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Alison L. Barth
1Department of Biological Sciences, Carnegie Mellon University, Pittsburgh Pennsylvania 15213
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Abstract

High-throughput anatomic data can stimulate and constrain new hypotheses about how neural circuits change in response to experience. Here, we use fluorescence-based reagents for presynaptic and postsynaptic labeling to monitor changes in thalamocortical synapses onto different compartments of layer 5 (L5) pyramidal (Pyr) neurons in somatosensory (barrel) cortex from mixed-sex mice during whisker-dependent learning (Audette et al., 2019). Using axonal fills and molecular-genetic tags for synapse identification in fixed tissue from Rbp4-Cre transgenic mice, we found that thalamocortical synapses from the higher-order posterior medial thalamic nucleus showed rapid morphologic changes in both presynaptic and postsynaptic structures at the earliest stages of sensory association training. Detected increases in thalamocortical synaptic size were compartment specific, occurring selectively in the proximal dendrites onto L5 Pyr and not at inputs onto their apical tufts in L1. Both axonal and dendritic changes were transient, normalizing back to baseline as animals became expert in the task. Anatomical measurements were corroborated by electrophysiological recordings at different stages of training. Thus, fluorescence-based analysis of input- and target-specific synapses can reveal compartment-specific changes in synapse properties during learning.

SIGNIFICANCE STATEMENT Synaptic changes underlie the cellular basis of learning, experience, and neurologic diseases. Neuroanatomical methods to assess synaptic plasticity can provide critical spatial information necessary for building models of neuronal computations during learning and experience but are technically and fiscally intensive. Here, we describe a confocal fluorescence microscopy–based analytical method to assess input, cell type, and dendritic location-specific synaptic plasticity in a sensory learning assay. Our method not only confirms prior electrophysiological measurements but allows us to predict functional strength of synapses in a pathway-specific manner. Our findings also indicate that changes in primary sensory cortices are transient, occurring during early learning. Fluorescence-based synapse identification can be an efficient and easily adopted approach to study synaptic changes in a variety of experimental paradigms.

  • apical dendrite
  • intrabodies
  • learning
  • LTP
  • plasticity
  • POm thalamus

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The Journal of Neuroscience: 43 (4)
Journal of Neuroscience
Vol. 43, Issue 4
25 Jan 2023
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Quantitative Fluorescence Analysis Reveals Dendrite-Specific Thalamocortical Plasticity in L5 Pyramidal Neurons during Learning
Ajit Ray, Joseph A. Christian, Matthew B. Mosso, Eunsol Park, Waja Wegner, Katrin I. Willig, Alison L. Barth
Journal of Neuroscience 25 January 2023, 43 (4) 584-600; DOI: 10.1523/JNEUROSCI.1372-22.2022

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Quantitative Fluorescence Analysis Reveals Dendrite-Specific Thalamocortical Plasticity in L5 Pyramidal Neurons during Learning
Ajit Ray, Joseph A. Christian, Matthew B. Mosso, Eunsol Park, Waja Wegner, Katrin I. Willig, Alison L. Barth
Journal of Neuroscience 25 January 2023, 43 (4) 584-600; DOI: 10.1523/JNEUROSCI.1372-22.2022
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Keywords

  • apical dendrite
  • intrabodies
  • learning
  • LTP
  • plasticity
  • POm thalamus

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