Translating single-neuron axonal reconstructions into meso-scale connectivity statistics in the mouse somatosensory thalamus

Characterizing the connectomic and morphological diversity of thalamic neurons is key for better understanding how the thalamus relays sensory inputs to the cortex. The recent public release of complete single-neuron morphological reconstructions enables the analysis of previously inaccessible conne...

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Main Authors: Nestor Timonidis, Rembrandt Bakker, Mario Rubio-Teves, Carmen Alonso-Martínez, Maria Garcia-Amado, Francisco Clascá, Paul H. E. Tiesinga
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-12-01
Series:Frontiers in Neuroinformatics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fninf.2023.1272243/full
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author Nestor Timonidis
Rembrandt Bakker
Rembrandt Bakker
Mario Rubio-Teves
Carmen Alonso-Martínez
Maria Garcia-Amado
Francisco Clascá
Paul H. E. Tiesinga
author_facet Nestor Timonidis
Rembrandt Bakker
Rembrandt Bakker
Mario Rubio-Teves
Carmen Alonso-Martínez
Maria Garcia-Amado
Francisco Clascá
Paul H. E. Tiesinga
author_sort Nestor Timonidis
collection DOAJ
description Characterizing the connectomic and morphological diversity of thalamic neurons is key for better understanding how the thalamus relays sensory inputs to the cortex. The recent public release of complete single-neuron morphological reconstructions enables the analysis of previously inaccessible connectivity patterns from individual neurons. Here we focus on the Ventral Posteromedial (VPM) nucleus and characterize the full diversity of 257 VPM neurons, obtained by combining data from the MouseLight and Braintell projects. Neurons were clustered according to their most dominantly targeted cortical area and further subdivided by their jointly targeted areas. We obtained a 2D embedding of morphological diversity using the dissimilarity between all pairs of axonal trees. The curved shape of the embedding allowed us to characterize neurons by a 1-dimensional coordinate. The coordinate values were aligned both with the progression of soma position along the dorsal-ventral and lateral-medial axes and with that of axonal terminals along the posterior-anterior and medial-lateral axes, as well as with an increase in the number of branching points, distance from soma and branching width. Taken together, we have developed a novel workflow for linking three challenging aspects of connectomics, namely the topography, higher order connectivity patterns and morphological diversity, with VPM as a test-case. The workflow is linked to a unified access portal that contains the morphologies and integrated with 2D cortical flatmap and subcortical visualization tools. The workflow and resulting processed data have been made available in Python, and can thus be used for modeling and experimentally validating new hypotheses on thalamocortical connectivity.
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spelling doaj.art-3d49a4ae94d14baca474d3064f924d412023-12-01T14:23:07ZengFrontiers Media S.A.Frontiers in Neuroinformatics1662-51962023-12-011710.3389/fninf.2023.12722431272243Translating single-neuron axonal reconstructions into meso-scale connectivity statistics in the mouse somatosensory thalamusNestor Timonidis0Rembrandt Bakker1Rembrandt Bakker2Mario Rubio-Teves3Carmen Alonso-Martínez4Maria Garcia-Amado5Francisco Clascá6Paul H. E. Tiesinga7Neuroinformatics Department, Donders Centre for Neuroscience, Radboud University Nijmegen, Nijmegen, NetherlandsNeuroinformatics Department, Donders Centre for Neuroscience, Radboud University Nijmegen, Nijmegen, NetherlandsInstitute of Neuroscience and Medicine (INM-6) and Institute for Advanced Simulation (IAS-6) and JARA BRAIN Institute I, Jülich Research Centre, Jülich, GermanyDepartment of Anatomy and Neuroscience, School of Medicine, Autónoma de Madrid University, Madrid, SpainDepartment of Anatomy and Neuroscience, School of Medicine, Autónoma de Madrid University, Madrid, SpainDepartment of Anatomy and Neuroscience, School of Medicine, Autónoma de Madrid University, Madrid, SpainInstitute of Neuroscience and Medicine (INM-6) and Institute for Advanced Simulation (IAS-6) and JARA BRAIN Institute I, Jülich Research Centre, Jülich, GermanyNeuroinformatics Department, Donders Centre for Neuroscience, Radboud University Nijmegen, Nijmegen, NetherlandsCharacterizing the connectomic and morphological diversity of thalamic neurons is key for better understanding how the thalamus relays sensory inputs to the cortex. The recent public release of complete single-neuron morphological reconstructions enables the analysis of previously inaccessible connectivity patterns from individual neurons. Here we focus on the Ventral Posteromedial (VPM) nucleus and characterize the full diversity of 257 VPM neurons, obtained by combining data from the MouseLight and Braintell projects. Neurons were clustered according to their most dominantly targeted cortical area and further subdivided by their jointly targeted areas. We obtained a 2D embedding of morphological diversity using the dissimilarity between all pairs of axonal trees. The curved shape of the embedding allowed us to characterize neurons by a 1-dimensional coordinate. The coordinate values were aligned both with the progression of soma position along the dorsal-ventral and lateral-medial axes and with that of axonal terminals along the posterior-anterior and medial-lateral axes, as well as with an increase in the number of branching points, distance from soma and branching width. Taken together, we have developed a novel workflow for linking three challenging aspects of connectomics, namely the topography, higher order connectivity patterns and morphological diversity, with VPM as a test-case. The workflow is linked to a unified access portal that contains the morphologies and integrated with 2D cortical flatmap and subcortical visualization tools. The workflow and resulting processed data have been made available in Python, and can thus be used for modeling and experimentally validating new hypotheses on thalamocortical connectivity.https://www.frontiersin.org/articles/10.3389/fninf.2023.1272243/fullsingle-cell morphologyVPMsomatosensory cortextopographyconnectomicsCoherent Point Drift
spellingShingle Nestor Timonidis
Rembrandt Bakker
Rembrandt Bakker
Mario Rubio-Teves
Carmen Alonso-Martínez
Maria Garcia-Amado
Francisco Clascá
Paul H. E. Tiesinga
Translating single-neuron axonal reconstructions into meso-scale connectivity statistics in the mouse somatosensory thalamus
Frontiers in Neuroinformatics
single-cell morphology
VPM
somatosensory cortex
topography
connectomics
Coherent Point Drift
title Translating single-neuron axonal reconstructions into meso-scale connectivity statistics in the mouse somatosensory thalamus
title_full Translating single-neuron axonal reconstructions into meso-scale connectivity statistics in the mouse somatosensory thalamus
title_fullStr Translating single-neuron axonal reconstructions into meso-scale connectivity statistics in the mouse somatosensory thalamus
title_full_unstemmed Translating single-neuron axonal reconstructions into meso-scale connectivity statistics in the mouse somatosensory thalamus
title_short Translating single-neuron axonal reconstructions into meso-scale connectivity statistics in the mouse somatosensory thalamus
title_sort translating single neuron axonal reconstructions into meso scale connectivity statistics in the mouse somatosensory thalamus
topic single-cell morphology
VPM
somatosensory cortex
topography
connectomics
Coherent Point Drift
url https://www.frontiersin.org/articles/10.3389/fninf.2023.1272243/full
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