Morpho-electric diversity of human hippocampal CA1 pyramidal neurons

Summary: Hippocampal pyramidal neuron activity underlies episodic memory and spatial navigation. Although extensively studied in rodents, extremely little is known about human hippocampal pyramidal neurons, even though the human hippocampus underwent strong evolutionary reorganization and shows lowe...

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Main Authors: Eline J. Mertens, Yoni Leibner, Jean Pie, Anna A. Galakhova, Femke Waleboer, Julia Meijer, Tim S. Heistek, René Wilbers, Djai Heyer, Natalia A. Goriounova, Sander Idema, Matthijs B. Verhoog, Brian E. Kalmbach, Brian R. Lee, Ryder P. Gwinn, Ed S. Lein, Eleonora Aronica, Jonathan Ting, Huibert D. Mansvelder, Idan Segev, Christiaan P.J. de Kock
Format: Article
Language:English
Published: Elsevier 2024-04-01
Series:Cell Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124724004285
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author Eline J. Mertens
Yoni Leibner
Jean Pie
Anna A. Galakhova
Femke Waleboer
Julia Meijer
Tim S. Heistek
René Wilbers
Djai Heyer
Natalia A. Goriounova
Sander Idema
Matthijs B. Verhoog
Brian E. Kalmbach
Brian R. Lee
Ryder P. Gwinn
Ed S. Lein
Eleonora Aronica
Jonathan Ting
Huibert D. Mansvelder
Idan Segev
Christiaan P.J. de Kock
author_facet Eline J. Mertens
Yoni Leibner
Jean Pie
Anna A. Galakhova
Femke Waleboer
Julia Meijer
Tim S. Heistek
René Wilbers
Djai Heyer
Natalia A. Goriounova
Sander Idema
Matthijs B. Verhoog
Brian E. Kalmbach
Brian R. Lee
Ryder P. Gwinn
Ed S. Lein
Eleonora Aronica
Jonathan Ting
Huibert D. Mansvelder
Idan Segev
Christiaan P.J. de Kock
author_sort Eline J. Mertens
collection DOAJ
description Summary: Hippocampal pyramidal neuron activity underlies episodic memory and spatial navigation. Although extensively studied in rodents, extremely little is known about human hippocampal pyramidal neurons, even though the human hippocampus underwent strong evolutionary reorganization and shows lower theta rhythm frequencies. To test whether biophysical properties of human Cornu Amonis subfield 1 (CA1) pyramidal neurons can explain observed rhythms, we map the morpho-electric properties of individual CA1 pyramidal neurons in human, non-pathological hippocampal slices from neurosurgery. Human CA1 pyramidal neurons have much larger dendritic trees than mouse CA1 pyramidal neurons, have a large number of oblique dendrites, and resonate at 2.9 Hz, optimally tuned to human theta frequencies. Morphological and biophysical properties suggest cellular diversity along a multidimensional gradient rather than discrete clustering. Across the population, dendritic architecture and a large number of oblique dendrites consistently boost memory capacity in human CA1 pyramidal neurons by an order of magnitude compared to mouse CA1 pyramidal neurons.
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spelling doaj.art-371ff7956af64d3bbda89f13ea9ec9652024-04-12T04:45:07ZengElsevierCell Reports2211-12472024-04-01434114100Morpho-electric diversity of human hippocampal CA1 pyramidal neuronsEline J. Mertens0Yoni Leibner1Jean Pie2Anna A. Galakhova3Femke Waleboer4Julia Meijer5Tim S. Heistek6René Wilbers7Djai Heyer8Natalia A. Goriounova9Sander Idema10Matthijs B. Verhoog11Brian E. Kalmbach12Brian R. Lee13Ryder P. Gwinn14Ed S. Lein15Eleonora Aronica16Jonathan Ting17Huibert D. Mansvelder18Idan Segev19Christiaan P.J. de Kock20Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsThe Edmond and Lily Safra Center for Brain Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, IsraelCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsAmsterdam UMC, location VUmc, Amsterdam 1081 HV, the NetherlandsCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the NetherlandsAllen Institute for Brain Science, Seattle, WA 98109, USAAllen Institute for Brain Science, Seattle, WA 98109, USAEpilepsy Surgery and Functional Neurosurgery, Swedish Neuroscience Institute, Seattle, WA 98122, USAAllen Institute for Brain Science, Seattle, WA 98109, USADepartment of (Neuro)Pathology, Amsterdam Neuroscience, Amsterdam University Medical Centers, University of Amsterdam, 1105 AZ Amsterdam, the NetherlandsAllen Institute for Brain Science, Seattle, WA 98109, USACenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands; Corresponding authorThe Edmond and Lily Safra Center for Brain Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel; Corresponding authorCenter for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands; Corresponding authorSummary: Hippocampal pyramidal neuron activity underlies episodic memory and spatial navigation. Although extensively studied in rodents, extremely little is known about human hippocampal pyramidal neurons, even though the human hippocampus underwent strong evolutionary reorganization and shows lower theta rhythm frequencies. To test whether biophysical properties of human Cornu Amonis subfield 1 (CA1) pyramidal neurons can explain observed rhythms, we map the morpho-electric properties of individual CA1 pyramidal neurons in human, non-pathological hippocampal slices from neurosurgery. Human CA1 pyramidal neurons have much larger dendritic trees than mouse CA1 pyramidal neurons, have a large number of oblique dendrites, and resonate at 2.9 Hz, optimally tuned to human theta frequencies. Morphological and biophysical properties suggest cellular diversity along a multidimensional gradient rather than discrete clustering. Across the population, dendritic architecture and a large number of oblique dendrites consistently boost memory capacity in human CA1 pyramidal neurons by an order of magnitude compared to mouse CA1 pyramidal neurons.http://www.sciencedirect.com/science/article/pii/S2211124724004285CP: NeuroscienceCP: Cell biology
spellingShingle Eline J. Mertens
Yoni Leibner
Jean Pie
Anna A. Galakhova
Femke Waleboer
Julia Meijer
Tim S. Heistek
René Wilbers
Djai Heyer
Natalia A. Goriounova
Sander Idema
Matthijs B. Verhoog
Brian E. Kalmbach
Brian R. Lee
Ryder P. Gwinn
Ed S. Lein
Eleonora Aronica
Jonathan Ting
Huibert D. Mansvelder
Idan Segev
Christiaan P.J. de Kock
Morpho-electric diversity of human hippocampal CA1 pyramidal neurons
Cell Reports
CP: Neuroscience
CP: Cell biology
title Morpho-electric diversity of human hippocampal CA1 pyramidal neurons
title_full Morpho-electric diversity of human hippocampal CA1 pyramidal neurons
title_fullStr Morpho-electric diversity of human hippocampal CA1 pyramidal neurons
title_full_unstemmed Morpho-electric diversity of human hippocampal CA1 pyramidal neurons
title_short Morpho-electric diversity of human hippocampal CA1 pyramidal neurons
title_sort morpho electric diversity of human hippocampal ca1 pyramidal neurons
topic CP: Neuroscience
CP: Cell biology
url http://www.sciencedirect.com/science/article/pii/S2211124724004285
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