Morpho-electric diversity of human hippocampal CA1 pyramidal neurons
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
Affiliations
Eline J. Mertens
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Yoni Leibner
The Edmond and Lily Safra Center for Brain Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel
Jean Pie
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Anna A. Galakhova
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Femke Waleboer
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Julia Meijer
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Tim S. Heistek
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
René Wilbers
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Djai Heyer
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Natalia A. Goriounova
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Sander Idema
Amsterdam UMC, location VUmc, Amsterdam 1081 HV, the Netherlands
Matthijs B. Verhoog
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands
Brian E. Kalmbach
Allen Institute for Brain Science, Seattle, WA 98109, USA
Brian R. Lee
Allen Institute for Brain Science, Seattle, WA 98109, USA
Ryder P. Gwinn
Epilepsy Surgery and Functional Neurosurgery, Swedish Neuroscience Institute, Seattle, WA 98122, USA
Ed S. Lein
Allen Institute for Brain Science, Seattle, WA 98109, USA
Eleonora Aronica
Department of (Neuro)Pathology, Amsterdam Neuroscience, Amsterdam University Medical Centers, University of Amsterdam, 1105 AZ Amsterdam, the Netherlands
Jonathan Ting
Allen Institute for Brain Science, Seattle, WA 98109, USA
Huibert D. Mansvelder
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands; Corresponding author
Idan Segev
The Edmond and Lily Safra Center for Brain Sciences, The Hebrew University of Jerusalem, Jerusalem 91904, Israel; Corresponding author
Christiaan P.J. de Kock
Center for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, the Netherlands; Corresponding author
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.