Large and fast human pyramidal neurons associate with intelligence

  1. Natalia A Goriounova  Is a corresponding author
  2. Djai B Heyer
  3. René Wilbers
  4. Matthijs B Verhoog
  5. Michele Giugliano
  6. Christophe Verbist
  7. Joshua Obermayer
  8. Amber Kerkhofs
  9. Harriët Smeding
  10. Maaike Verberne
  11. Sander Idema
  12. Johannes C Baayen
  13. Anton W Pieneman
  14. Christiaan PJ de Kock
  15. Martin Klein
  16. Huib D Mansvelder
  1. Vrije Universiteit Amsterdam, Netherlands
  2. University of Antwerp, Belgium
  3. Stichting Epilepsie Instellingen Nederland (SEIN), Netherlands
  4. VU Medical Center, Netherlands

Abstract

It is generally assumed that human intelligence relies on efficient processing by neurons in our brain. Although grey matter thickness and activity of temporal and frontal cortical areas correlate with IQ scores, no direct evidence exists that links structural and physiological properties of neurons to human intelligence. Here, we find that high IQ scores and large temporal cortical thickness associate with larger, more complex dendrites of human pyramidal neurons. We show in silico that larger dendritic trees enable pyramidal neurons to track activity of synaptic inputs with higher temporal precision, due to fast action potential kinetics. Indeed, we find that human pyramidal neurons of individuals with higher IQ scores sustain fast action potential kinetics during repeated firing. These findings provide the first evidence that human intelligence is associated with neuronal complexity, action potential kinetics and efficient information transfer from inputs to output within cortical neurons.

Data availability

Numerical data for fall figures are available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.83dv5j7 (doi number 10.5061/dryad.83dv5j7).All customized Matlab scripts used for physiological data analysis are available at https://github.com/INF-Rene/Morphys

The following data sets were generated

Article and author information

Author details

  1. Natalia A Goriounova

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    For correspondence
    n.a.goriounova@vu.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5917-983X
  2. Djai B Heyer

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. René Wilbers

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  4. Matthijs B Verhoog

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Michele Giugliano

    Molecular, Cellular, and Network Excitability Lab, Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2626-594X
  6. Christophe Verbist

    Molecular, Cellular, and Network Excitability Lab, Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium
    Competing interests
    The authors declare that no competing interests exist.
  7. Joshua Obermayer

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Amber Kerkhofs

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  9. Harriët Smeding

    Department of Psychology, Stichting Epilepsie Instellingen Nederland (SEIN), Heemstede, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  10. Maaike Verberne

    Department of Psychology, Stichting Epilepsie Instellingen Nederland (SEIN), Zwolle, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  11. Sander Idema

    Department of Neurosurgery, VU Medical Center, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  12. Johannes C Baayen

    Department of Neurosurgery, VU Medical Center, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  13. Anton W Pieneman

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  14. Christiaan PJ de Kock

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  15. Martin Klein

    Department of Medical Psychology, VU Medical Center, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  16. Huib D Mansvelder

    Department of Integrative Neurophysiology, Centre for Neurogenomics and Cognitive Research, Vrije Universiteit Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1365-5340

Funding

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (VENI grant)

  • Natalia A Goriounova

H2020 European Research Council (Human Brain Project)

  • Huib D Mansvelder

Fonds Wetenschappelijk Onderzoek (G0F1517N)

  • Michele Giugliano

Nederlandse Organisatie voor Wetenschappelijk Onderzoek (VICI grant)

  • Huib D Mansvelder

H2020 European Research Council (ERC StG)

  • Huib D Mansvelder

H2020 European Research Council (Human Brain Project)

  • Michele Giugliano

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: All procedures were performed with the approval of the Medical Ethical Committee of the VU University Medical Centre (2012/362), and in accordance with Dutch license procedures and the Declaration of Helsinki. Written informed consent was provided by all subjects for data and tissue use for scientific research. All data were anonymized.

Reviewing Editor

  1. David Badre, Brown University, United States

Publication history

  1. Received: September 5, 2018
  2. Accepted: December 17, 2018
  3. Accepted Manuscript published: December 18, 2018 (version 1)
  4. Version of Record published: February 5, 2019 (version 2)

Copyright

© 2018, Goriounova et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Natalia A Goriounova
  2. Djai B Heyer
  3. René Wilbers
  4. Matthijs B Verhoog
  5. Michele Giugliano
  6. Christophe Verbist
  7. Joshua Obermayer
  8. Amber Kerkhofs
  9. Harriët Smeding
  10. Maaike Verberne
  11. Sander Idema
  12. Johannes C Baayen
  13. Anton W Pieneman
  14. Christiaan PJ de Kock
  15. Martin Klein
  16. Huib D Mansvelder
(2018)
Large and fast human pyramidal neurons associate with intelligence
eLife 7:e41714.
https://doi.org/10.7554/eLife.41714
  1. Further reading

Further reading

  1. Larger neurons seem to lead to higher IQs.

    1. Neuroscience
    Frédéric Roux, George Parish ... Simon Hanslmayr
    Research Article Updated

    Theta and gamma oscillations in the medial temporal lobe are suggested to play a critical role for human memory formation via establishing synchrony in neural assemblies. Arguably, such synchrony facilitates efficient information transfer between neurons and enhances synaptic plasticity, both of which benefit episodic memory formation. However, to date little evidence exists from humans that would provide direct evidence for such a specific role of theta and gamma oscillations for episodic memory formation. Here, we investigate how oscillations shape the temporal structure of neural firing during memory formation in the medial temporal lobe. We measured neural firing and local field potentials in human epilepsy patients via micro-wire electrode recordings to analyze whether brain oscillations are related to co-incidences of firing between neurons during successful and unsuccessful encoding of episodic memories. The results show that phase-coupling of neurons to faster theta and gamma oscillations correlates with co-firing at short latencies (~20–30 ms) and occurs during successful memory formation. Phase-coupling at slower oscillations in these same frequency bands, in contrast, correlates with longer co-firing latencies and occurs during memory failure. Thus, our findings suggest that neural oscillations play a role for the synchronization of neural firing in the medial temporal lobe during the encoding of episodic memories.