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Cited by 177Neuroscience and Neuropharmacology ResearchNeural dynamics and brain functionMemory and Neural Mechanisms

High Bandwidth Synaptic Communication and Frequency Tracking in Human Neocortex

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Testa-Silva, Guilherme, Verhoog, Matthijs B., Linaro, Daniele, de Kock, Christiaan P. J., Baayen, Johannes C., Meredith, Rhiannon M., De Zeeuw, Chris I., Giugliano, Michele +1 more·2014·PLoS Biology
DOI 10.1371/journal.pbio.1002007PMC PMC4244038
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Abstract

Neuronal firing, synaptic transmission, and its plasticity form the building blocks for processing and storage of information in the brain. It is unknown whether adult human synapses are more efficient in transferring information between neurons than rodent synapses. To test this, we recorded from connected pairs of pyramidal neurons in acute brain slices of adult human and mouse temporal cortex and probed the dynamical properties of use-dependent plasticity. We found that human synaptic connections were purely depressing and that they recovered three to four times more swiftly from depression than synapses in rodent neocortex. Thereby, during realistic spike trains, the temporal resolution of synaptic information exchange in human synapses substantially surpasses that in mice. Using information theory, we calculate that information transfer between human pyramidal neurons exceeds that of mouse pyramidal neurons by four to nine times, well into the beta and gamma frequency range. In addition, we found that human principal cells tracked fine temporal features, conveyed in received synaptic inputs, at a wider bandwidth than for rodents. Action potential firing probability was reliably phase-locked to input transients up to 1,000 cycles/s because of a steep onset of action potentials in human pyramidal neurons during spike trains, unlike in rodent neurons. Our data show that, in contrast to the widely held views of limited information transfer in rodent depressing synapses, fast recovering synapses of human neurons can actually transfer substantial amounts of information during spike trains. In addition, human pyramidal neurons are equipped to encode high synaptic information content. Thus, adult human cortical microcircuits relay information at a wider bandwidth than rodent microcircuits.

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  • By 10 MPT, the neurons displayed sustained firing and mature-looking APs that closely resemble those of mature human pyramidal neurons.

    “By 10 MPT, the neurons displayed sustained firing and mature-looking APs that closely resemble those of mature human pyramidal neurons”

    From Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits (2019) · cites this paper as Testa-Silva et al., 2014

  • Transplanted human neurons integrating the mouse cortex display protracted physiological maturation over months, until 11 MPT, at which stage their properties resemble those of adult cortical neurons.

    “Thus, transplanted human neurons integrating the mouse cortex display protracted physiological maturation over months, until 11 MPT, at which stage their properties resemble those of adult cortical neurons”

    From Xenotransplanted human cortical neurons reveal species-specific development and functional integration into mouse visual circuits (2019) · cites this paper as Testa-Silva et al., 2014

    The Results and Discussion describe recordings from adult human cortical tissue and separate mouse cortical tissue, not human neurons transplanted into mice. Searches for transplanted neurons, months post-transplantation, and 11 MPT found no passage addressing their maturation or properties at that time point. (LLM, conf=0.76)

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Authors
Testa-Silva, G., Verhoog, M. B., Linaro, D., de Kock, C. P. J., Baayen, J. C., Meredith, R. M., De Zeeuw, C. I., Giugliano, M., & Mansvelder, H. D.
Affiliations
  • Netherlands Institute for Neuroscience (NL)
  • Vrije Universiteit Amsterdam (NL)
  • University of Antwerp (BE)
  • Amsterdam Neuroscience (NL)
Corresponding author
Mansvelder, Huibert D.
ORCID
Venue
PLoS Biology
Publisher
Public Library of Science (PLoS)
Published
2014-11-25
Volume
12
Issue
11
Pages
e1002007
ISSN
  • 1544-9173 (ISSN-L)
  • 1545-7885
DOI
10.1371/journal.pbio.1002007
PMC
PMC4244038
OpenAlex
W2095478325
Cited by
177
References
3
Citations by year
2026: 10 · 2025: 16 · 2024: 18 · 2023: 15 · 2022: 16 · 2021: 17 · 2020: 14 · 2019: 16 · 2018: 19 · 2017: 16 · 2016: 9 · 2015: 9 · 2014: 2
FWCI
5.49
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
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  • PubMed (publishedVersion)
  • Pure Amsterdam UMC (publishedVersion)
  • Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
  • KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
  • VU Research Portal (publishedVersion, other-oa)
  • SDL (submittedVersion, cc-by)
  • IRIS UNIMORE (University of Modena and Reggio Emilia) (submittedVersion, cc-by)
  • EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
  • Virtual Community of Pathological Anatomy (University of Castilla La Mancha) (submittedVersion, other-oa)
  • RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
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  • ANU Open Research (Australian National University) (submittedVersion, cc-by)
  • Data Archiving and Networked Services (DANS) (submittedVersion)
Funders
  • European Commission (264872, 306502, 242167)
  • Belgian Federal Science Policy Office (IUAP-VII/20)
  • Fonds Wetenschappelijk Onderzoek (G088812N)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (604102, 917.76.360, 912.06.148)
  • Vlaamse regering
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords
human neocortex, pyramidal neurons, synaptic depression, synaptic plasticity, use-dependent plasticity, synaptic recovery, temporal resolution, frequency tracking, phase locking, spike trains, information theory, temporal cortex, gamma oscillations, beta oscillations
MeSH terms
Adolescent, Adult, Animals, Humans, Mice, Inbred C57BL, Middle Aged, Synapses, Pyramidal Cells, Neocortex, Young Adult

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