title: High bandwidth synaptic communication and frequency tracking in human neocortex.
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.
authors.affiliation: Department of Integrative Neurophysiology, CNCR, VU University Amsterdam, The Netherlands; Department of Neuroscience, Erasmus Medical Center, Rotterdam, The Netherlands; Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences (KNAW), Amsterdam, The Netherlands.
authors.forename: Guilherme
authors.initials: G
authors.lastname: Testa-Silva
authors.affiliation: Department of Integrative Neurophysiology, CNCR, VU University Amsterdam, The Netherlands.
authors.forename: Matthijs B
authors.initials: MB
authors.lastname: Verhoog
authors.affiliation: Department of Biomedical Sciences, University of Antwerp, Belgium.
authors.forename: Daniele
authors.initials: D
authors.lastname: Linaro
authors.affiliation: Department of Integrative Neurophysiology, CNCR, VU University Amsterdam, The Netherlands.
authors.forename: Christiaan P J
authors.initials: CP
authors.lastname: de Kock
authors.affiliation: Department of Neurosurgery, VU University Medical Center, Neuroscience Campus, Amsterdam, The Netherlands.
authors.forename: Johannes C
authors.initials: JC
authors.lastname: Baayen
authors.affiliation: Department of Integrative Neurophysiology, CNCR, VU University Amsterdam, The Netherlands.
authors.forename: Rhiannon M
authors.initials: RM
authors.lastname: Meredith
authors.affiliation: Department of Neuroscience, Erasmus Medical Center, Rotterdam, The Netherlands; Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences (KNAW), Amsterdam, The Netherlands.
authors.forename: Chris I
authors.initials: CI
authors.lastname: De Zeeuw
authors.affiliation: Department of Biomedical Sciences, University of Antwerp, Belgium; Department of Computer Science, University of Sheffield, United Kingdom; Brain Mind Institute, Swiss Federal Institute of Technology of Lausanne, Switzerland.
authors.forename: Michele
authors.initials: M
authors.lastname: Giugliano
authors.affiliation: Department of Integrative Neurophysiology, CNCR, VU University Amsterdam, The Netherlands.
authors.forename: Huibert D
authors.initials: HD
authors.lastname: Mansvelder
mesh_terms: D000293:Adolescent; D000328:Adult; D000818:Animals; D006801:Humans; D008810:Mice, Inbred C57BL; D008875:Middle Aged; D019579:Neocortex / Q000502:physiology*; D017966:Pyramidal Cells / Q000502:physiology*; D013569:Synapses / Q000502:physiology*; D055815:Young Adult