High Bandwidth Synaptic Communication and Frequency Tracking in Human Neocortex

PLoS Biol. 2014 Nov 25;12(11):e1002007. doi: 10.1371/journal.pbio.1002007. eCollection 2014 Nov.

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.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Humans
  • Mice, Inbred C57BL
  • Middle Aged
  • Neocortex / physiology*
  • Pyramidal Cells / physiology*
  • Synapses / physiology*
  • Young Adult

Associated data

  • Dryad/10.5061/dryad.3723P

Grant support

HDM received funding for this work from the Netherlands Organization for Scientific Research (NWO; 917.76.360, 912.06.148 and a VICI grant), ERC StG ‘BrainSignals’, the Dutch Fund for Economic Structure Reinforcement (FES, 0908 “NeuroBasic PharmaPhenomics project”), EU 7th Framework Programmes (HEALTH-F2-2009-242167 ‘SynSys’ and grant agreement no. 604102 ‘Human Brain Project’). MG received funding from the EC-FP7 (Marie Curie Network “NAMASEN”, grant n. 264872, ICT-FET project “BRAINLEAP”, grant n. 306502, Research Foundation Flanders, grants n. G.0888.12N and 12C9112N, and the Belgian Science Policy Office [grant n. IUAP-VII/20]). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.