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.

Index fileList and description of all files and foldersindex.xlsx30Hz_EPSPsAll EPSPs used as examples on figures 1 and S1 and where all EPSP parameteres have been calculated from.Code_Fig3_and_SFig2Matlab code used to generate our model based panels.Figure 1ANeurolucida reconstructed pair of synaptically connected human pyramidal cells.Poisson_Humanraw traces used in the average trace displayed in Figure 3B.Poisson_Mouseraw traces used in the average trace displayed in Figure 3A.Data_Fig5_and_SFig4Raw data used to produce Figure 5 and Figure S4.Data S1Excel sheet with numbers displayed in Figures 1C, 1D, 1E and S1A, S1B, S1C and S1D.Data S2Excel sheet with numbers displayed in Figure 2.Data S3Excel sheet with numbers displayed in Figures 5 and S4.Data_Fig4_and_SFig3_HumanRaw data used to produce Figure 4 and Figure S3 (Human dataset)Data_Fig4_and_SFig3_Mouse_Part1Raw data used to produce Figure 4 and Figure S3 (Mouse dataset part 1)Data_Fig4_and_SFig3_Mouse_Part2Raw data used to produce Figure 4 and Figure S3 (Mouse dataset part 2)Data_Fig4_and_SFig3_Mouse_Part3Raw data used to produce Figure 4 and Figure S3 (Mouse dataset part 3)Data_Fig4_and_SFig3_Mouse_Part4Raw data used to produce Figure 4 and Figure S3 (Mouse dataset part 4)