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Non-invasive single-trial EEG detection of evoked human neocortical population spikes

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Citation

Waterstraat, G., Burghoff, M., Fedele, T., Nikulin, V. V., Scheer, H. J., & Curio, G. (2015). Non-invasive single-trial EEG detection of evoked human neocortical population spikes. NeuroImage, 105, 13-20. doi:10.1016/j.neuroimage.2014.10.024.


Cite as: https://hdl.handle.net/11858/00-001M-0000-002D-3C1C-8
Abstract
Question

Human high-frequency (> 400 Hz) components of somatosensory evoked potentials (hf-SEPs), which can be recorded non-invasively at the scalp, are generated by cortical population spikes, as inferred from microelectrode recordings in non-human primates. It is a critical limitation to broader neurophysiological study of hf-SEPs in that hundreds of responses have to be averaged to detect hf-SEPs reliably. Here, we establish a framework for detecting human hf-SEPs non-invasively in single trials.
Methods

Spatio-temporal features were extracted from band-pass filtered (400-900 Hz) hf-SEPs by bilinear Common Spatio-Temporal Patterns (bCSTP) and then classified by a weighted Extreme Learning Machine (w-ELM). The effect of varying signal-to-noise ratio (SNR), number of trials, and degree of w-ELM re-weighting was characterized using surrogate data. For practical demonstration of the algorithm, median nerve hf-SEPs were recorded inside a shielded room in four subjects, spanning the hf-SEP signal-to-noise ratio characteristic for a larger population, utilizing a custom-built 29-channel low-noise EEG amplifier.
Results

Using surrogate data, the SNR proved to be pivotal to detect hf-SEPs in single trials efficiently, with the trade-off between sensitivity and specificity of the algorithm being obtained by the w-ELM re-weighting parameter. In practice, human hf-SEPs were detected non-invasively in single trials with a sensitivity of up to 99% and a specificity of up to 97% in two subjects, even without any recourse to knowledge of stimulus timing. Matching with the results of the surrogate data analysis, these rates dropped to 62–79% sensitivity and 18–31% specificity in two subjects with lower SNR.
Conclusions

Otherwise buried in background noise, human high-frequency EEG components can be extracted from low-noise recordings. Specifically, refined supervised filter optimization and classification enables the reliable detection of single-trial hf-SEPs, representing non-invasive correlates of cortical population spikes.
Significance

While low-frequency EEG reflects summed postsynaptic potentials, and thereby neuronal input, we suggest that high-frequency EEG (> 400 Hz) can provide non-invasive access to the unaveraged output of neuronal computation, i.e., single-trial population spike activity evoked in the responsive neuronal ensemble.