Neural adaptation and fractional dynamics as a window to underlying neural excitability

The relationship between macroscale electrophysiological recordings and the dynamics of underlying neural activity remains unclear. We have previously shown that low frequency EEG activity (<1 Hz) is decreased at the seizure onset zone (SOZ), while higher frequency activity (1-50 Hz) is increased. These changes result in power spectral densities (PSDs) with flattened slopes near the SOZ, which are assumed to be areas of increased excitability. We wanted to understand possible mechanisms underlying PSD changes in brain regions of increased excitability. We hypothesized that these observations are consistent with changes in adaptation within the neural circuit. We developed a theoretical framework and tested the effect of adaptation mechanisms, such as spike frequency adaptation and synaptic depression, on excitability and PSDs using filter-based neural mass models and conductance-based models. We compared the contribution of single timescale adaptation and multiple timescale adaptation. We found that adaptation with multiple timescales alters the PSDs. Multiple timescales of adaptation can approximate fractional dynamics, a form of calculus related to power laws, history dependence, and non-integer order derivatives. Coupled with input changes, these dynamics changed circuit responses in unexpected ways. Increased input without synaptic depression increases broadband power. However, increased input with synaptic depression may decrease power. The effects of adaptation were most pronounced for low frequency activity (< 1Hz). Increased input combined with a loss of adaptation yielded reduced low frequency activity and increased higher frequency activity, consistent with clinical EEG observations from SOZs. Spike frequency adaptation and synaptic depression, two forms of multiple timescale adaptation, affect low frequency EEG and the slope of PSDs. These neural mechanisms may underlie changes in EEG activity near the SOZ and relate to neural hyperexcitability. Neural adaptation may be evident in macroscale electrophysiological recordings and provide a window to understanding neural circuit excitability.