Decreased interictal EEG slowing is consistent with increased multiple timescale neural adaptation

Human invasive EEG recordings are used to guide clinical decision-making for epilepsy patients and offer an opportunity to better understand underlying neurophysiology. However, the relationship between macroscale electrophysiological recordings and underlying neural networks mechanisms remain unclear. Lundstrom et al [1,2] have shown that interictal (between-seizure) 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 interictal power spectral densities (PSDs) with flattened slopes near the SOZ, which are areas of increased neural excitability. We hypothesized that these observations are consistent with changes in short-term plasticity, or adaptation, within the neural circuit. We used filter-based neural mass models and conductance-based models that incorporated short-term plasticity, including spike frequency adaptation and synaptic depression. We focused on multiple timescales of adaptation, which can approximate fractional dynamics, a form of calculus related to power laws and history dependence that is related to neural adaptation [3,4]. We found that when multiple timescale adaptation approximates fractional dynamics, PSDs retain a linear form with a decreased slope, similar to experimental findings. Coupled with input changes, short-term plasticity changed circuit responses in unexpected ways. For example, although increased input typically increases broadband power, 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 near the SOZ. Modeling supports increased multiple timescale adaptation as a reasonable explanation for decreased interictal EEG slowing near the SOZ. Changes in neural adaptation and short-term plasticity may be evident in macroscale electrophysiological recordings and provide a window to assessing and understanding neural circuit excitability.