Columnar Localization and Laminar Origin of Cortical Surface Electrical Potentials.

Electrocorticography (ECoG) methodologically bridges basic neuroscience and understanding of human brains in health and disease. However, the localization of ECoG signals across the surface of the brain and the spatial distribution of their generating neuronal sources are poorly understood. To address this gap, we recorded from rat auditory cortex using customized µECoG, and simulated cortical surface electrical potentials with a full-scale, biophysically detailed cortical column model. Experimentally, µECoG-derived auditory representations were tonotopically organized and signals were anisotropically localized to less than or equal to ±200 µm, that is, a single cortical column. Biophysical simulations reproduce experimental findings and indicate that neurons in cortical layers V and VI contribute ∼85% of evoked high-gamma signal recorded at the surface. Cell number and synchrony were the primary biophysical properties determining laminar contributions to evoked µECoG signals, whereas distance was only a minimal factor. Thus, evoked µECoG signals primarily originate from neurons in the infragranular layers of a single cortical column.SIGNIFICANCE STATEMENT ECoG methodologically bridges basic neuroscience and understanding of human brains in health and disease. However, the localization of ECoG signals across the surface of the brain and the spatial distribution of their generating neuronal sources are poorly understood. We investigated the localization and origins of sensory-evoked ECoG responses. We experimentally found that ECoG responses were anisotropically localized to a cortical column. Biophysically detailed simulations revealed that neurons in layers V and VI were the primary sources of evoked ECoG responses. These results indicate that evoked ECoG high-gamma responses are primarily generated by the population spike rate of pyramidal neurons in layers V and VI of single cortical columns and highlight the possibility of understanding how microscopic sources produce mesoscale signals.

Laminar origin of evoked ECoG high-gamma activity.

High-gamma (Hγ) activity from electrocorticography (ECoG) is a common-used signal for understanding the human brain, but its interpretation is impeded by a lack of spatial localization. To address this, we developed a novel recording approach to simultaneously record µECoG cortical surface electrical potentials (CSEPs) and laminar multiunit activity (MUA). We demonstrate that stimulus evoked CSEPs carry a multi-modal frequency response, peaking in the Hγ range. Laminar MUA responses exhibited similar tuning to CSEP Hγ directly over the intracortical recording site, suggesting a functional relationship. We fit CSEP Hγ to the simultaneously-recorded laminar MUA using a state-of-the-art sparse multi-linear regression model to identify laminar contributions to cortical surface Hγ. Our results indicate that CSEP Hγ recorded by ECoG reflects spiking activity from neurons in layer 3. These results provide initial insight into localizing the sources of CSEPs, which will guide clinical and BMI device decisions.