Spatiotemporal dynamics of direct cortical response depression during spreading depolarizations

Spreading depolarizations (SDs) induce a transient depression of cortical activity, including a depression of direct cortical responses (DCRs). Here, we examined the spatiotemporal dynamics of DCR depression during SDs induced by high-potassium or pinprick, using ECoG arrays and intracortical silicon probes in the anesthetized rat cortex. While SDs consistently suppressed DCRs, somatosensory-evoked responses, and spontaneous activity, the spatiotemporal pattern of DCR depression specifically depended on the direction of SD propagation relative to the stimulation and recording sites. When the SD wave first invaded the stimulation site, it triggered a simultaneous, “blanket” inhibition of DCRs across all recording sites of the ECoG array, preceding the local DC shift and suppression of spontaneous and sensory-evoked activity. Conversely, when the SD first invaded the recording sites of the ECoG array, DCR depression followed a sequential, “wave-like” pattern with a concomitant DC shift, and depression of local activity. Comparing the DCR onset and offset times across the ECoG array with the SD-related DC shifts, we found that the spatiotemporal organization of DCR depression provides reliable estimates of SD propagation direction, and the algorithm proposed here could be useful for both SD detection and propagation direction assessment during multisite ECoG recordings.