Sustained stimulus-selective multi-unit activity in human primary visual cortex

Introduction: Neural activity related to visual working memory (WM) has been found in various cortical areas of primates and humans. However, the role of multi-unit activity in human V1 during WM tasks is not fully understood. We explored this by examining intracortical recordings from an awake blind human with a visual prosthesis (Utah array in parafoveal V1) during a delayed-response WM task. Methods: In 90 trials, one of three chosen electrodes stimulated a visual percept (phosphene) in the participant (stimulation period), who then had to remember its shape and location for 3 or 5 seconds (delay period), followed by an auditory cue and a recall period, during which the participant was asked to intently visualize the remembered phosphene. Neural activity was recorded and analyzed for multi-unit activity (MUA), entire spiking activity (ESA), and local field potential (LFP). Results: Significant differences in MUA, ESA, and LFP (theta, alpha, and beta bands) were observed across different trial periods (stimulation, delay, recall, and spontaneous; t-tests, p<.05). Each electrode's neural signature was distinct during delay and recall (over 90% accuracy in leave-one-trial-out cross-validation), with day-to-day drifts. The directions of maximum variability in the recall period neural activity formed a representative neural basis for each electrode, and enabled classification with a random forest classifier for both delay (97% accuracy) and stimulation period activities (88% accuracy). These shared signatures could be learned from the delay or recall period activity, but not from the electrically evoked activity, suggesting that WM elicits a subset of the full activity present during electrical stimulation. Conclusion: Our findings underscore V1's crucial role in retaining information at the neuronal level over delay periods. The transformation of representations during the recall period suggests that the encoded information is more abstract than the sensory activity evoked during stimulation.