Jacob Granley¹ (), Lily M. Turkstra¹, Galen Pogoncheff¹, Fabrizio Grani², Leili Soo², Alfonso Rodil², Cristina Soto², Thomas C. Sprague¹, Eduardo Fernandez², Michael Beyeler¹; ¹University of California, Santa Barbara, ²University of Miguel Hernandez, Elche, Spain

Neural activity in early visual cortex (EVC) is known to contribute to visual working memory (WM) and mental imagery (MI), but the role of spiking activity in humans remains unclear. This study investigates computational techniques for extracting spiking activity and their ability to reveal correlates of WM and MI. Intracortical recordings were collected from two awake blind humans implanted with a 96-channel visual prosthesis in EVC during a delayed-match-to-sample (DMTS) WM task and a MI visualization task. In 465 trials of the WM task, participants encoded visual perceptions (phosphenes) elicited by stimulation of one of three electrodes, maintained them over a 5-second delay, and recalled whether a subsequent phosphene was the same or different. The MI task followed a similar structure, with recall replaced by vivid mental visualization. Neural activity during stimulation, delay, recall, and spontaneous periods was analyzed using methods to extract multi-unit activity (MUA), entire spiking activity (ESA), and local field potential (LFP) signals. Significant differences were observed in MUA, ESA, and LFP (theta, alpha, and beta bands) across trial periods (t-tests, p < 0.05). ESA and MUA exhibited electrode-specific neural signatures during delay and recall periods, with over 90% classification accuracy in leave-one-trial-out cross-validation (LOOCV). Stimulus-specific ESA changes remained decodable throughout delay and recall (random forest classifier sliding window, LOOCV, 70% of windows above chance), indicating sustained stimulus-selective activity for both tasks despite day-to-day variability. These findings reveal sustained stimulus-selective spiking activity in human EVC during WM and MI tasks, underscoring its critical role in retaining and recalling information and providing new insights into the neural mechanisms underlying perception and cognition.

Acknowledgements: NIH DP2-LM014268 to MB; Alfred P. Sloan Foundation Research Fellowship to TCS; PDC2022-133952-100, PID2022-141606OB-I00 from the Spanish Ministerio de Ciencia, Innovación y Universidades, Grant No. 899287 (NeuraViPeR) from European Union’s Horizon 2020 Research and Innovation Programme to EFJ.