Small neuronal ensembles of primate lateral prefrontal cortex encode spatial working memory in two reference frames

Abstract

Single neurons in the primate lateral prefrontal cortex (LPFC) encode spatial information during working memory (WM). However, it is poorly understood whether ensembles of neurons of a certain size can encode memorized locations based on different frames of reference during spatial WM. We trained two rhesus monkeys on a modified version of the oculomotor delayed-response task. For each trial, animals fixated a dot displayed at one of sixteen different positions on the screen and a target transiently appeared for 1000ms. Animals maintained fixation for another 1000ms and upon extinction of the fixation dot they made a saccade to the remembered target location to obtain a reward. Such task design allowed us to analyze the data for remembered locations relative to the fixation dot (retinotopic frame), and relative to the target location (spatio-centered frame). We recorded the extra-cellular unitary/multi-unitary activity by implanting multi-electrode arrays in the dorso-lateral (dLPFC) and ventro-lateral (vLPFC) prefrontal cortices. We grouped trials by quadrants within each reference frame (RF), computed the average firing rate during the WM delay for each unit, and determined their spatial selectivity (Mutual information test). We then constructed neuronal ensembles of different sizes (n=1,…50) and trained linear classifiers to decode the visual quadrant that included the memorized cue position from each ensemble size, and across 20 decoding iterations. We found that ensembles of dLPFC and vLPFC cells yielded decoding accuracies of 69% and 79% in the retinotopic RF, respectively, and 55% and 52% in the spatiotopic RF. Interestingly, the classifiers frequently based their performance on spatially selective units for the smaller ensemble sizes (n <= 5), and gradually reduce this proportion as the size of ensembles increased (n >= 6). Neuronal ensembles of small size in the LFPC could encode locations during spatial WM in the retinotopic and spatiotopic reference frames