Multiunit frontal eye field activity codes the visuomotor transformation, but not gaze prediction or target memory, in a delayed saccade task

Abstract

Single-unit (SU) activity [mdash] action potentials isolated from one neuron — has traditionally been employed to relate neuronal activity to behavior. However, recent investigations have shown that multi-unit (MU) activity — ensemble neural activity recorded within the vicinity of one microelectrode — may also contain accurate estimations of task-related neural population dynamics. Here, using a well-established model-fitting approach, we compared the spatial codes of SU response fields with corresponding MU response fields recorded from the frontal eye fields (FEF) in head-unrestrained monkeys (Macaca mulatta) during a memory-guided saccade task. We focused on characterizing the visuomotor transformation from Target-in-Eye coordinates to future Gaze-in-Eye coordinates (Sajad et al., 2015). Most SU visual response fields coded targets (with some predicting Gaze), whereas the MU population only coded targets. Most SU motor responses coded Gaze, but many still retained a target code. In contrast, MU motor activity predominantly coded Gaze with very little target coding. Finally, both SU and MU populations showed a progressive transition through intermediate 'Target-to-Gaze' codes during the delay period, but the MU activity showed a 'smoother' transition. These results confirm the theoretical and practical potential of MU activity recordings as a biomarker for fundamental sensorimotor transformations (e.g., Target-to-Gaze coding in the oculomotor system), while also highlighting the importance of SU activity for coding more cognitive (e.g., predictive / memory) aspects of sensorimotor behavior.