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 - 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. SIGNIFICANCE STATEMENTMulti-unit recordings (undifferentiated signals from several neurons) are relatively easy to record and provide a simplified estimate of neural dynamics, but it is not clear which single-unit signals are retained, amplified, or lost. Here, we compared single-/multi-unit activity from a well-defined structure (the frontal eye fields) and behavior (memory-delay saccade task), tracking their spatial codes through time. The progressive transformation from target to gaze coding observed in single-unit activity was retained in multi-unit activity, but gaze prediction (in the visual response) and target memory (in the motor response) were lost. This suggests that multi-unit activity provides an excellent biomarker for healthy sensorimotor transformations, at the cost of missing more subtle cognitive signals.