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

Abstract

ABSTRACTSingle-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 SUvisualresponse fields coded targets (with some predicting Gaze), whereas the MU population only coded targets. Most SUmotorresponses 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.