Rapid Input-Output Transformation between Local Field Potential and Spiking Activity during Sensation But Not Action in the Superior Colliculus.

Sensorimotor transformation is the sequential process of registering a sensory signal in the environment and then responding with the relevant movement at an appropriate time. For visually-guided eye movements, neural signatures in the form of spiking activity of neurons have been extensively studied along the dorsoventral axis of the superior colliculus (SC). In contrast, the local field potential (LFP), which represents the putative input to a region, remains largely unexplored in the SC. We therefore compared amplitude levels and onset times of both spike bursts and LFP modulations recorded simultaneously with a laminar probe along the dorsoventral axis of SC in three male monkeys performing the visually-guided delayed saccade task. Both signals displayed a gradual transition from sensory activity in the superficial layers to a predominantly motor response in the deeper layers, although the transition from principally sensory to mostly motor response occurred ∼500 μm deeper for the LFP. For the sensory response, LFP modulation preceded spike burst onset by less than 5 ms in the superficial and intermediate layers and only when data were analyzed on a trial-by-trial basis. The motor burst in the spiking activity led LFP modulation by over 25 ms in the deeper layers. The results reveal a fast and efficient input-output transformation between LFP modulation and spike burst in the visually responsive layers activity during sensation but not during action. The spiking pattern observed during the movement phase is likely dominated by intracollicular processing that is not captured in the LFP. Significance Statement: What is the sequence of events between LFP modulation and spiking activity during sensorimotor transformation? A trial-by-trial analysis reveals that the LFP activity leads the spike burst in the superficial and intermediate layers of the superior colliculus during visual processing, while both trial-by-trial and the average analyses show that the spike burst leads the LFP modulation during movement generation. These results suggest an almost instantaneous LFP input, spike burst output transformation in the visually responsive layers of the SC when registering the stimulus. In contrast, substantial intracollicular processing likely results in a saccade-related spike burst that leads LFP modulation.