Instantaneous Midbrain Control of Saccade Velocity

The ability to interact with our environment requires the brain to transform spatially represented sensory signals into temporally encoded motor commands for appropriate control of the relevant effectors. For visually guided eye movements, or saccades, the superior colliculus (SC) is assumed to be the final stage of spatial representation, and instantaneous control of the movement is achieved through a rate code representation in the lower brain stem. We investigated whether SC activity in nonhuman primates (Macaca mulatta, 2 male and 1 female) also uses a dynamic rate code, in addition to the spatial representation. Noting that the kinematics of amplitude-matched movements exhibit trial-to-trial variability, we regressed instantaneous SC activity with instantaneous eye velocity and found a robust correlation throughout saccade duration. Peak correlation was tightly linked to time of peak velocity, the optimal efferent delay between SC activity and eye velocity was constant at ~12 ms both at onset and during the saccade, and SC neurons with higher firing rates exhibited stronger correlations. Moreover, the strong correlative relationship and constant efferent delay observation were preserved when eye movement profiles were substantially altered by a blink-induced perturbation. These results indicate that the rate code of individual SC neurons can control instantaneous eye velocity and argue against a serial process of spatial-to-temporal transformation. They also motivated us to consider a new framework of saccade control that does not incorporate traditionally accepted elements, such as the comparator and resettable integrator, whose neural correlates have remained elusive.

SIGNIFICANCE STATEMENT All movements exhibit time-varying features that are under instantaneous control of the innervating neural command. At what stage in the brain is dynamical control present? It is well known that, in the skeletomotor system, neurons in the motor cortex use dynamical control. In the oculomotor system, in contrast, instantaneous velocity control of saccadic eye movements is not thought to be enforced until the lower brainstem. Using correlations between residual signals across trials, we show that instantaneous control of saccade velocity is present earlier in the visuo-oculomotor neuraxis, at the level of superior colliculus. The results require us to consider alternate frameworks of the neural control of saccades.

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