A transient signal in foveal superior colliculus neurons for jumpstarting peripheral saccadic orienting
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The superior colliculus (SC) both senses the environment and orients gaze within it. While the SC’s sensory and motor bursts appear qualitatively similar to each other, population activity structure in the two processing regimes is very different, necessitating a hitherto unexplored rapid representational transformation, occurring on the scale of only tens of milliseconds. Here, using male rhesus macaque monkeys, we first show that when a planned saccade is released with a go signal, peripheral SC neurons representing the saccade target location exhibit a transient, short-latency pause right before their motor bursts eventually erupt. This pause starts within ∼50 ms from the go signal, and it is stimulus-dependent. It is also absent in the primary visual cortex, and is significantly weaker in purely visual SC neurons than in saccade-related ones. Foveal SC neurons, on the other hand, burst, and their bursts lead the peripheral neurons’ pauses by ∼10 milliseconds. Remarkably, during immediate visually-guided saccade tasks, requiring a transformation from visual to motor peripheral bursts in <50-100 ms, the transient foveal SC bursts still occur, resulting in simultaneous short-latency bursting at two disparate SC loci: one foveal; and one eccentric and responding to the visual appearance of the saccade target. Our results suggest that in classic saccade tasks used to investigate visual, motor, and cognitive processes in primate brains, a transient foveal SC signal may jumpstart peripheral saccadic orienting by facilitating a necessary rapid representational transformation needed for SC saccade motor bursts to ensue.
Significance
Studies of eye movement control often involve behavioral paradigms involving sensing, deliberating, and ultimately releasing an instructed rapid eye movement (saccade). While the sensing, deliberation, and movement aspects of saccades have been well studied in the past, the releasing phase is less understood. Using classic saccade behavioral paradigms, we discovered that foveal superior colliculus neurons exhibit transient activity bursts during instructed saccade releasing, which likely enables rapid representational transformations from a visual to a motor regime in the collicular neurons driving the eye movements.
