Primate Saccade Rhythmicity

Abstract

Rhythmic sampling is a hallmark of many sensory systems in many diverse organisms. In primate vision, rapid foveating eye movements continuously scan the visual environment at a rate of 2-6 Hz, but the statistics of inter-saccadic interval distributions could equally well be described by non-rhythmic stochastic processes as by a (putatively variable) rhythmic oscillator. This raises the fundamental question whether primate visual scanning actually differs from the numerous examples of rhythmic sampling strategies exhibited across species and sensory modalities. Here, using experiments in humans, macaques, and a marmoset, as well as statistical approaches inspired by studies of temporal structure in neuronal spiking patterns, we show that primate saccade generation is unambiguously rooted in a rhythmic source. This finding was remarkably consistent across the three primate species despite their significant evolutionary distance. We find that saccade rate undergoes smooth, slow fluctuations. Accounting for those rate fluctuations was crucial for revealing the true degree of saccade rhythmicity. Thus, exact saccade timing is determined by an interaction between the slow saccade-rate fluctuations with the more temporally-local rhythmic generator. This demonstration of rhythmicity in overt oculomotor sampling behavior provides a link to the fundamental rhythmic nature of many central perceptual and cognitive processes, and places primate saccadic sampling into the large family of rhythmic active sampling behaviors.