Species-specific oculomotor control tolerances predict saccadic suppression strength in macaques and zebrafish

Abstract

Active sensing necessarily requires integrating information about both self-generated movements as well as past, present, and future afferent inputs. However, such information is inherently variable and relies, at least in part, on uncertain extrapolations. Here, using saccadic suppression of visual sensitivity as a classic example of sensory-motor integration, we show that suppression strength in two drastically different species, macaque monkeys and zebrafish larvae, may be a direct outcome of efficient state estimation in the presence of uncontrollable sensory and motor variability. Bayesian estimator models suggest that optimal saccadic suppression should rely not just on the sensory-motor information being processed, but also on the time-dependent magnitude of unexplained variability in the nervous system encoding it. In both macaques and zebrafish larvae, and using matching visual stimulation regimes optimized for each species receptive field properties, we experimentally measured saccadic suppression strength in the superior colliculus (SC) of the monkeys and the homologous optic tectum (OT) of the fish. We also experimentally quantified additive and multiplicative motor noise components in the oculomotor behavior of both species, and we furthermore estimated noise in the sensory systems. We found that inter-species differences in sensory and motor noise levels and their theoretically predicted impacts on visual sensitivity are consistent with our experimentally observed differences in saccadic suppression strength between the fish and the monkeys. Because sensory and motor noise levels can reflect the amounts of available neural resources committed to a given task, our results strongly underscore the value of incorporating computational resource limits into investigating performance differences that have evolved in homologous brain areas.