Deficits in Visual-Motor Integration in Mice Reared Germ-free are Compensated for by Environmental Exposure and Experience

Abstract

The superior colliculus (SC) of mammals controls fundamental aspects of visual-spatial orienting behavior, attentional control and computing the emotional valence of visual stimuli. Accumulating and recent evidence suggests a key role for early host-microbiome interactions and microglia activity towards shaping midbrain circuitry homologous to the SC in several aquatic species during development, namely tadpoles and larval zebrafish. However, how and whether microbiome manipulation and/or immune cell changes early in development influences natural SC-dependent visual behaviors and how that impacts the structure of mammalian SC was unknown. We examined natural prey capture behavior in mice raised germ free and analyzed cellular structures in the SC as well as visual cortex. Visual areas are subject to well described sensory experience-dependent plasticity during development and are linked to visual prey capture performance in mice. We found specific visual-motor integration deficits in mice reared germ-free that were partially compensated for by prey capture experience as adults. Changes in neuron number, microglia density and inhibitory tone were also found specifically in the SC relative to the visual cortex of germ-free mice with prey capture experience. This establishes a link between microbiome and SC development that impacts an adaptive visual behavior and revealed that predatory hunting allows animals to compensate for developmental deficits in visual-motor behavior induced by microorganism deprivation.