Locomotor activity enhances environmental representation by boosting visuo-frontal communication

Abstract

During environment exploration we rapidly acquire visual information to identify targets of interest. Here, we discovered that locomotion limits how long natural scenes are viewed dur- ing free exploration. Whether the brain has developed compensatory mechanisms to ensure that sensory information is accurately transmitted to downstream areas during and after locomotion is unknown. We examined this issue by recording the spiking activity of popula- tions of neurons in visual and prefrontal cortex in conjunction with wireless recordings of oculomotor events while macaques moved freely to explore their environment or performed treadmill bipedal locomotion. The communication between visuo-frontal cortical areas was enhanced during and after locomotion to increase visual-evoked responses and population coding accuracy in prefrontal, but not visual cortical neurons. This in turn improved behav- ioral performance in a freely moving visual detection task after locomotion. Electrical stim- ulation further revealed elevated inter-areal synaptic efficacy during locomotor activity. The mechanism whereby locomotion enhances stimulus coding accuracy in prefrontal cortex and behavioral performance by increasing visuo-frontal communication is functionally beneficial during environmental exploration when incoming stimuli are rapidly changing and the win- dow for perceptual decisions is temporally restricted.