Abstract

Essential to spatial orientation in the natural environment is a dynamic representation of direction and distance to objects. Despite the importance of 3D spatial localization to parse objects in the environment and to guide movement, most neurophysiological investigations of sensory mapping have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here, we show for the first time that sensory neurons in the midbrain superior colliculus (SC) of the free-flying echolocating bat encode 3D egocentric space, and that the bat's inspection of objects in the physical environment sharpens tuning of single neurons, and shifts peak responses to represent closer distances. These findings emerged from wireless neural recordings in free-flying bats, in combination with an echo model that computes the animal's instantaneous stimulus space. Our research reveals dynamic 3D space coding in a freely moving mammal engaged in a real-world navigation task.

Highlights

  • As humans and other animals move in a 3D world, they rely on dynamic sensory information to guide their actions, seek food, track targets and steer around obstacles

  • Previous work in other systems has shown that the gamma frequency band (40–140 Hz - Sridharan and Knudsen, 2015) of the local field potential (LFP) in the superior colliculus (SC) increases in power when an animal is attending in space (Gregoriou et al, 2009; Gunduz et al, 2011; Sridharan and Knudsen, 2015), and we investigated whether this conserved indicator of spatial attention appears during sonar sound groups (SSGs) production

  • An animal must compute the direction and distance to targets and obstacles, and update this information as it moves through space

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Summary

Introduction

As humans and other animals move in a 3D world, they rely on dynamic sensory information to guide their actions, seek food, track targets and steer around obstacles. Such natural behaviors invoke feedback between sensory space representation, attention and action-selection (Lewicki et al, 2014). Animals that rely on active sensing provide a powerful system to investigate the neural underpinnings of sensory-guided behaviors, as they produce the very signals that inform motor actions. Echolocating bats, for example, transmit sonar signals and process auditory information carried by returning echoes to guide behavioral decisions for spatial orientation (Griffin, 1958). The bat’s acoustic behaviors provide a quantitative metric of spatial gaze, and can be analyzed together with neural recordings to investigate the dynamic representation of sensory space

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