Abstract

Our natural world is three-dimensional. A fundamental requirement of spatial orientating behaviors in the natural environment is the representation of 3D sensory space. Despite the importance of 3D sensory coding of a natural scene to guide movement, most neurophysiological investigations of this problem have been limited to studies of restrained subjects, tested with 2D, artificial stimuli. Here we show for the first time that auditory neurons in the midbrain superior colliculus of the free-flying echolocating bat encode 3D egocentric sensory space, and that sonar-guided inspection of objects in the environment sharpens spatial tuning of single neurons. Combining wireless multichannel neural recordings from free-flying bats, synchronized with video and audio data, and an echo model that computes the flying animal’s instantaneous, stimulus space, we demonstrate 3D echo-evoked receptive fields of single auditory midbrain neurons in animals orienting in a complex environment. We discovered that the bat’s ac...

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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