title: Human Exploration of Enclosed Spaces through Echolocation.
abstract: Some blind humans have developed echolocation, as a method of navigation in space. Echolocation is a truly active sense because subjects analyze echoes of dedicated, self-generated sounds to assess space around them. Using a special virtual space technique, we assess how humans perceive enclosed spaces through echolocation, thereby revealing the interplay between sensory and vocal-motor neural activity while humans perform this task. Sighted subjects were trained to detect small changes in virtual-room size analyzing real-time generated echoes of their vocalizations. Individual differences in performance were related to the type and number of vocalizations produced. We then asked subjects to estimate virtual-room size with either active or passive sounds while measuring their brain activity with fMRI. Subjects were better at estimating room size when actively vocalizing. This was reflected in the hemodynamic activity of vocal-motor cortices, even after individual motor and sensory components were removed. Activity in these areas also varied with perceived room size, although the vocal-motor output was unchanged. In addition, thalamic and auditory-midbrain activity was correlated with perceived room size; a likely result of top-down auditory pathways for human echolocation, comparable with those described in echolocating bats. Our data provide evidence that human echolocation is supported by active sensing, both behaviorally and in terms of brain activity. The neural sensory-motor coupling complements the fundamental acoustic motor-sensory coupling via the environment in echolocation.SIGNIFICANCE STATEMENTPassive listening is the predominant method for examining brain activity during echolocation, the auditory analysis of self-generated sounds. We show that sighted humans perform better when they actively vocalize than during passive listening. Correspondingly, vocal motor and cerebellar activity is greater during active echolocation than vocalization alone. Motor and subcortical auditory brain activity covaries with the auditory percept, although motor output is unchanged. Our results reveal behaviorally relevant neural sensory-motor coupling during echolocation.
authors.affiliation: German Center for Vertigo and Balance Disorders, Ludwig-Maximilians-Universität (LMU Munich), Munich, Germany, vflanagin@lrz.uni-muenchen.de.
authors.forename: Virginia L
authors.initials: VL
authors.lastname: Flanagin
authors.affiliation: Division of Neurobiology, Department of Biology II, LMU Munich, Munich, Germany.
authors.forename: Sven
authors.identifier: 0000-0002-5372-0162
authors.initials: S
authors.lastname: Schörnich
authors.affiliation: Division of Neurobiology, Department of Biology II, LMU Munich, Munich, Germany.
authors.forename: Michael
authors.initials: M
authors.lastname: Schranner
authors.affiliation: German Center for Vertigo and Balance Disorders, Ludwig-Maximilians-Universität (LMU Munich), Munich, Germany.
authors.forename: Nadine
authors.initials: N
authors.lastname: Hummel
authors.affiliation: Division of Neurobiology, Department of Biology II, LMU Munich, Munich, Germany.
authors.forename: Ludwig
authors.initials: L
authors.lastname: Wallmeier
authors.affiliation: Fjord&Bælt and University of Southern Denmark, DK-5300 Kerteminde, Denmark, and.
authors.forename: Magnus
authors.initials: M
authors.lastname: Wahlberg
authors.affiliation: German Center for Vertigo and Balance Disorders, Ludwig-Maximilians-Universität (LMU Munich), Munich, Germany.|Department of Neurology, LMU Munich, Munich, Germany.
authors.forename: Thomas
authors.identifier: 0000-0002-4913-5630
authors.initials: T
authors.lastname: Stephan
authors.affiliation: Division of Neurobiology, Department of Biology II, LMU Munich, Munich, Germany.
authors.forename: Lutz
authors.identifier: 0000-0002-9289-6187
authors.initials: L
authors.lastname: Wiegrebe
mesh_terms: D000161:Acoustic Stimulation / Q000379:methods*; D000328:Adult; D000818:Animals; D001307:Auditory Perception / Q000502:physiology*; D004455:Echolocation / Q000502:physiology*; D005260:Female; D006801:Humans; D008279:Magnetic Resonance Imaging / Q000379:methods; D008297:Male; D013017:Sound Localization / Q000502:physiology*; D055815:Young Adult
keywords: echolocation; fMRI; sensory-motor coupling; spatial processing; virtual acoustic space