title: Auditory distance coding in rabbit midbrain neurons and human perception: monaural amplitude modulation depth as a cue.
abstract: Mechanisms underlying sound source distance localization are not well understood. Here we tested the hypothesis that a novel mechanism can create monaural distance sensitivity: a combination of auditory midbrain neurons' sensitivity to amplitude modulation (AM) depth and distance-dependent loss of AM in reverberation. We used virtual auditory space (VAS) methods for sounds at various distances in anechoic and reverberant environments. Stimulus level was constant across distance. With increasing modulation depth, some rabbit inferior colliculus neurons increased firing rates whereas others decreased. These neurons exhibited monotonic relationships between firing rates and distance for monaurally presented noise when two conditions were met: (1) the sound had AM, and (2) the environment was reverberant. The firing rates as a function of distance remained approximately constant without AM in either environment and, in an anechoic condition, even with AM. We corroborated this finding by reproducing the distance sensitivity using a neural model. We also conducted a human psychophysical study using similar methods. Normal-hearing listeners reported perceived distance in response to monaural 1 octave 4 kHz noise source sounds presented at distances of 35-200 cm. We found parallels between the rabbit neural and human responses. In both, sound distance could be discriminated only if the monaural sound in reverberation had AM. These observations support the hypothesis. When other cues are available (e.g., in binaural hearing), how much the auditory system actually uses the AM as a distance cue remains to be determined.
authors.affiliation: Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030, kim@neuron.uchc.edu.
authors.forename: Duck O
authors.initials: DO
authors.lastname: Kim
authors.affiliation: Division of Communicative Disorders, Department of Surgery, University of Louisville School of Medicine, Louisville, Kentucky 40292 and.
authors.forename: Pavel
authors.initials: P
authors.lastname: Zahorik
authors.affiliation: University of Rochester, Rochester, New York 14642.
authors.forename: Laurel H
authors.identifier: http://orcid.org/0000-0002-4729-5702
authors.initials: LH
authors.lastname: Carney
authors.affiliation: Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030.
authors.forename: Brian B
authors.initials: BB
authors.lastname: Bishop
authors.affiliation: Department of Neuroscience, University of Connecticut Health Center, Farmington, Connecticut 06030.
authors.forename: Shigeyuki
authors.initials: S
authors.lastname: Kuwada
mesh_terms: D000161:Acoustic Stimulation; D000200:Action Potentials / Q000502:physiology; D000293:Adolescent; D000818:Animals; D003463:Cues; D004215:Distance Perception / Q000502:physiology*; D005260:Female; D006801:Humans; D007245:Inferior Colliculi / Q000166:cytology* / Q000502:physiology*; D008297:Male; D008959:Models, Neurological; D009474:Neurons / Q000502:physiology*; D011817:Rabbits; D013017:Sound Localization / Q000502:physiology*; D055815:Young Adult
keywords: amplitude; localization; looming; modulation; personal space; sound
references.citation: Trends Neurosci. 1992 Mar;15(3):86-92
references.pmid: 1373923
references.citation: Proc Natl Acad Sci U S A. 2012 Jul 3;109(27):11019-24
references.pmid: 22699495
references.citation: Physiol Rev. 2010 Jul;90(3):983-1012
references.pmid: 20664077
references.citation: Proc Meet Acoust. 2012 Jun 1;15:null
references.pmid: 23437416
references.citation: Hear Res. 2014 Jan;307:86-97
references.pmid: 23886698
references.citation: J Neurophysiol. 2000 Jul;84(1):255-73
references.pmid: 10899201
references.citation: J Acoust Soc Am. 2011 Sep;130(3):1530-41
references.pmid: 21895092
references.citation: J Acoust Soc Am. 2009 Aug;126(2):776-91
references.pmid: 19640043
references.citation: J Assoc Res Otolaryngol. 2010 Dec;11(4):541-57
references.pmid: 20526728
references.citation: Psychol Rev. 1974 Mar;81(2):119-45
references.pmid: 4817611
references.citation: Adv Exp Med Biol. 2013;787:273-82
references.pmid: 23716233
references.citation: Science. 1995 Oct 13;270(5234):303-4
references.pmid: 7569981
references.citation: Curr Biol. 2008 Jul 8;18(13):963-8
references.pmid: 18585039
references.citation: J Neurophysiol. 2014 Sep 15;112(6):1340-55
references.pmid: 24944219
references.citation: J Acoust Soc Am. 2002 Nov;112(5 Pt 1):2110-7
references.pmid: 12430822
references.citation: Front Psychol. 2014 Oct 07;5:1097
references.pmid: 25339924
references.citation: J Acoust Soc Am. 1983 Nov;74(5):1380-91
references.pmid: 6643850
references.citation: Acta Otolaryngol. 2008 Apr;128(4):382-7
references.pmid: 18368570
references.citation: J Assoc Res Otolaryngol. 2015 Apr;16(2):255-62
references.pmid: 25595542
references.citation: Nature. 1999 Feb 11;397(6719):517-20
references.pmid: 10028966
references.citation: J Acoust Soc Am. 1999 Oct;106(4 Pt 1):1956-68
references.pmid: 10530020
references.citation: Front Neural Circuits. 2012 Jun 28;6:42
references.pmid: 22754505
references.citation: Physiol Rev. 2004 Apr;84(2):541-77
references.pmid: 15044682
references.citation: Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):8005-10
references.pmid: 8755593
references.citation: Perception. 1989;18(3):403-16
references.pmid: 2798023
references.citation: J Acoust Soc Am. 2010 Sep;128(3):1224-34
references.pmid: 20815458
references.citation: Nat Neurosci. 2005 Dec;8(12):1684-9
references.pmid: 16286934
references.citation: Nature. 1999 Feb 4;397(6718):428-30
references.pmid: 9989407
references.citation: J Assoc Res Otolaryngol. 2003 Sep;4(3):294-311
references.pmid: 14690049
references.citation: Proc Natl Acad Sci U S A. 2002 Nov 26;99(24):15755-7
references.pmid: 12429855
references.citation: J Acoust Soc Am. 2004 Oct;116(4 Pt 1):2173-86
references.pmid: 15532650
references.citation: J Acoust Soc Am. 2013 Nov;134(5):3395-8
references.pmid: 24180748
references.citation: J Acoust Soc Am. 2008 Jul;124(1):450-61
references.pmid: 18646989
references.citation: Cogn Process. 2004 Jun;5(2):94-105
references.pmid: 16467906
references.citation: Annu Rev Psychol. 1991;42:135-59
references.pmid: 2018391
references.citation: J Neurosci. 2008 Jun 18;28(25):6430-8
references.pmid: 18562614
references.citation: J Acoust Soc Am. 2003 Dec;114(6 Pt 1):3394-411
references.pmid: 14714819
references.citation: J Acoust Soc Am. 2014 Jan;135(1):283-6
references.pmid: 24437768
references.citation: Perception. 1979;8(3):311-22
references.pmid: 534158
references.citation: Neuron. 2011 Sep 8;71(5):926-40
references.pmid: 21903084
references.citation: Curr Biol. 2003 Feb 4;13(3):R91-3
references.pmid: 12573234
references.citation: J Acoust Soc Am. 2005 May;117(5):3100-15
references.pmid: 15957778
references.citation: J Acoust Soc Am. 2004 Jul;116(1):478-90
references.pmid: 15296007
references.citation: J Neurosci. 2013 Feb 27;33(9):4128-39
references.pmid: 23447621
references.citation: J Neurophysiol. 2007 Jan;97(1):522-39
references.pmid: 17079342
references.citation: J Acoust Soc Am. 2002 Apr;111(4):1832-46
references.pmid: 12002867
references.citation: Psychol Rev. 1957 Nov;64, Part 1(6):384-404
references.pmid: 13505974
references.citation: J Neurosci. 2013 Feb 27;33(9):3891-904
references.pmid: 23447600
references.citation: J Acoust Soc Am. 1990 Sep;88(3):1367-73
references.pmid: 2229672