title: Sustained firing of model central auditory neurons yields a discriminative spectro-temporal representation for natural sounds.
abstract: The processing characteristics of neurons in the central auditory system are directly shaped by and reflect the statistics of natural acoustic environments, but the principles that govern the relationship between natural sound ensembles and observed responses in neurophysiological studies remain unclear. In particular, accumulating evidence suggests the presence of a code based on sustained neural firing rates, where central auditory neurons exhibit strong, persistent responses to their preferred stimuli. Such a strategy can indicate the presence of ongoing sounds, is involved in parsing complex auditory scenes, and may play a role in matching neural dynamics to varying time scales in acoustic signals. In this paper, we describe a computational framework for exploring the influence of a code based on sustained firing rates on the shape of the spectro-temporal receptive field (STRF), a linear kernel that maps a spectro-temporal acoustic stimulus to the instantaneous firing rate of a central auditory neuron. We demonstrate the emergence of richly structured STRFs that capture the structure of natural sounds over a wide range of timescales, and show how the emergent ensembles resemble those commonly reported in physiological studies. Furthermore, we compare ensembles that optimize a sustained firing code with one that optimizes a sparse code, another widely considered coding strategy, and suggest how the resulting population responses are not mutually exclusive. Finally, we demonstrate how the emergent ensembles contour the high-energy spectro-temporal modulations of natural sounds, forming a discriminative representation that captures the full range of modulation statistics that characterize natural sound ensembles. These findings have direct implications for our understanding of how sensory systems encode the informative components of natural stimuli and potentially facilitate multi-sensory integration.
authors.affiliation: Department of Electrical and Computer Engineering, The Center for Language and Speech Processing, Johns Hopkins University, Baltimore, Maryland, United States of America.
authors.forename: Michael A
authors.initials: MA
authors.lastname: Carlin
authors.forename: Mounya
authors.initials: M
authors.lastname: Elhilali
mesh_terms: D000161:Acoustic Stimulation; D000818:Animals; D001303:Auditory Cortex / Q000166:cytology / Q000502:physiology*; D001307:Auditory Perception / Q000502:physiology*; D016000:Cluster Analysis; D019295:Computational Biology / Q000379:methods*; D005260:Female; D005289:Ferrets; D006801:Humans; D008297:Male; D008959:Models, Neurological; D009474:Neurons / Q000502:physiology*; D009622:Noise; D013060:Speech; D014828:Vocalization, Animal
references.citation: J Comput Neurosci. 2000 Jul-Aug;9(1):85-111
references.pmid: 10946994
references.citation: Curr Opin Neurobiol. 2004 Aug;14(4):481-7
references.pmid: 15321069
references.citation: IEEE Trans Neural Netw. 2001;12(6):1471-4
references.pmid: 18249975
references.citation: Neural Comput. 2002 Apr;14(4):715-70
references.pmid: 11936959
references.citation: Neuroscience. 2008 Nov 19;157(2):484-94
references.pmid: 19143093
references.citation: Neural Comput. 2011 Dec;23(12):3287-302
references.pmid: 21919780
references.citation: Nature. 1996 Jun 13;381(6583):607-9
references.pmid: 8637596
references.citation: Philos Trans R Soc Lond B Biol Sci. 1992 Jun 29;336(1278):367-73
references.pmid: 1354376
references.citation: Neural Comput. 1991 Summer;3(2):194-200
references.pmid: 31167302
references.citation: PLoS One. 2011 Jan 11;6(1):e16104
references.pmid: 21264310
references.citation: PLoS Biol. 2008 Jan;6(1):e16
references.pmid: 18232737
references.citation: J Neurophysiol. 2001 Mar;85(3):1220-34
references.pmid: 11247991
references.citation: Neuron. 2008 Jun 26;58(6):938-55
references.pmid: 18579083
references.citation: J Neurophysiol. 2009 Dec;102(6):3329-39
references.pmid: 19759321
references.citation: Nat Neurosci. 2005 Oct;8(10):1371-9
references.pmid: 16136039
references.citation: Curr Opin Neurobiol. 2001 Aug;11(4):475-80
references.pmid: 11502395
references.citation: Neural Comput. 2006 Aug;18(8):1868-95
references.pmid: 16771656
references.citation: J Neurosci. 2009 Mar 4;29(9):2780-93
references.pmid: 19261874
references.citation: Nature. 2006 Feb 23;439(7079):978-82
references.pmid: 16495999
references.citation: Neural Comput. 1991 Fall;3(3):312-320
references.pmid: 31167313
references.citation: J Acoust Soc Am. 2008 Dec;124(6):3751-71
references.pmid: 19206802
references.citation: J Acoust Soc Am. 2003 Dec;114(6 Pt 1):3394-411
references.pmid: 14714819
references.citation: Curr Opin Neurobiol. 2011 Oct;21(5):761-7
references.pmid: 21704508
references.citation: Hear Res. 2007 Jul;229(1-2):81-93
references.pmid: 17346911
references.citation: Neuron. 2007 Apr 5;54(1):153-65
references.pmid: 17408584
references.citation: J Neurosci. 2004 Feb 4;24(5):1159-72
references.pmid: 14762134
references.citation: J Neurosci. 2010 Nov 24;30(47):15969-80
references.pmid: 21106835
references.citation: Biol Cybern. 1981;42(2):133-43
references.pmid: 7326288
references.citation: Nat Neurosci. 2005 Jul;8(7):851-2
references.pmid: 16136671
references.citation: Annu Rev Neurosci. 2001;24:1193-216
references.pmid: 11520932
references.citation: J Vis. 2005 Jul 20;5(6):579-602
references.pmid: 16097870
references.citation: J Neurosci. 2009 Mar 18;29(11):3374-86
references.pmid: 19295144
references.citation: J Neurophysiol. 2002 Jan;87(1):516-27
references.pmid: 11784767
references.citation: J Neurosci. 2003 Aug 27;23(21):7940-9
references.pmid: 12944525
references.citation: J Acoust Soc Am. 2005 Aug;118(2):887-906
references.pmid: 16158645
references.citation: Network. 2001 Aug;12(3):255-70
references.pmid: 11563529
references.citation: Nat Neurosci. 2003 Nov;6(11):1216-23
references.pmid: 14583754
references.citation: Nature. 2005 May 19;435(7040):341-6
references.pmid: 15902257
references.citation: Network. 2003 Nov;14(4):765-88
references.pmid: 14653502
references.citation: Neural Comput. 2003 Mar;15(3):663-91
references.pmid: 12620162
references.citation: Neural Comput. 2006 Oct;18(10):2495-508
references.pmid: 16907634
references.citation: Network. 2001 Aug;12(3):289-316
references.pmid: 11563531
references.citation: J Neurophysiol. 2004 Jan;91(1):206-12
references.pmid: 12904330
references.citation: Neural Comput. 2008 Apr;20(4):1026-41
references.pmid: 18085988
references.citation: PLoS Comput Biol. 2012;8(7):e1002594
references.pmid: 22807665
references.citation: Science. 2000 Feb 18;287(5456):1273-6
references.pmid: 10678835
references.citation: Neural Comput. 2010 Dec;22(12):2979-3035
references.pmid: 20858129