Spectrally specific temporal analyses of spike-train responses to complex sounds: A unifying framework.
Acoustic Stimulation
Animals
Auditory Perception
/ physiology
Chinchilla
/ physiology
Cochlear Nerve
/ physiology
Computational Biology
Disease Models, Animal
Evoked Potentials, Auditory
/ physiology
Hearing Loss, Sensorineural
/ physiopathology
Humans
Models, Animal
Models, Neurological
Nonlinear Dynamics
Psychoacoustics
Sound
Spatio-Temporal Analysis
Speech Intelligibility
/ physiology
Speech Perception
/ physiology
Translational Research, Biomedical
Journal
PLoS computational biology
ISSN: 1553-7358
Titre abrégé: PLoS Comput Biol
Pays: United States
ID NLM: 101238922
Informations de publication
Date de publication:
02 2021
02 2021
Historique:
received:
14
07
2020
accepted:
04
02
2021
revised:
04
03
2021
pubmed:
23
2
2021
medline:
22
6
2021
entrez:
22
2
2021
Statut:
epublish
Résumé
Significant scientific and translational questions remain in auditory neuroscience surrounding the neural correlates of perception. Relating perceptual and neural data collected from humans can be useful; however, human-based neural data are typically limited to evoked far-field responses, which lack anatomical and physiological specificity. Laboratory-controlled preclinical animal models offer the advantage of comparing single-unit and evoked responses from the same animals. This ability provides opportunities to develop invaluable insight into proper interpretations of evoked responses, which benefits both basic-science studies of neural mechanisms and translational applications, e.g., diagnostic development. However, these comparisons have been limited by a disconnect between the types of spectrotemporal analyses used with single-unit spike trains and evoked responses, which results because these response types are fundamentally different (point-process versus continuous-valued signals) even though the responses themselves are related. Here, we describe a unifying framework to study temporal coding of complex sounds that allows spike-train and evoked-response data to be analyzed and compared using the same advanced signal-processing techniques. The framework uses a set of peristimulus-time histograms computed from single-unit spike trains in response to polarity-alternating stimuli to allow advanced spectral analyses of both slow (envelope) and rapid (temporal fine structure) response components. Demonstrated benefits include: (1) novel spectrally specific temporal-coding measures that are less confounded by distortions due to hair-cell transduction, synaptic rectification, and neural stochasticity compared to previous metrics, e.g., the correlogram peak-height, (2) spectrally specific analyses of spike-train modulation coding (magnitude and phase), which can be directly compared to modern perceptually based models of speech intelligibility (e.g., that depend on modulation filter banks), and (3) superior spectral resolution in analyzing the neural representation of nonstationary sounds, such as speech and music. This unifying framework significantly expands the potential of preclinical animal models to advance our understanding of the physiological correlates of perceptual deficits in real-world listening following sensorineural hearing loss.
Identifiants
pubmed: 33617548
doi: 10.1371/journal.pcbi.1008155
pii: PCOMPBIOL-D-20-01242
pmc: PMC7932515
doi:
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e1008155Subventions
Organisme : NIDCD NIH HHS
ID : R01 DC009838
Pays : United States
Organisme : NIDCD NIH HHS
ID : R01 DC015989
Pays : United States
Déclaration de conflit d'intérêts
The authors have declared that no competing interests exist.
Références
J Neurosci. 2003 Jul 16;23(15):6345-50
pubmed: 12867519
J Acoust Soc Am. 1978 Nov;64(5):1386-91
pubmed: 744838
Hear Res. 2014 Mar;309:55-62
pubmed: 24315815
J Acoust Soc Am. 1980 Jan;67(1):318-26
pubmed: 7354199
J Acoust Soc Am. 2006 Mar;119(3):1562-73
pubmed: 16583901
J Acoust Soc Am. 2013 Jul;134(1):436-46
pubmed: 23862819
J Acoust Soc Am. 1989 May;85(5):1978-94
pubmed: 2732379
Science. 1995 Oct 13;270(5234):303-4
pubmed: 7569981
J Acoust Soc Am. 2008 Dec;124(6):3937-46
pubmed: 19206818
Hear Res. 2010 Jun 1;264(1-2):48-55
pubmed: 19944140
J Acoust Soc Am. 1999 Jun;105(6):3509-23
pubmed: 10380673
Neural Comput. 2002 Feb;14(2):325-46
pubmed: 11802915
J Acoust Soc Am. 1984 Mar;75(3):887-96
pubmed: 6707318
J Acoust Soc Am. 1983 Feb;73(2):602-15
pubmed: 6841800
Ear Hear. 2006 Apr;27(2):93-103
pubmed: 16518138
J Acoust Soc Am. 1995 May;97(5 Pt 1):3099-111
pubmed: 7759650
Int J Audiol. 2009;48(10):729-41
pubmed: 19626512
J Neurophysiol. 1996 Sep;76(3):1698-716
pubmed: 8890286
J Acoust Soc Am. 2011 Sep;130(3):1475-87
pubmed: 21895088
Nature. 2002 Mar 7;416(6876):87-90
pubmed: 11882898
J Acoust Soc Am. 1986 Jun;79(6):1896-914
pubmed: 3722600
Acta Acust United Acust. 2018 Sep-Oct;104(5):914-917
pubmed: 33273897
J Neurosci. 2019 Aug 28;39(35):6879-6887
pubmed: 31285299
Ear Hear. 2016 Mar-Apr;37(2):e91-e103
pubmed: 26583482
Adv Exp Med Biol. 2013;787:501-10
pubmed: 23716257
J Assoc Res Otolaryngol. 2009 Sep;10(3):407-23
pubmed: 19365691
J Assoc Res Otolaryngol. 2016 Apr;17(2):133-43
pubmed: 26920344
Hear Res. 2008 Nov;245(1-2):35-47
pubmed: 18765275
J Acoust Soc Am. 2016 Oct;140(4):2670
pubmed: 27794330
Hear Res. 2018 Mar;360:40-54
pubmed: 29395616
Neuroimage. 2014 Mar;88:41-6
pubmed: 24188816
IEEE Trans Biomed Eng. 2014 May;61(5):1555-64
pubmed: 24759284
J Acoust Soc Am. 2019 Nov;146(5):3710
pubmed: 31795699
Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18866-9
pubmed: 17116863
Ear Hear. 2010 Jun;31(3):302-24
pubmed: 20084007
Neuron. 2008 Jun 12;58(5):789-801
pubmed: 18549789
J Assoc Res Otolaryngol. 2003 Sep;4(3):294-311
pubmed: 14690049
Hear Res. 2015 May;323:91-8
pubmed: 25724819
J Acoust Soc Am. 2018 Oct;144(4):2400
pubmed: 30404467
J Neurophysiol. 2004 May;91(5):2051-65
pubmed: 15069097
Hear Res. 2019 Apr;375:25-33
pubmed: 30772133
J Assoc Res Otolaryngol. 2021 Feb;22(1):51-66
pubmed: 33188506
Hear Res. 2006 Jun-Jul;216-217:19-30
pubmed: 16644160
J Acoust Soc Am. 1997 Jun;101(6):3602-16
pubmed: 9193048
Cell Tissue Res. 2015 Jul;361(1):129-58
pubmed: 25920587
J Acoust Soc Am. 1980 Sep;68(3):843-57
pubmed: 7419820
Ear Hear. 2013 Jan-Feb;34(1):42-51
pubmed: 22874644
J Acoust Soc Am. 1983 Aug;74(2):502-17
pubmed: 6619427
J Acoust Soc Am. 1978 Feb;63(2):442-55
pubmed: 670542
J Acoust Soc Am. 1969 Oct;46(4):924-38
pubmed: 4309951
J Neurophysiol. 1969 Jul;32(4):613-36
pubmed: 5810617
J Acoust Soc Am. 1979 Nov;66(5):1381-1403
pubmed: 500976
J Acoust Soc Am. 1984 Mar;75(3):866-78
pubmed: 6707316
J Assoc Res Otolaryngol. 2010 Dec;11(4):657-73
pubmed: 20556628
J Assoc Res Otolaryngol. 2014 Oct;15(5):767-87
pubmed: 24890715
J Acoust Soc Am. 1992 Jan;91(1):215-32
pubmed: 1737873
Audiol Neurootol. 2000 Nov-Dec;5(6):312-21
pubmed: 11025331