Perceptual warping exposes categorical representations for speech in human brainstem responses.

Jared A Carter, Gavin M Bidelman
Author Information
  1. Jared A Carter: Institute for Intelligent Systems, University of Memphis, Memphis, TN, USA; School of Communication Sciences and Disorders, University of Memphis, Memphis, TN, USA; Division of Clinical Neuroscience, School of Medicine, Hearing Sciences - Scottish Section, University of Nottingham, Glasgow, Scotland, UK.
  2. Gavin M Bidelman: Department of Speech, Language and Hearing Sciences, Indiana University, Bloomington, IN, USA; Program in Neuroscience, Indiana University, Bloomington, IN, USA. Electronic address: gbidel@indiana.edu.

Abstract

The brain transforms continuous acoustic events into discrete category representations to downsample the speech signal for our perceptual-cognitive systems. Such phonetic categories are highly malleable, and their percepts can change depending on surrounding stimulus context. Previous work suggests these acoustic-phonetic mapping and perceptual warping of speech emerge in the brain no earlier than auditory cortex. Here, we examined whether these auditory-category phenomena inherent to speech perception occur even earlier in the human brain, at the level of auditory brainstem. We recorded speech-evoked frequency following responses (FFRs) during a task designed to induce more/less warping of listeners' perceptual categories depending on stimulus presentation order of a speech continuum (random, forward, backward directions). We used a novel clustered stimulus paradigm to rapidly record the high trial counts needed for FFRs concurrent with active behavioral tasks. We found serial stimulus order caused perceptual shifts (hysteresis) near listeners' category boundary confirming identical speech tokens are perceived differentially depending on stimulus context. Critically, we further show neural FFRs during active (but not passive) listening are enhanced for prototypical vs. category-ambiguous tokens and are biased in the direction of listeners' phonetic label even for acoustically-identical speech stimuli. These findings were not observed in the stimulus acoustics nor model FFR responses generated via a computational model of cochlear and auditory nerve transduction, confirming a central origin to the effects. Our data reveal FFRs carry category-level information and suggest top-down processing actively shapes the neural encoding and categorization of speech at subcortical levels. These findings suggest the acoustic-phonetic mapping and perceptual warping in speech perception occur surprisingly early along the auditory neuroaxis, which might aid understanding by reducing ambiguity inherent to the speech signal.

Keywords

References

  1. Nat Neurosci. 2006 Nov;9(11):1367-8 [PMID: 17041591]
  2. Hear Res. 2019 Apr;375:25-33 [PMID: 30772133]
  3. Neuroimage. 2019 Dec;203:116185 [PMID: 31520743]
  4. Brain Lang. 2014 Aug;135:85-95 [PMID: 24992572]
  5. Neuropsychologia. 2014 May;58:23-32 [PMID: 24690415]
  6. Hear Res. 2017 May;348:1-15 [PMID: 28137699]
  7. Neuroimage. 2020 Jan 1;204:116253 [PMID: 31600592]
  8. Eur J Neurosci. 2014 Aug;40(4):2662-73 [PMID: 24890664]
  9. Hear Res. 2017 Mar;345:30-42 [PMID: 28043881]
  10. J Acoust Soc Am. 2017 Apr;141(4):2857 [PMID: 28464636]
  11. Eur J Neurosci. 2017 Mar;45(5):690-699 [PMID: 28112440]
  12. Neuroreport. 2020 Jan 27;31(2):162-166 [PMID: 31834142]
  13. Percept Psychophys. 1985 Apr;37(4):369-76 [PMID: 4034355]
  14. Nature. 1965 Jun 5;206(988):1048-50 [PMID: 5839063]
  15. Front Integr Neurosci. 2014 Feb 21;8:19 [PMID: 24600361]
  16. Neurosci Lett. 2021 Feb 16;746:135664 [PMID: 33497718]
  17. J Cogn Neurosci. 2021 Apr 1;33(5):840-852 [PMID: 34449838]
  18. Neuroreport. 2000 Dec 18;11(18):3989-93 [PMID: 11192615]
  19. Hear Res. 2019 Oct;382:107795 [PMID: 31479953]
  20. Neuroimage. 2015 Oct 15;120:191-200 [PMID: 26146197]
  21. J Neurophysiol. 1988 Dec;60(6):1799-822 [PMID: 3236052]
  22. Nat Commun. 2019 Nov 6;10(1):5036 [PMID: 31695046]
  23. Audiology. 1979;18(5):358-81 [PMID: 496719]
  24. eNeuro. 2021 Dec 23;8(6): [PMID: 34799409]
  25. J Neurosci Methods. 2021 Oct 1;362:109290 [PMID: 34273451]
  26. J Neurosci. 2019 Nov 6;39(45):8916-8928 [PMID: 31541020]
  27. Neuroreport. 1995 Nov 27;6(17):2363-7 [PMID: 8747154]
  28. Commun Biol. 2019 Jul 19;2:265 [PMID: 31341964]
  29. J Speech Lang Hear Res. 2019 Mar 25;62(3):587-601 [PMID: 30950746]
  30. Neuroimage. 2019 Nov 1;201:116022 [PMID: 31310863]
  31. J Neurophysiol. 2009 Oct;102(4):2358-74 [PMID: 19675285]
  32. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2008 Feb;194(2):169-83 [PMID: 18228080]
  33. Ear Hear. 2012 Jan-Feb;33(1):144-50 [PMID: 21760513]
  34. Curr Biol. 2018 May 7;28(9):1419-1427.e4 [PMID: 29681473]
  35. J Acoust Soc Am. 2006 Aug;120(2):1063-74 [PMID: 16938992]
  36. Hear Res. 2008 Jul;241(1-2):34-42 [PMID: 18562137]
  37. Adv Exp Med Biol. 2013;787:231-8 [PMID: 23716228]
  38. Neuroimage. 2018 Jul 15;175:56-69 [PMID: 29604459]
  39. Neuroreport. 2012 May 30;23(8):498-502 [PMID: 22495037]
  40. Hear Res. 2022 Nov;425:108488 [PMID: 35351323]
  41. Percept Psychophys. 1993 Apr;53(4):443-9 [PMID: 8483708]
  42. Cognition. 2011 Apr;119(1):131-6 [PMID: 21144500]
  43. Front Neurosci. 2021 Dec 20;15:747303 [PMID: 34987356]
  44. Neuroreport. 1998 Jun 1;9(8):1889-93 [PMID: 9665621]
  45. Neuroreport. 2011 Nov 16;22(16):801-3 [PMID: 21934635]
  46. Percept Psychophys. 1973 Jun 1;13(2):253-260 [PMID: 23226880]
  47. J Neurosci Methods. 2015 Feb 15;241:94-100 [PMID: 25561397]
  48. J Am Acad Audiol. 2014 Sep;25(8):715-26 [PMID: 25380118]
  49. Electroencephalogr Clin Neurophysiol. 1980 Aug;49(3-4):314-22 [PMID: 6158407]
  50. J Exp Psychol Hum Percept Perform. 1982 Feb;8(1):68-80 [PMID: 6460086]
  51. Neuroimage. 2013 Oct 1;79:201-12 [PMID: 23648960]
  52. Front Hum Neurosci. 2020 Jul 08;14:250 [PMID: 32733220]
  53. Front Psychol. 2013 May 13;4:264 [PMID: 23717294]
  54. Percept Mot Skills. 1993 Jun;76(3 Pt 2):1231-41 [PMID: 8337070]
  55. J Neurolinguistics. 2010 Jan 1;23(1):81-95 [PMID: 20161561]
  56. Brain Lang. 2019 Jul;194:77-83 [PMID: 31129300]
  57. Int J Audiol. 2018 Sep;57(9):665-672 [PMID: 29764252]
  58. Electroencephalogr Clin Neurophysiol. 1977 May;42(5):656-64 [PMID: 67025]
  59. Neuron. 2009 Nov 12;64(3):311-9 [PMID: 19914180]
  60. Neurobiol Aging. 2014 Nov;35(11):2526-2540 [PMID: 24908166]
  61. J Neurosci. 2012 Oct 10;32(41):14156-64 [PMID: 23055485]
  62. Hear Res. 2008 Nov;245(1-2):35-47 [PMID: 18765275]
  63. JASA Express Lett. 2022 Apr;2(4):045201 [PMID: 35434716]
  64. Nat Neurosci. 2010 Nov;13(11):1428-32 [PMID: 20890293]
  65. Neuroreport. 2020 Jul 10;31(10):702-707 [PMID: 32453027]
  66. Brain Behav. 2017 Apr 26;7(6):e00665 [PMID: 28638700]
  67. J Exp Psychol Hum Percept Perform. 1994 Feb;20(1):3-16 [PMID: 8133223]
  68. Proc Natl Acad Sci U S A. 2018 Dec 18;115(51):13129-13134 [PMID: 30509989]
  69. Electroencephalogr Clin Neurophysiol. 1990 Jul-Aug;77(4):295-308 [PMID: 1695141]
  70. Ear Hear. 2010 Jun;31(3):302-24 [PMID: 20084007]
  71. Front Aging Neurosci. 2018 Nov 08;10:357 [PMID: 30467474]
  72. Ear Hear. 2012 May-Jun;33(3):330-9 [PMID: 22374321]
  73. Neuroreport. 2006 Oct 23;17(15):1601-5 [PMID: 17001276]
  74. Ear Hear. 2005 Oct;26(5):424-34 [PMID: 16230893]
  75. Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):11807-14 [PMID: 11050213]
  76. Exp Biol. 1986;45(3):233-65 [PMID: 3525222]
  77. J Acoust Soc Am. 2014 Jan;135(1):283-6 [PMID: 24437768]
  78. Audiol Res. 2014 Jan 03;3(1):e8 [PMID: 26557347]
  79. Science. 1973 Oct 12;182(4108):177-80 [PMID: 4730062]
  80. Front Neural Circuits. 2021 Jan 22;14:615259 [PMID: 33551756]
  81. J Neurosci Methods. 2018 Jan 01;293:59-66 [PMID: 28917659]
  82. Hear Res. 2007 Feb;224(1-2):75-83 [PMID: 17207949]
  83. Neuroimage. 2021 Jul 15;235:118014 [PMID: 33794356]
  84. J Neural Eng. 2021 Mar 23;18(4): [PMID: 33690177]
  85. Nat Neurosci. 2004 Mar;7(3):295-301 [PMID: 14966525]
  86. Neuron. 2012 Oct 18;76(2):435-49 [PMID: 23083744]
  87. Int J Psychophysiol. 2000 Apr;36(1):35-44 [PMID: 10700621]
  88. Neuropsychologia. 2014 Nov;64:13-23 [PMID: 25220167]
  89. J Exp Psychol Hum Percept Perform. 1978 Nov;4(4):599-609 [PMID: 722250]
  90. Neuropsychologia. 1971 Mar;9(1):97-113 [PMID: 5146491]
  91. Nat Neurosci. 2010 Feb;13(2):253-60 [PMID: 20037578]
  92. Brain Res. 2019 Jul 1;1714:182-192 [PMID: 30796895]
  93. Physiol Rev. 2004 Apr;84(2):541-77 [PMID: 15044682]
  94. Psychophysiology. 2010 Mar 1;47(2):236-46 [PMID: 19824950]
  95. Science. 1975 Oct 3;190(4209):69-72 [PMID: 1166301]
  96. Front Neurosci. 2021 Dec 10;15:717572 [PMID: 34955707]
  97. Brain Res. 2021 Nov 15;1771:147643 [PMID: 34473999]
  98. Neuroimage. 2016 Mar;128:32-43 [PMID: 26763154]
  99. Neuroimage. 2022 Sep 16;263:119627 [PMID: 36122686]
  100. Electroencephalogr Clin Neurophysiol. 1975 Nov;39(5):465-72 [PMID: 52439]
  101. Clin Neurophysiol. 2007 Dec;118(12):2544-90 [PMID: 17931964]
  102. Neuroimage. 2021 Feb 1;226:117545 [PMID: 33186711]
  103. Brain Res. 2015 Nov 11;1626:146-64 [PMID: 26187756]
  104. Hear Res. 2015 May;323:68-80 [PMID: 25660195]
  105. Hear Res. 2002 Apr;166(1-2):192-201 [PMID: 12062771]
  106. Neuroimage. 2016 Apr 1;129:214-223 [PMID: 26774614]
  107. J Assoc Res Otolaryngol. 2018 Feb;19(1):83-97 [PMID: 28971333]
  108. Neuroimage. 2021 May 1;231:117866 [PMID: 33592244]
  109. Wiley Interdiscip Rev Cogn Sci. 2010 Jan;1(1):69-78 [PMID: 26272840]
  110. Neuroreport. 2009 Mar 4;20(4):408-13 [PMID: 19223793]
  111. Clin Neurophysiol. 2004 Sep;115(9):2021-30 [PMID: 15294204]
  112. Elife. 2017 Oct 10;6: [PMID: 28992445]
  113. Hear Res. 2009 Aug;254(1-2):15-24 [PMID: 19364526]
  114. Nat Commun. 2016 Mar 24;7:11070 [PMID: 27009409]
  115. Percept Psychophys. 1974;15(2):285-290 [PMID: 23226881]
  116. Neurosci Lett. 2023 Jan 10;793:136976 [PMID: 36427816]
  117. Eur J Neurosci. 2005 Dec;22(11):2879-85 [PMID: 16324123]
  118. J Acoust Soc Am. 1998 Oct;104(4):2385-99 [PMID: 10491702]
  119. Brain Res. 2021 May 15;1759:147385 [PMID: 33631210]
  120. Brain Lang. 2015 Feb;141:62-9 [PMID: 25540857]
  121. J Acoust Soc Am. 2016 Oct;140(4):EL358 [PMID: 27794347]

Grants

  1. R01 DC016267/NIDCD NIH HHS

MeSH Term

Humans
Speech
Brain
Brain Stem
Auditory Perception
Speech Perception
Acoustic Stimulation

Word Cloud

Created with Highcharts 10.0.0speechstimulusperceptualwarpingauditoryFFRsbraindependingperceptionresponseslisteners'categoryrepresentationssignalphoneticcategoriescontextacoustic-phoneticmappingearlierinherentoccurevenhumanbrainstemfollowingorderactiveconfirmingtokensneuralfindingsmodelFFRsuggesttransformscontinuousacousticeventsdiscretedownsampleperceptual-cognitivesystemshighlymalleableperceptscanchangesurroundingPreviousworksuggestsemergecortexexaminedwhetherauditory-categoryphenomenalevelrecordedspeech-evokedfrequencytaskdesignedinducemore/lesspresentationcontinuumrandomforwardbackwarddirectionsusednovelclusteredparadigmrapidlyrecordhightrialcountsneededconcurrentbehavioraltasksfoundserialcausedshiftshysteresisnearboundaryidenticalperceiveddifferentiallyCriticallyshowpassivelisteningenhancedprototypicalvscategory-ambiguousbiaseddirectionlabelacoustically-identicalstimuliobservedacousticsgeneratedviacomputationalcochlearnervetransductioncentralorigineffectsdatarevealcarrycategory-levelinformationtop-downprocessingactivelyshapesencodingcategorizationsubcorticallevelssurprisinglyearlyalongneuroaxismightaidunderstandingreducingambiguityPerceptualexposescategoricalCategoricalCPFrequencyresponseHysteresisNonlineardynamics

Similar Articles

Cited By