Frequency-Following Responses to Speech Sounds Are Highly Conserved across Species and Contain Cortical Contributions.

G Nike Gnanateja, Kyle Rupp, Fernando Llanos, Madison Remick, Marianny Pernia, Srivatsun Sadagopan, Tobias Teichert, Taylor J Abel, Bharath Chandrasekaran
Author Information
  1. G Nike Gnanateja: Department of Communication Sciences and Disorders, University of Pittsburgh, Pittsburgh, Pennsylvania 15260. ORCID
  2. Kyle Rupp: Department of Neurological Surgery, UPMC Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania 15213.
  3. Fernando Llanos: Department of Linguistics, The University of Texas at Austin, Austin, Texas 78712.
  4. Madison Remick: Department of Neurological Surgery, UPMC Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania 15213.
  5. Marianny Pernia: Center for Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15261.
  6. Srivatsun Sadagopan: Department of Communication Sciences and Disorders, University of Pittsburgh, Pittsburgh, Pennsylvania 15260. ORCID
  7. Tobias Teichert: Center for Neuroscience, University of Pittsburgh, Pittsburgh, Pennsylvania 15261.
  8. Taylor J Abel: Department of Neurological Surgery, UPMC Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania 15213.
  9. Bharath Chandrasekaran: Department of Communication Sciences and Disorders, University of Pittsburgh, Pittsburgh, Pennsylvania 15260 b.chandra@pitt.edu.

Abstract

Time-varying pitch is a vital cue for human speech perception. Neural processing of time-varying pitch has been extensively assayed using scalp-recorded frequency-following responses (FFRs), an electrophysiological signal thought to reflect integrated phase-locked neural ensemble activity from subcortical auditory areas. Emerging evidence increasingly points to a putative contribution of auditory cortical ensembles to the scalp-recorded FFRs. However, the properties of cortical FFRs and precise characterization of laminar sources are still unclear. Here we used direct human intracortical recordings as well as extracranial and intracranial recordings from macaques and guinea pigs to characterize the properties of cortical sources of FFRs to time-varying pitch patterns. We found robust FFRs in the auditory cortex across all species. We leveraged representational similarity analysis as a translational bridge to characterize similarities between the human and animal models. Laminar recordings in animal models showed FFRs emerging primarily from the thalamorecipient layers of the auditory cortex. FFRs arising from these cortical sources significantly contributed to the scalp-recorded FFRs via volume conduction. Our research paves the way for a wide array of studies to investigate the role of cortical FFRs in auditory perception and plasticity.

Keywords

References

  1. Electroencephalogr Clin Neurophysiol. 1975 Apr;38(4):379-86 [PMID: 46818]
  2. Nat Commun. 2019 Nov 6;10(1):5036 [PMID: 31695046]
  3. PLoS Biol. 2006 Jul;4(7):e215 [PMID: 16774452]
  4. Hear Res. 2016 Jun;336:29-43 [PMID: 27085798]
  5. Front Neural Circuits. 2018 Jul 24;12:55 [PMID: 30087597]
  6. Ear Hear. 2010 Jun;31(3):302-24 [PMID: 20084007]
  7. Hear Res. 2018 Jan;357:25-32 [PMID: 29156225]
  8. Front Neurol. 2020 Dec 16;11:570010 [PMID: 33391145]
  9. J Neurophysiol. 2016 Nov 1;116(5):2346-2355 [PMID: 27535374]
  10. Otolaryngol Head Neck Surg (1979). 1980 Sep-Oct;88(5):613-8 [PMID: 7443268]
  11. J Acoust Soc Am. 1976 Sep;60(3):687-95 [PMID: 824334]
  12. Front Syst Neurosci. 2008 Nov 24;2:4 [PMID: 19104670]
  13. J Neurosci. 2017 Jan 25;37(4):830-838 [PMID: 28123019]
  14. Ear Hear. 2017 Jul/Aug;38(4):e200-e214 [PMID: 28319479]
  15. Sci Rep. 2016 Dec 22;6:39009 [PMID: 28005070]
  16. J Neurosci. 2021 May 5;41(18):4073-4087 [PMID: 33731448]
  17. Science. 1978 Aug 18;201(4356):639-41 [PMID: 675250]
  18. Front Neurosci. 2017 Aug 25;11:479 [PMID: 28890684]
  19. PLoS Biol. 2015 Jul 14;13(7):e1002196 [PMID: 26172057]
  20. Audiology. 1979;18(5):358-81 [PMID: 496719]
  21. Trends Cogn Sci. 2004 May;8(5):204-10 [PMID: 15120678]
  22. Comput Intell Neurosci. 2011;2011:879716 [PMID: 21584256]
  23. Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):11800-6 [PMID: 11050212]
  24. Electroencephalogr Clin Neurophysiol. 1968 Jul;25(1):42-52 [PMID: 4174782]
  25. Trends Cogn Sci. 2007 Sep;11(9):369-72 [PMID: 17698406]
  26. Curr Biol. 2018 May 7;28(9):1419-1427.e4 [PMID: 29681473]
  27. Philos Trans R Soc Lond B Biol Sci. 2021 Jan 4;376(1815):20190633 [PMID: 33190601]
  28. J Neurosci. 2016 Feb 17;36(7):2302-15 [PMID: 26888939]
  29. Neuroimage. 2018 Jul 15;175:56-69 [PMID: 29604459]
  30. J Am Acad Audiol. 2001 Nov-Dec;12(10):523-33 [PMID: 11791939]
  31. Neuroreport. 2012 May 30;23(8):498-502 [PMID: 22495037]
  32. Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):11793-9 [PMID: 11050211]
  33. PLoS One. 2012;7(12):e51646 [PMID: 23251604]
  34. Neurosurgery. 2018 Jan 1;82(1):E15-E16 [PMID: 29048504]
  35. Neurosci Lett. 2000 Oct 6;292(2):123-7 [PMID: 10998564]
  36. Percept Mot Skills. 2014 Jun;118(3):681-90 [PMID: 25068740]
  37. J Neurolinguistics. 2010 Jan 1;23(1):81-95 [PMID: 20161561]
  38. PLoS One. 2014 Sep 22;9(9):e106719 [PMID: 25244253]
  39. Electroencephalogr Clin Neurophysiol. 1994 May;92(3):204-14 [PMID: 7514990]
  40. J Assoc Res Otolaryngol. 2016 Apr;17(2):133-43 [PMID: 26920344]
  41. Neurobiol Aging. 2014 Nov;35(11):2526-2540 [PMID: 24908166]
  42. J Neurosci. 2012 Oct 10;32(41):14156-64 [PMID: 23055485]
  43. J Acoust Soc Am. 2019 Nov;146(5):3743 [PMID: 31795705]
  44. Electroencephalogr Clin Neurophysiol. 1974 Apr;36(4):415-24 [PMID: 4140069]
  45. Exp Brain Res. 2000 Jun;132(4):445-56 [PMID: 10912825]
  46. J Acoust Soc Am. 2003 Jul;114(1):307-21 [PMID: 12880043]
  47. J Neurophysiol. 1999 Nov;82(5):2346-57 [PMID: 10561410]
  48. J Acoust Soc Am. 1991 May;89(5):2421-9 [PMID: 1861002]
  49. Hear Res. 2014 May;311:36-48 [PMID: 24445149]
  50. Eur J Neurosci. 2009 Nov;30(9):1779-89 [PMID: 19840111]
  51. Hear Res. 2014 Jan;307:53-64 [PMID: 23938209]
  52. J Neurosci Methods. 2017 Nov 1;291:101-112 [PMID: 28807860]
  53. Hear Res. 2019 Oct;382:107779 [PMID: 31505395]
  54. J Neurosurg Pediatr. 2018 Jul;22(1):37-46 [PMID: 29676681]
  55. Psychophysiology. 2010 Mar 1;47(2):236-46 [PMID: 19824950]
  56. Cereb Cortex. 2001 Oct;11(10):946-53 [PMID: 11549617]
  57. J Assoc Res Otolaryngol. 2017 Aug;18(4):635-648 [PMID: 28447225]
  58. Neuroimage. 2021 Feb 1;226:117545 [PMID: 33186711]
  59. Electroencephalogr Clin Neurophysiol. 1975 Nov;39(5):465-72 [PMID: 52439]
  60. Sci Rep. 2017 Nov 30;7(1):16687 [PMID: 29192170]
  61. Hear Res. 2015 May;323:68-80 [PMID: 25660195]
  62. Hear Res. 2010 Sep 1;268(1-2):60-6 [PMID: 20457239]
  63. Atten Percept Psychophys. 2019 May;81(4):1020-1033 [PMID: 30565097]
  64. Neuroimage. 2021 May 1;231:117866 [PMID: 33592244]
  65. Percept Mot Skills. 2001 Feb;92(1):99-106 [PMID: 11322612]
  66. J Neurosurg. 1981 Jun;54(6):740-50 [PMID: 7017075]
  67. Nat Commun. 2016 Mar 24;7:11070 [PMID: 27009409]
  68. J Neurophysiol. 2017 Feb 1;117(2):594-603 [PMID: 27832606]
  69. Electroencephalogr Clin Neurophysiol. 1975 Feb;38(2):113-9 [PMID: 45941]
  70. J Am Assoc Lab Anim Sci. 2007 Jan;46(1):20-2 [PMID: 17203911]
  71. J Neurosci Methods. 2020 Dec 1;346:108906 [PMID: 32822693]
  72. J Neurophysiol. 2016 Nov 1;116(5):2125-2139 [PMID: 27512021]
  73. Neuroimage. 2012 Aug 15;62(2):774-81 [PMID: 22248573]
  74. J Neurosci Methods. 2004 Mar 15;134(1):9-21 [PMID: 15102499]
  75. Neuroimage. 2019 Dec;203:116185 [PMID: 31520743]

Grants

  1. R01 DC013315/NIDCD NIH HHS
  2. R01 DC017141/NIDCD NIH HHS
  3. RF1 MH114223/NIMH NIH HHS

MeSH Term

Acoustic Stimulation
Animals
Auditory Cortex
Electroencephalography
Guinea Pigs
Phonetics
Pitch Perception
Speech Perception

Word Cloud

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