Abstract
This study investigated to which extent the primary auditory cortex of young normal-hearing and mild hearing-impaired aged animals is able to maintain invariant representation of critical temporal-modulation features when sounds are submitted to degradations of fine spectro-temporal acoustic details. This was achieved by recording ensemble of cortical responses to conspecific vocalizations in guinea pigs with either normal hearing or mild age-related sensorineural hearing loss. The vocalizations were degraded using a tone vocoder. The neuronal responses and their discrimination capacities (estimated by mutual information) were analyzed at single recording and population levels. For normal-hearing animals, the neuronal responses decreased as a function of the number of the vocoder frequency bands, so did their discriminative capacities at the single recording level. However, small neuronal populations were found to be robust to the degradations induced by the vocoder. Similar robustness was obtained when broadband noise was added to exacerbate further the spectro-temporal distortions produced by the vocoder. A comparable pattern of robustness to degradations in fine spectro-temporal details was found for hearing-impaired animals. However, the latter showed an overall decrease in neuronal discrimination capacities between vocalizations in noisy conditions. Consistent with previous studies, these results demonstrate that the primary auditory cortex maintains robust neural representation of temporal envelope features for communication sounds under a large range of spectro-temporal degradations.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alain C, Roye A, Salloum C (2014) Effects of age-related hearing loss and background noise on neuromagnetic activity from auditory cortex. Front Syst Neurosci 8:8
Apoux F, Healy EW (2011) Relative contribution of target and masker temporal fine structure to the unmasking of consonants in noise. J Acoust Soc Am 130(6):4044–4052. https://doi.org/10.1121/1.3652888
Apoux F, Yoho SE, Youngdahl CL, Healy EW (2013) Role and relative contribution of temporal envelope and fine structure cues in sentence recognition by normal-hearing listeners. J Acoust Soc Am 134(3):2205–2212. https://doi.org/10.1121/1.4816413
Baskent D (2006) Speech recognition in normal hearing and sensorineural hearing loss as a function of the number of spectral channels. J Acoust Soc Am 120(5):2908–2925. https://doi.org/10.1121/1.2354017
Belin P, Zatorre RJ, Lafaille P, Ahad P, Pike B (2000) Voice-selective areas in human auditory cortex. Nature 403(6767):309–312. https://doi.org/10.1038/35002078
Bitterman Y, Mukamel R, Malach R, Fried I, Nelken I (2008) Ultra-fine frequency tuning revealed in single neurons of human auditory cortex. Nature 451(7175):197–201. https://doi.org/10.1038/nature06476
Chechik G, Nelken I (2012) Auditory abstraction from spectro-temporal features to coding auditory entities. Proc Natl Acad Sci U S A 109(46):18968–18973. https://doi.org/10.1073/pnas.1111242109
Chechik G, Anderson MJ, Bar-Yosef O, Young ED, Tishby N, Nelken I (2006) Reduction of information redundancy in the ascending auditory pathway. Neuron 51(3):359–368. https://doi.org/10.1016/j.neuron.2006.06.030
Clinard CG, Tremblay KL, Krishnan AR (2010) Aging alters the perception and physiological representation of frequency: evidence from human frequency-following response recordings. Hear Res 264(1–2):48–55. https://doi.org/10.1016/j.heares.2009.11.010
Cotillon-Williams N, Edeline JM (2003) Evoked oscillations in the thalamo-cortical auditory system are present in anesthetized but not in unanesthetized rats. J Neurophysiol 89(4):1968–1984. https://doi.org/10.1152/jn.00728.2002
Ding N, Chatterjee M, Simon JZ (2014) Robust cortical entrainment to the speech envelope relies on the spectro-temporal fine structure. Neuroimage 88:41–46. https://doi.org/10.1016/j.neuroimage.2013.10.054
Drullman R (1995) Temporal envelope and fine structure cues for speech intelligigibility. J Acoust Soc Am 97(1):585–592. https://doi.org/10.1121/1.413112
Dudley H (1939) Remaking speech. J Acoust Soc Am 11(2):169–177. https://doi.org/10.1121/1.1916020
Duquesnoy AJ, Plomp R (1980) Effect of reverberation and noise on the intelligibility of sentences in cases of presbyacusis. J Acoust Soc Am 68(2):537–544. https://doi.org/10.1121/1.384767
Edeline JM, Weinberger NM (1993) Receptive field plasticity in the auditory cortex during frequency discrimination training: selective retuning independent of task difficulty. Behav Neurosci 107(1):82–103. https://doi.org/10.1037/0735-7044.107.1.82
Edeline JM, Dutrieux G, Manunta Y, Hennevin E (2001) Diversity of receptive field changes in auditory cortex during natural sleep. Eur J Neurosci 14(11):1865–1880. https://doi.org/10.1046/j.0953-816x.2001.01821.x
Engineer CT, Perez CA, Chen YH, Carraway RS, Reed AC, Shetake JA, Jakkamsetti V, Chang KQ, Kilgard MP (2008) Cortical activity patterns predict speech discrimination ability. Nat Neurosci 11(5):603–608. https://doi.org/10.1038/nn.2109
Engle JR, Recanzone GH (2013) Characterizing spatial tuning functions of neurons in the auditory cortex of young and aged monkeys: a new perspective on old data. Front Aging Neurosci 4:36. https://doi.org/10.3389/fnagi.2012.00036
Fishbach A, Nelken I, Yeshurun Y (2001) Auditory edge detection: a neural model for physiological and psychoacoustical responses to amplitude transients. J Neurophysiol 85(6):2303–2323
Fitzgibbons PJ, Gordon-Salant S (2010) Age-related differences in discrimination of temporal intervals in accented tone sequences. Hear Res 264(1–2):41–47. https://doi.org/10.1016/j.heares.2009.11.008
Friesen LM, Shannon RV, Baskent D, Wang X (2001) Speech recognition in noise as a function of the number of spectral channels: comparison of acoustic hearing and cochlear implants. J Acoust Soc Am 110(2):1150–1163. https://doi.org/10.1121/1.1381538
Frisina DR, Frisina RD (1997) Speech recognition in noise and presbycusis: relations to possible neural mechanisms. Hear Res 106(1–2):95–104. https://doi.org/10.1016/S0378-5955(97)00006-3
Füllgrabe C (2013) Age-dependent changes in temporal-fine-structure processing in the absence of peripheral hearing loss. Am J Audiol 22(2):313–315. https://doi.org/10.1044/1059-0889(2013/12-0070).
Füllgrabe C, Moore BC (2014) Effects of age and hearing loss on stream segregation based on interaural time differences. J Acoust Soc Am 136(2):EL185–EL191. https://doi.org/10.1121/1.4890201
Füllgrabe C, Moore BC, Stone MA (2015) Age-group differences in speech identification despite matched audiometrically normal hearing: contributions from auditory temporal processing and cognition. Front Aging Neurosci 6:347. https://doi.org/10.3389/fnagi.2014.00347
Gaucher Q, Edeline JM (2015) Stimulus-specific effects of noradrenaline in auditory cortex: implications for the discrimination of communication sounds. J Physiol Lond 593(4):1003–1020. https://doi.org/10.1113/jphysiol.2014.282855
Gaucher Q, Edeline JM, Gourévitch B (2012) How different are the local field potentials and spiking activities? Insights from multi-electrodes arrays. J Physiol Paris 106(3–4):93–103. https://doi.org/10.1016/j.jphysparis.2011.09.006
Gaucher Q, Huetz C, Gourévitch B, Edeline J-M (2013a) Cortical inhibition reduces information redundancy at presentation of communication sounds in the primary auditory cortex. J Neurosci 33(26):10713–10728. https://doi.org/10.1523/JNEUROSCI.0079-13.2013
Gaucher Q, Huetz C, Gourévitch B, Laudanski J, Occelli F, Edeline JM (2013b) How do auditory cortex neurons represent communication sounds ? Hear Res 305:102–112. https://doi.org/10.1016/j.heares.2013.03.011
Gnansia D, Pean V, Meyer B, Lorenzi C (2009) Effects of spectral smearing and temporal fine structure degradation on speech masking release. J Acoust Soc Am 125(6):4023–4033. https://doi.org/10.1121/1.3126344
Gnansia D, Pressnitzer D, Pean V, Meyer B, Lorenzi C (2010) Intelligibility of interrupted and interleaved speech for normal-hearing listeners and cochlear implantees. Hear Res 265(1–2):46–53. https://doi.org/10.1016/j.heares.2010.02.012
Gourévitch B, Edeline JM (2011) Age-related changes in the guinea pig auditory cortex: relationship with peripheral changes and comparison with tone-induced hearing loss. Eur J Neurosci 34(12):1953–1965. https://doi.org/10.1111/j.1460-9568.2011.07905.x
Gourévitch B, Doisy T, Avillac M, Edeline JM (2009) Follow-up of latency and threshold shifts of auditory brainstem responses after single and interrupted acoustic trauma in guinea pig. Brain Res 1304:66–79. https://doi.org/10.1016/j.brainres.2009.09.041
Grose JH, Mamo SK (2010) Processing of temporal fine structure as a function of age. Ear Hear 31(6):755–760. https://doi.org/10.1097/AUD.0b013e3181e627e7
Grose JH, Mamo SK (2012) Frequency modulation detection as a measure of temporal processing: age-related monaural and binaural effects. Hear Res 294(1–2):49–54. https://doi.org/10.1016/j.heares.2012.09.007
Grose JH, Mamo SK, Buss E, Hall JW (2015) Temporal processing deficits in middle age. Am J Audiol 24(2):91–93. https://doi.org/10.1044/2015_AJA-14-0053
He NJ, Mills JH, Dubno JR (2007) Frequency modulation detection: effects of age, psychophysical method, and modulation waveform. J Acoust Soc Am 122(1):467–477. https://doi.org/10.1121/1.2741208
He NJ, Mills JH, Ahlstrom JB, Dubno JR (2008) Age-related differences in the temporal modulation transfer function with pure-tone carriers. J Acoust Soc Am 124(6):3841–3849. https://doi.org/10.1121/1.2998779
Heil P (1997a) Auditory cortical onset responses revisited. I. First-spike timing. J Neurophysiol 77(5):2616–2641
Heil P (1997b) Auditory cortical onset responses revisited. II. Response strength. J Neurophysiol 77(5):2642–2660
Hohmann V (2002) Frequency analysis and synthesis using a Gammatone filterbank. Acust Acta Acust 88:433–442
Hopkins K, Moore BC (2011) The effects of age and cochlear hearing loss on temporal fine structure sensitivity, frequency selectivity, and speech reception in noise. J Acoust Soc Am 130(1):334–349. https://doi.org/10.1121/1.3585848
Huetz C, Philibert B, Edeline JM (2009) A spike-timing code for discriminating conspecific vocalizations in the thalamocortical system of anesthetized and awake guinea pigs. J Neurosci 29(2):334–350. https://doi.org/10.1523/JNEUROSCI.3269-08.2009
Huetz C, Gourévitch B, Edeline J-M (2011) Neural codes in the thalamocortical auditory system: from artificial stimuli to communication sounds. Hear Res 271(1-2):147–158. https://doi.org/10.1016/j.heares.2010.01.010
Ince RAA, Panzeri S, Kayser C (2013) Neural codes formed by small and temporally precise populations in auditory cortex. J Neurosci 33(46):18277–18287. https://doi.org/10.1523/JNEUROSCI.2631-13.2013
King A, Hopkins K, Plack CJ (2014) The effects of age and hearing loss on interaural phase difference discrimination. J Acoust Soc Am 135(1):342–351. https://doi.org/10.1121/1.4838995
Laudanski J, Edeline JM, Huetz C (2012) Differences between spectro-temporal receptive fields derived from artificial and natural stimuli in the auditory cortex. PLoS One 7(11):e50539. https://doi.org/10.1371/journal.pone.0050539
Liégeois-Chauvel C, Lorenzi C, Trébuchon A, Régis J, Chauvel P (2004) Temporal envelope processing in the human left and right auditory cortices. Cereb Cortex 14(7):731–740. https://doi.org/10.1093/cercor/bhh033
Liu RC, Schreiner CE (2007) Auditory cortical detection and discrimination correlates with communicative significance. PLoS Biol 5(7):e173. https://doi.org/10.1371/journal.pbio.0050173
Lorenzi C, Gilbert G, Carn H, Garnier S, Moore BCJ (2006) Speech perception problems of the hearing impaired reflect inability to use temporal fine structure. Proc Natl Acad Sci U S A 103(49):18866–18869. https://doi.org/10.1073/pnas.0607364103
Lutman ME, Gatehouse S, Worthington AG (1991) Frequency resolution as a function of hearing threshold and age. J Acoust Soc Am 89(1):320–328. https://doi.org/10.1121/1.400513
Machens CK, Wehr MS, Zador AM (2004) Linearity of cortical receptive fields measured with natural sounds. J Neurosci 24(5):1089–1100. https://doi.org/10.1523/JNEUROSCI.4445-03.2004
Manunta Y, Edeline JM (1999) Effects of noradrenaline on frequency tuning of auditory cortex neurons during wakefulness and slow-wave sleep. Eur J Neurosci 11(6):2134–2150. https://doi.org/10.1046/j.1460-9568.1999.00633.x
Massaux A, Edeline JM (2003) Bursts in the medial geniculate body: a comparison between anesthetized and unanesthetized states in guinea-pig. Exp Brain Res 153(4):573–578. https://doi.org/10.1007/s00221-003-1516-3
Massaux A, Dutrieux G, Cotillon-Williams N, Manunta Y, Edeline JM (2004) Auditory thalamus bursts in anesthetized and non-anesthetized states: contribution to functional properties. J Neurophysiol 91(5):2117–2134. https://doi.org/10.1152/jn.00970.2003
Mesgarani N, David SV, Fritz JB, Shamma SA (2014) Mechanisms of noise robust representation of speech in primary auditory cortex. Proc Natl Acad Sci U S A 111(18):6792–6797. https://doi.org/10.1073/pnas.1318017111
Moore BC, Hafter ER, Glasberg BR (1996) The probe-signal method and auditory-filter shape: results from normal- and hearing-impaired subjects. J Acoust Soc Am 99(1):542–552. https://doi.org/10.1121/1.414512
Moore BC, Glasberg BR, Stoev M, Füllgrabe C, Hopkins K (2012a) The influence of age and high-frequency hearing loss on sensitivity to temporal fine structure at low frequencies (L). J Acoust Soc Am 131(2):1003–1006. https://doi.org/10.1121/1.3672808
Moore BC, Vickers DA, Mehta A (2012b) The effects of age on temporal fine structure sensitivity in monaural and binaural conditions. Int J Audiol 51(10):715–721. https://doi.org/10.3109/14992027.2012.690079
Nagarajan SS, Cheung SW, Bedenbaugh P, Beitel RE, Schreiner CE, Merzenich MM (2002) Representation of spectral and temporal envelope of twitter vocalizations in common marmoset primary auditory cortex. J Neurophysiol 87(4):1723–1737. https://doi.org/10.1152/jn.00632.2001
Nelson PB, Jin SH, Carney AE, Nelson DA (2003) Understanding speech in modulated interference : cochlear implant users and normal-hearing listenners. J Acoust Soc Am 115:2286–2294
Occelli F, Suied C, Pressnitzer D, Edeline JM, Gourévitch B (2016) A neural substrate for rapid timbre recognition? Neural and behavioral discrimination of very brief acoustic vowels. Cereb Cortex 26(6):2483–2496. https://doi.org/10.1093/cercor/bhv071
Overton JA, Recanzone GH (2016) Effects of aging on the response of single neurons to amplitude-modulated noise in primary auditory cortex of rhesus macaque. J Neurophysiol 115(6):2911–2923. https://doi.org/10.1152/jn.01098.2015
Paraouty N, Lorenzi C (2017) Using individual differences to assess modulation-processing mechanisms and age effects. Hear Res 344:38–49. https://doi.org/10.1016/j.heares.2016.10.024
Paraouty N, Ewert SD, Wallaert N, Lorenzi C (2016) Interactions between amplitude modulation and frequency modulation processing: effects of age and hearing loss. J Acoust Soc Am 140(1):121–131. https://doi.org/10.1121/1.4955078
Patterson RD (1987) A pulse ribbon model of monaural phase perception. J Acoust Soc Am 82(5):1560–1586. https://doi.org/10.1121/1.395146
Peters RW, Moore BCJ (1992) Auditory filters and aging: filters when auditory thresholds are normal. In: Cazals Y, Demany L, Horner K (eds) Auditory physiology and perception. Pergamon, Oxford, pp 179–185. https://doi.org/10.1016/B978-0-08-041847-6.50026-5
Presacco A, Simon JZ, Anderson S (2016) Evidence of degraded representation of speech in noise, in the aging midbrain and cortex. J Neurophysiol 116(5):2346–2355. https://doi.org/10.1152/jn.00372.2016
Ranasinghe KG, Vrana WA, Matney CJ, Kilgard MP (2012) Neural mechanisms supporting robust discrimination of spectrally and temporally degraded speech. J Assoc Res Otolaryngol 13(4):527–542. https://doi.org/10.1007/s10162-012-0328-1
Rennaker RL, Carey HL, Anderson SE, Sloan AM, Kilgard MP (2007) Anesthesia suppresses nonsynchronous responses to repetitive broadband stimuli. Neuroscience 145(1):357–369. https://doi.org/10.1016/j.neuroscience.2006.11.043
Romanski LM, Averbeck BB (2009) The primate cortical auditory system and neural representation of conspecific vocalizations. Annu Rev Neurosci 32(1):315–346. https://doi.org/10.1146/annurev.neuro.051508.135431
Ross B, Fujioka T, Tremblay KL, Picton TW (2007) Aging in binaural hearing begins in mid-life: evidence from cortical auditory-evoked responses to changes in interaural phase. J Neurosci 27(42):11172–11178. https://doi.org/10.1523/JNEUROSCI.1813-07.2007
Sayles M, Winter IM (2010) Equivalent-rectangular bandwidth of single units in the anaesthetized guinea-pig ventral cochlear nucleus. Hear Res 262(1–2):26–33. https://doi.org/10.1016/j.heares.2010.01.015
Schnupp JW, Hall TM, Kokelaar RF, Ahmed B (2006) Plasticity of temporal pattern codes for vocalization stimuli in primary auditory cortex. J Neurosci 26(18):4785–4795. https://doi.org/10.1523/JNEUROSCI.4330-05.2006
Schoof T, Rosen S (2014) The role of auditory and cognitive factors in understanding speech in noise by normal-hearing older listeners. Front Aging Neurosci 6:307. https://doi.org/10.3389/fnagi.2014.00307
Schvartz KC, Chatterjee M, Gordon-Salant S (2008) Recognition of spectrally degraded phonemes by younger, middle-aged, and older normal-hearing listeners. J Acoust Soc Am 124(6):3972–3988. https://doi.org/10.1121/1.2997434
Sergeyenko Y, Lall K, Liberman MC, Kujawa SG (2013) Age-related cochlear synaptopathy: an early-onset contributor to auditory functional decline. J Neurosci 33(34):13686–13694. https://doi.org/10.1523/JNEUROSCI.1783-13.2013
Shamma S, Lorenzi C (2013) On the balance of envelope and temporal fine structure in the encoding of speech in the early auditory system. J Acoust Soc Am 133(5):2818–2833. https://doi.org/10.1121/1.4795783
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27(3):379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Shannon RV, Zeng FG, Kamath V, Wygonski J, Ekelid M (1995) Speech recognition with primary temporal cues. Science 270(5234):303–304. https://doi.org/10.1126/science.270.5234.303
Sheft S, Ardoint M, Lorenzi C (2008) Speech identification based on temporal fine structure cues. J Acoust Soc Am 124(1):562–575. https://doi.org/10.1121/1.2918540
Sheldon S, Pichora-Fuller MK, Schneider BA (2008) Effect of age, presentation method, and learning on identification of noise-vocoded words. J Acoust Soc Am 123(1):476–488. https://doi.org/10.1121/1.2805676
Smith ZM, Delgutte B, Oxenham AJ (2002) Chimaeric sounds reveal dichotomies in auditory perception. Nature 416(6876):87–90. https://doi.org/10.1038/416087a
Sörös P, Teismann IK, Manemann E, Lütkenhöner B (2009) Auditory temporal processing in healthy aging: a magnetoencephalographic study. BMC Neurosci 10(1):34. https://doi.org/10.1186/1471-2202-10-34
Souza PE, Boike KT (2006) Combining temporal-envelope cues across channels: effects of age and hearing loss. J Speech Lang Hear Res 49(1):138–149. https://doi.org/10.1044/1092-4388(2006/011)
Souza PE, Kitch V (2001) The contribution of amplitude envelope cues to sentence identification in young and aged listeners. Ear Hear 22(2):112–119. https://doi.org/10.1097/00003446-200104000-00004
Stone MA, Füllgrabe C, Mackinnon RC, Moore BCJ (2011) The importance for speech intelligibility of random fluctuations in “steady” background noise. J Acoust Soc Am 130(5):2874–2881. https://doi.org/10.1121/1.3641371
Takahashi GA, Bacon SP (1992) Modulation detection, modulation masking, and speech understanding in noise in the elderly. J Speech Hear Res 35(6):1410–1421. https://doi.org/10.1044/jshr.3506.1410
Ter-Mikaelian M, Semple MN, Sanes DH (2013) Effects of spectral and temporal disruption on cortical encoding of gerbil vocalizations. J Neurophysiol 110(5):1190–1204. https://doi.org/10.1152/jn.00645.2012
Wallace MN, Palmer AR (2008) Laminar differences in the response properties of cells in the primary auditory cortex. Exp Brain Res 184(2):179–191. https://doi.org/10.1007/s00221-007-1092-z
Wallace MN, Rutkowski RG, Palmer AR (2000) Identification and localisation of auditory areas in guinea pig cortex. Exp Brain Res 132(4):445–456. https://doi.org/10.1007/s002210000362
Wallaert N, Moore BC, Lorenzi C (2016) Comparing the effects of age on amplitude modulation and frequency modulation detection. J Acoust Soc Am 139(6):3088–3096. https://doi.org/10.1121/1.4953019
Wallaert N, Moore BC, Ewert SD, Lorenzi C (2017) Sensorineural hearing loss enhances auditory sensitivity and temporal integration for amplitude modulation. J Acoust Soc Am 141(2):971–980. https://doi.org/10.1121/1.4976080
Walton JP, Frisina RD, O’Neill WE (1998) Age-related alteration in processing of temporal sound features in the auditory midbrain of the CBA mouse. J Neurosci 18(7):2764–2776
Whitmal NA, Poissant SF, Freyman RL, Helfer KS (2007) Speech intelligibility in cochlear implant simulations: effects of carrier type, interfering noise, and subject experience. J Acoust Soc Am 122(4):2376–2388. https://doi.org/10.1121/1.2773993
Woolley SM, Gill PR, Theunissen FE (2006) Stimulus-dependent auditory tuning results in synchronous population coding of vocalizations in the songbird midbrain. J Neurosci 26(9):2499–2512. https://doi.org/10.1523/JNEUROSCI.3731-05.2006
Zeng FG, Nie K, Stickney GS, Kong YY, Vongphoe M, Bhargave A, Wei C, Cao K (2005) Speech recognition with amplitude and frequency modulations. Proc Natl Acad Sci 102(7):2293–2298. https://doi.org/10.1073/pnas.0406460102
Acknowledgements
Special thanks to Fabien Lhericel and Céline Dubois for taking care of the guinea pig colony and to Dr. Grégoire Levasseur for helping generating high quality figures.
Funding
This work was supported by grants from the National Research Agency (ANR Blanc2011, HearFin and ANR Blanc2014, Heart) to CL and JME. This work was also supported by ANR-11-0001-02 PSL* and ANR-10-LABX-0087. SS was supported by the Fondation pour la Recherche Médicale (FRM grant number ECO20160736099 to [SS]).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Aushana, Y., Souffi, S., Edeline, JM. et al. Robust Neuronal Discrimination in Primary Auditory Cortex Despite Degradations of Spectro-temporal Acoustic Details: Comparison Between Guinea Pigs with Normal Hearing and Mild Age-Related Hearing Loss. JARO 19, 163–180 (2018). https://doi.org/10.1007/s10162-017-0649-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10162-017-0649-1