Neural Responses and Perceptual Sensitivity to Sound Depend on Sound-Level Statistics.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
12 06 2020
12 06 2020
Historique:
received:
20
11
2019
accepted:
22
05
2020
entrez:
14
6
2020
pubmed:
14
6
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Sensitivity to sound-level statistics is crucial for optimal perception, but research has focused mostly on neurophysiological recordings, whereas behavioral evidence is sparse. We use electroencephalography (EEG) and behavioral methods to investigate how sound-level statistics affect neural activity and the detection of near-threshold changes in sound amplitude. We presented noise bursts with sound levels drawn from distributions with either a low or a high modal sound level. One participant group listened to the stimulation while EEG was recorded (Experiment I). A second group performed a behavioral amplitude-modulation detection task (Experiment II). Neural activity depended on sound-level statistical context in two different ways. Consistent with an account positing that the sensitivity of neurons to sound intensity adapts to ambient sound level, responses for higher-intensity bursts were larger in low-mode than high-mode contexts, whereas responses for lower-intensity bursts did not differ between contexts. In contrast, a concurrent slow neural response indicated prediction-error processing: The response was larger for bursts at intensities that deviated from the predicted statistical context compared to those not deviating. Behavioral responses were consistent with prediction-error processing, but not with neural adaptation. Hence, neural activity adapts to sound-level statistics, but fine-tuning of perceptual sensitivity appears to involve neural prediction-error responses.
Identifiants
pubmed: 32533068
doi: 10.1038/s41598-020-66715-1
pii: 10.1038/s41598-020-66715-1
pmc: PMC7293331
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
9571Subventions
Organisme : CIHR
ID : MOP133450
Pays : Canada
Références
Wark, B., Lundstrom, B. N. & Fairhall, A. Sensory adaptation. Current Opinion in Neurobiology 17, 423–429 (2007).
pubmed: 17714934
pmcid: 2084204
doi: 10.1016/j.conb.2007.07.001
Kluender, K. R., Stilp, C. E. & Kiefte, M. In Vowel Inherent Spectral Change (eds. Geoffrey Stewart Morrison & Peter F. Assmann) 117–151 (Springer, 2013).
Lewicki, M. S. Efficient coding of natural sounds. Nature 5, 356–363 (2002).
Whitmire, C. J. & Stanley, G. B. Rapid Sensory Adaptation Redux: A Circuit Perspective. Neuron 92, 298–315 (2016).
pubmed: 27764664
pmcid: 5076890
doi: 10.1016/j.neuron.2016.09.046
Laughlin, S. A simple coding procedure enhances a neuron’s information capacity. Zeitschrift fur Naturforschung. C, Journal of biosciences 36, 910–912 (1981).
Viemeister, N. F. Intensity coding and the dynamic range problem. Hearing Research 34, 267–274 (1988).
pubmed: 3170367
doi: 10.1016/0378-5955(88)90007-X
Furman, A. C., Kujawa, S. G. & Liberman, M. C. Noise-induced cochlear neuropathy is selective for fibers with low spontaneous rates. Journal of Neurophysiology 110, 577–586 (2013).
pubmed: 23596328
pmcid: 3742994
doi: 10.1152/jn.00164.2013
Taberner, A. M. & Liberman, M. C. Response properties of single auditory nerve fibers in the mouse. Journal of Neurophysiology 93, 557–569 (2005).
pubmed: 15456804
doi: 10.1152/jn.00574.2004
Evans, E. F. In Neuronal Mechanisms in Hearing (eds. J. Syka & L. Aitkin) 69–85 (Plenum Press, 1981).
Dean, I., Harper, N. S. & McAlpine, D. Neural population coding of sound level adapts to stimulus statistics. Nature Neuroscience 8, 1684–1689 (2005).
pubmed: 16286934
doi: 10.1038/nn1541
Robinson, B. L., Harper, N. S. & McAlpine, D. Meta-adaptation in the auditory midbrain under cortical influence. Nature Communications 7, 13442 (2016).
pubmed: 27883088
pmcid: 5123015
doi: 10.1038/ncomms13442
Salinas, E. & Thier, P. Gain Modulation: A Major Computational Principle of the Central Nervous System. Neuron 27, 15–21 (2000).
pubmed: 10939327
doi: 10.1016/S0896-6273(00)00004-0
Robinson, B. L. & McAlpine, D. Gain control mechanisms in the auditory pathway. Current Opinion in Neurobiology 19, 402–407 (2009).
pubmed: 19665367
doi: 10.1016/j.conb.2009.07.006
Dahmen, J. C., Keating, P., Nodal, F. R., Schulz, A. L. & King, A. J. Adaptation to Stimulus Statistics in the Perception and Neural Representation of Auditory Space. Neuron 66, 937–948 (2010).
pubmed: 20620878
pmcid: 2938477
doi: 10.1016/j.neuron.2010.05.018
Herrmann, B., Schlichting, N. & Obleser, J. Dynamic Range Adaptation to Spectral Stimulus Statistics in Human Auditory Cortex. The Journal of Neuroscience 34, 327–331 (2014).
pubmed: 24381293
pmcid: 3866491
doi: 10.1523/JNEUROSCI.3974-13.2014
Nagel, K. I. & Doupe, A. J. Temporal Processing and Adaptation in the Songbird Auditory Forebrain. Neuron 51, 845–859 (2006).
pubmed: 16982428
doi: 10.1016/j.neuron.2006.08.030
Hildebrandt, K. J., Benda, J. & Hennig, R. M. Multiple Arithmetic Operations in a Single Neuron: The Recruitment of Adaptation Processes in the Cricket Auditory Pathway Depends on Sensory Context. The Journal of Neuroscience 31, 14142–14150 (2011).
pubmed: 21976499
pmcid: 6623665
doi: 10.1523/JNEUROSCI.2556-11.2011
Wen, B., Wang, G. I., Dean, I. & Delgutte, B. Dynamic Range Adaptation to Sound Level Statistics in the Auditory Nerve. The Journal of Neuroscience 29, 13797–13808 (2009).
pubmed: 19889991
pmcid: 2774902
doi: 10.1523/JNEUROSCI.5610-08.2009
Wen, B., Wang, G. I., Dean, I. & Delgutte, B. Time course of dynamic range adaptation in the auditory nerve. Journal of Neurophysiology 108, 69–82 (2012).
pubmed: 22457465
pmcid: 3434618
doi: 10.1152/jn.00055.2012
Dean, I., Robinson, B. L., Harper, N. S. & McAlpine, D. Rapid Neural Adaptation to Sound Level Statistics. The Journal of Neuroscience 28, 6430–6438 (2008).
pubmed: 18562614
pmcid: 6670892
doi: 10.1523/JNEUROSCI.0470-08.2008
Herrmann, B., Maess, B. & Johnsrude, I. S. Aging Affects Adaptation to Sound-Level Statistics in Human Auditory Cortex. The Journal of Neuroscience 38, 1989–1999 (2018).
pubmed: 29358362
pmcid: 6705886
doi: 10.1523/JNEUROSCI.1489-17.2018
Rocchi, F. & Ramachandran, R. Neuronal adaptation to sound statistics in the inferior colliculus of behaving macaques does not reduce the effectiveness of the masking noise. Journal of Neurophysiology 120, 2819–2833 (2018).
pubmed: 30256735
pmcid: 6337033
doi: 10.1152/jn.00875.2017
Näätänen, R., Paavilainen, P., Alho, K., Reinikainen, K. & Sams, M. Do event-related potentials reveal the mechanism of the auditory sensory memory in the human brain? Neuroscience Letters 98, 217–221 (1989).
pubmed: 2710416
doi: 10.1016/0304-3940(89)90513-2
Paavilainen, P., Alho, K., Reinikainen, K., Sams, M. & Näätänen, R. Right hemisphere dominance of different mismatch negativities. Electroencephalography and clinical Neurophysiology 78, 466–479 (1991).
pubmed: 1712282
doi: 10.1016/0013-4694(91)90064-B
Schröger, E. & Winkler, I. Presentation rate and magnitude of stimulus deviance effects on human pre-attentive change detection. Neuroscience Letters 193, 185–188 (1995).
pubmed: 7478179
doi: 10.1016/0304-3940(95)11696-T
Tervaniemi, M. et al. Test-retest reliability of mismatch negativity for duration, frequency and intensity changes. Clinical Neurophysiology 110, 1388–1393 (1999).
pubmed: 10454274
doi: 10.1016/S1388-2457(99)00108-X
Winkler, I., Denham, S. L. & Nelken, I. Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends in Cognitive Sciences 13, 532–540 (2009).
pubmed: 19828357
doi: 10.1016/j.tics.2009.09.003
Friston, K. J. A Theory of Cortical Response. Philosophical Transactions: Biological Sciences 360, 815–836 (2005).
doi: 10.1098/rstb.2005.1622
Malmierca, M. S., Anderson, L. A. & Antunes, F. M. The cortical modulation of stimulus-specific adaptation in the auditory midbrain and thalamus: a potential neuronal correlate for predictive coding. Frontiers in Systems Neuroscience 9, Articles 19 (2015).
doi: 10.3389/fnsys.2015.00019
Parras, G. G. et al. Neurons along the auditory pathway exhibit a hierarchical organization of prediction error. Nature Communications 8, 2148 (2017).
pubmed: 29247159
pmcid: 5732270
doi: 10.1038/s41467-017-02038-6
Bakay, W. M. H., Anderson, L. A., Garcia-Lazaro, J. A., McAlpine, D. & Schaette, R. Hidden hearing loss selectively impairs neural adaptation to loud sound environments. Nature Communications 9, 4298 (2018).
pubmed: 30327471
pmcid: 6191434
doi: 10.1038/s41467-018-06777-y
Duque, D., Wang, X., Nieto-Diego, J., Krumbholz, K. & Malmierca, M. S. Neurons in the inferior colliculus of the rat show stimulus-specific adaptation for frequency, but not for intensity. Scientific Reports 6, 24114 (2016).
pubmed: 27066835
pmcid: 4828641
doi: 10.1038/srep24114
Simpson, A. J. R., Harper, N. S., Reiss, J. D. & McAlpine, D. Selective Adaptation to “Oddball” Sounds by the Human Auditory System. The Journal of Neuroscience 2014, 1963–1969 (2014).
doi: 10.1523/JNEUROSCI.4274-13.2013
Schwent, V. L., Hillyard, S. A. & Galambos, R. Selective attention and the auditory vertex potential. I. Effects of stimulus delivery rate. Electroencephalography and Clinical Neurophysiology 40, 604–614 (1976).
pubmed: 57046
doi: 10.1016/0013-4694(76)90135-8
de Boer, J. & Krumbholz, K. Auditory Attention Causes Gain Enhancement and Frequency Sharpening at Successive Stages of Cortical Processing—Evidence from Human Electroencephalography. Journal of Cognitive Neuroscience 30, 785–798 (2018).
pubmed: 29488851
doi: 10.1162/jocn_a_01245
Polich, J., Aung, M. & Dalessio, D. J. Long Latency Auditory Evoked Potentials: Intensity, Inter-Stimulus Interval, and Habituation. The Pavlovian Journal of Biological Science 23, 35–40 (1988).
pubmed: 3357711
Briley, P. M. & Krumbholz, K. The specificity of stimulus-specific adaptation in human auditory cortex increases with repeated exposure to the adapting stimulus. Journal of Neurophysiology 110, 2679–2688 (2013).
pubmed: 24047909
pmcid: 3882815
doi: 10.1152/jn.01015.2012
Lanting, C. P., Briley, P. M., Summer, C. J. & Krumbholz, K. Mechanisms of adaptation in human auditory cortex. Journal of Neurophysiology 110, 973–983 (2013).
pubmed: 23719212
pmcid: 3742970
doi: 10.1152/jn.00547.2012
Laffont, F. et al. Effects of age on auditory evoked responses (AER) and augmenting-reducing. Clinical Neurophysiology 19, 15–23 (1989).
pubmed: 2716728
doi: 10.1016/S0987-7053(89)80081-4
Picton, T. W., Woods, D. L. & Proulx, G. B. Human auditory sustained potentials. II. Stimulus relationships. Electroencephalography and clinical Neurophysiology 45, 198–210 (1978).
pubmed: 78830
doi: 10.1016/0013-4694(78)90004-4
Davis, H., Mast, T., Yoshie, N. & Zerlin, S. The slow response of the human cortex to auditory stimuli: Recovery process. Electroencephalography and Clinical Neurophysiology 21, 105–113 (1966).
pubmed: 4162003
doi: 10.1016/0013-4694(66)90118-0
Picton, T. W., John, S. M., Dimitrijevic, A. & Purcell, D. W. Human auditory steady-state responses. International Journal of Audiology 42, 177–219 (2003).
pubmed: 12790346
doi: 10.3109/14992020309101316
Näätänen, R. & Picton, T. W. The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 24, 375–425 (1987).
pubmed: 3615753
doi: 10.1111/j.1469-8986.1987.tb00311.x
Malmierca, M. S., Cristaudo, S., Pérez-González, D. & Covey, E. Stimulus-Specific Adaptation in the Inferior Colliculus of the Anesthetized Rat. The Journal of Neuroscience 29, 5483–5493 (2009).
pubmed: 19403816
pmcid: 2715893
doi: 10.1523/JNEUROSCI.4153-08.2009
Herrmann, B., Parthasarathy, A., Han, E. X., Obleser, J. & Bartlett, E. L. Sensitivity of rat inferior colliculus neurons to frequency distributions. Journal of Neurophysiology 114, 2941–2954 (2015).
pubmed: 26354316
pmcid: 4737421
doi: 10.1152/jn.00555.2015
Malmierca, M. S., Sanchez-Vives, M. V., Escera, C. & Bendixen, A. Neuronal adaptation, novelty detection and regularity encoding in audition. Frontiers in Systems Neuroscience 8, Article 111 (2014).
pubmed: 25009474
Farley, B. J., Quirk, M. C., Doherty, J. J. & Christian, E. P. Stimulus-Specific Adaptation in Auditory Cortex Is an NMDA-Independent Process Distinct from the Sensory Novelty Encoded by the Mismatch Negativity. The Journal of Neuroscience 30, 16475–16484 (2010).
pubmed: 21147987
pmcid: 6634869
doi: 10.1523/JNEUROSCI.2793-10.2010
Watkins, P. V. & Barbour, D. L. Specialized neuronal adaptation for preserving input sensitivity. Nature Neuroscience 11, 1259–1261 (2008).
pubmed: 18820690
doi: 10.1038/nn.2201
Natan, R. G. et al. Complementary control of sensory adaptation by two types of cortical interneurons. eLife 4, e09868 (2015).
pubmed: 26460542
pmcid: 4641469
doi: 10.7554/eLife.09868
Silver, R. A. Neuronal arithmetic. Nature Reviews Neuroscience 11, 474–489 (2010).
pubmed: 20531421
pmcid: 4750293
doi: 10.1038/nrn2864
Isaacson, J. S. & Scanziani, M. How Inhibition Shapes Cortical Activity. Neuron 72, 231–243 (2011).
pubmed: 22017986
pmcid: 3236361
doi: 10.1016/j.neuron.2011.09.027
Blackwell, J. M. & Geffen, M. N. Progress and challenges for understanding the function of cortical microcircuits in auditory processing. Nature Communications 8, 2165 (2017).
pubmed: 29255268
pmcid: 5735136
doi: 10.1038/s41467-017-01755-2
Schröger, E. Mismatch Negativity: A Microphone into Auditory Memory. Journal of Psychophysiology 21, 138–146 (2007).
doi: 10.1027/0269-8803.21.34.138
Maess, B., Jacobsen, T., Schröger, E. & Friederici, A. D. Localizing pre-attentive auditory memory-based comparison: Magnetic mismatch negativity to pitch change. NeuroImage 37, 561–571 (2007).
pubmed: 17596966
doi: 10.1016/j.neuroimage.2007.05.040
Willmore, B. D. B., Cooke, J. E. & King, A. J. Hearing in noisy environments: noise invariance and contrast gain control. The Journal of Physiology 592, 3371–3381 (2014).
pubmed: 24907308
pmcid: 4229334
doi: 10.1113/jphysiol.2014.274886
Houtgast, T. Psychophysical Evidence for Lateral Inhibition in Hearing. The Journal of the Acoustical Society of America 51, 1885–1894 (1972).
pubmed: 4339849
doi: 10.1121/1.1913048
Zeng, F.-G., Turner, C. W. & Relkin, E. M. Recovery from prior stimulation II: Effects upon intensity discrimination. Hearing Research 55, 223–230 (1991).
pubmed: 1757290
doi: 10.1016/0378-5955(91)90107-K
Jesteadt, W., Bacon, S. P. & Lehman, J. R. Forward masking as a function of frequency, masker level, and signal delay. The Journal of the Acoustical Society of America 71, 950–962 (1982).
pubmed: 7085983
doi: 10.1121/1.387576
Herrmann, B. & Johnsrude, I. S. Attentional State Modulates the Effect of an Irrelevant Stimulus Dimension on. Perception. Journal of Experimental Psychology: Human Perception and Performance 44, 89–105 (2018).
pubmed: 28447846
doi: 10.1037/xhp0000432
Herrmann, B. & Johnsrude, I. S. Neural signatures of the processing of temporal patterns in sound. The Journal of Neuroscience 38, 5466–5477 (2018).
pubmed: 29773757
doi: 10.1523/JNEUROSCI.0346-18.2018
Makeig, S., Bell, A. J., Jung, T.-P. & Sejnowski, T. J. in Advances in Neural Information Processing Systems Vol. 8 (eds D. Touretzky, M. Mozer, & M. Hasselmo) (MIT Press, 1996).
Bell, A. J. & Sejnowski, T. J. An information maximization approach to blind separation and blind deconvolution. Neural Computation 7, 1129–1159 (1995).
pubmed: 7584893
doi: 10.1162/neco.1995.7.6.1129
Oostenveld, R., Fries, P., Maris, E. & Schoffelen, J. M. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Computational Intelligence and Neuroscience 2011, Article ID 156869 (2011).
doi: 10.1155/2011/156869
Smulders, F. T. Y. Simplifying jackknifing of ERPs and getting more out of it: Retrieving estimates of participants’ latencies. Psychophysiology 47, 387–392 (2010).
pubmed: 20003147
doi: 10.1111/j.1469-8986.2009.00934.x
Bendixen, A. & Andersen, S. K. Measuring target detection performance in paradigms with high event rates. Clinical Neurophysiology 124, 928–940 (2013).
pubmed: 23266090
doi: 10.1016/j.clinph.2012.11.012
Rosenthal, R. & Rubin, D. B. requivalent: A Simple Effect Size Indicator. Psychological Methods 8, 492–496 (2003).
pubmed: 14664684
doi: 10.1037/1082-989X.8.4.492
Masson, M. E. J. & Loftus, G. R. Using confidence intervals for graphically based data interpretation. Canadian Journal of Experimental Psychology and Aging 57, 203–220 (2003).
doi: 10.1037/h0087426
Genovese, C. R., Lazar, N. A. & Nichols, T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 15, 870–878 (2002).
pubmed: 11906227
doi: 10.1006/nimg.2001.1037
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B 57, 289–300 (1995).