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Robust Neuronal Discrimination in Primary Auditory Cortex

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Robust Neuronal Discrimination in Primary Auditory Cortex 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 Yonane Aushana, Samira Souffi, Jean-Marc Edeline, Christian Lorenzi, Chloé Huetz To cite this version: Yonane Aushana, Samira Souffi, Jean-Marc Edeline, Christian Lorenzi, Chloé Huetz. Robust Neu- ronal 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. Journal of the Association for Research in Otolaryngology, Springer Verlag, 2018, 19 (2), pp.163-180. 10.1007/s10162-017-0649-1. hal-02111943 HAL Id: hal-02111943 https://hal.archives-ouvertes.fr/hal-02111943 Submitted on 26 Apr 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Journal of the Association for Research in Otolaryngology 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 --Manuscript Draft-- Manuscript Number: JARO-D-17-00039R3 Full Title: 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 Article Type: Original Article Keywords: vocoder, envelope, fine structure, electrophysiology, auditory cortex, neural discrimination performance, spike-timing Corresponding Author: Jean-Marc EDELINE, PhD Neuro-PSI UMR CNRS 9197 ORSAY, FRANCE Corresponding Author Secondary Information: Corresponding Author's Institution: Neuro-PSI UMR CNRS 9197 Corresponding Author's Secondary Institution: First Author: Yonane Aushana First Author Secondary Information: Order of Authors: Yonane Aushana Samira Souffi Jean-Marc EDELINE, PhD Christian Lorenzi Chloe Huetz Order of Authors Secondary Information: Funding Information: Agence Nationale de la Recherche Pr Christian Lorenzi (ANR-11-0001-02) Agence Nationale de la Recherche Pr Christian Lorenzi (ANR-10-LABX-0087) 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 Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation range of spectro-temporal degradations. Powered by Editorial Manager® and ProduXion Manager® from Aries Systems Corporation Cover Letter Orsay, November 9th, 2017 Dear Editor in Chief, Dear Paul, Dear Associate Editor, Please find on the website a revised version of our MS JARO-D-17-00039R1 that we re-submit for publication to JARO as research article. We have taken into account the reviewers comments and have changed our MS accordingly. All the changes are in RED in the new MS for the version named “Aushana et al 09112017_RED” and we also provide a clean version in black “Aushana et al 09112017_B&W”. Best regards, Yonane Aushana, Samira Souffi, Jean-Marc Edeline, Christian Lorenzi, Chloé Huetz Response to Reviewer Comments Reviewer #1: The manuscript is very much improved. I am reasonably happy that they caveat their results reasonably. I still have a slight issue with the terminology of 'discrimination' - which is used throughout the manuscript with respect to the mutual-information analysis. My worry is that this term implies perceptual discrimination ability, and that the limitations of the stimulus - the small number and obvious differences in basic things like onset latency - make it difficult to generalise to perceptual discrimination of vocalisations. It would be nice to caveat that further. We agree with the reviewer and we clarified what should be understood by the word “discrimination”. We have added a small paragraph on page 19 to clarify this point. In brief, this term was only used to point out that primary auditory cortex neurons are able to display different responses, in terms of temporal spike patterns, at presentation of set of stimuli. This term could be considered as ambiguous so we want to make it clear that our results do not suggest that guinea pigs discriminate between the original or the vocoded vocalizations. Animal groupings are improved but still not clear. P6L44 "Based on the ABR, two groups of animals were separated". Yet the only criteria given for splitting is age. It is clear from figure 2A that there were differences in ABR thresholds between the groups, but no indication of how ABR was a basis for separation. That could only be the case here if there were no overlap at all in the ABR thresholds of individuals in the two groups - is this the case? If so, and ABR was indeed part of the separating into groups then that criteria should be specified. I would guess that in practice they split the groups on age, and there was a group difference in the ABRs. That is OK - but they need to be clear about it. Also, this would amount to an uncontrolled confound of hearing loss age - which needs discussing. If there IS any overlap in the ABRs then it would be interesting if there were guinea-pigs of different ages with similar audiograms. The reviewer is correct: We have used animals of two ages and when looking at their ABR, they can be classified as normal hearing vs. aged-related hearing-loss. We show in the supplementary figure below that there is very little overlap between the two groups. We specified this point in the method section (page 6) and would like to add the figure as supplementary material. Audiograms of the young normal-hearing (NH, black lines) and mild age-related hearing loss (mARHL, red lines) animals. Typos P14 L10 audiogram -> audiograms P19 L46 "Unknown is what will be" grammar. The typos were corrected, thank you. Reviewer #2: The revision addresses all of my concerns from the original submission. Minor concerns: Title: The word "or" in the title should be "and", since it is a comparison. The title was corrected, thank you. Abstract: First sentence: The word "young" should be inserted before "normal hearing" and the word "aged" (or some variant) should be inserted before "hearing-impaired". Introduction, page 3, line 32: "i.e., a frequency modulated (FM) carrier" is not correct in general, and especially so in this project, where the synthesized carrier is constant frequency. These two corrections were made, thank you. Manuscript Click here to download Manuscript MS_Aushana-et-al- 28_11_17.docx Click here to view linked References 1 2 Robust neuronal discrimination in primary auditory cortex despite degradations of 3 4 spectro-temporal acoustic details: comparison between guinea pigs with normal hearing 5 and mild age-related hearing loss 6 7 8 9 10 Yonane Aushana 1,2, Samira Souffi 1,2, Jean-Marc Edeline 1,2 11 3 1,2 12 Christian Lorenzi , Chloé Huetz 13 14 15 Paris-Saclay Institute of Neurosciences (Neuro-PSI) 16 Department Cognition and Behavior 17 1 2 18 CNRS UMR 9197, Université Paris-Sud, Bâtiment 446, 19 91405 Orsay cedex, France 20 21 3 Laboratoire des systèmes Perceptifs, UMR CNRS 8248, 22 Département d’Etudes Cognitives, Ecole normale supérieure (ENS), 23 Paris Sciences & Lettres Research University, 75005 Paris, France 24 25 26 Emails: 27 Yonane Aushana: [email protected] 28 Samira Souffi: [email protected] 29 Jean-Marc Edeline: [email protected] 30 31 Christian Lorenzi: [email protected] 32 Chloé Huetz: [email protected] 33 34 Running title: Responses to vocoded vocalizations in AI 35 36 Total number of pages: 22 37 38 Total number of figures: 6 39 Total number of words:
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