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  1. Evaluation Summary:

    This work generates helpful new data on the network of brain areas employed for listening to speech in cochlear implant users. This is a difficult undertaking because functional MR is not possible in this group. The work uses a new type of near infrared spectroscopy to obtain measures related to brain activity in superficial areas and shows increased activity in frontal areas during speech perception.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #1 and Reviewer #2 agreed to share their name with the authors.)

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  2. Reviewer #1 (Public Review):

    The work addresses an important issue: whether subjects with cochlear implants use the same neural resources for speech listening as normal listeners. In order to address this fMRI is not possible and in this work the authors use a high-resolution form of fNIRS which measures superficial-cortex activity related to blood flow. The data implicate the use of a part of dorsolateral prefrontal cortex by CI users in the task which is not part of the specialist language network: the area has previously been suggested to be part of the multiple demand network involved in tasks including spatial working memory. The work supports additional neural resources for listening in CI users.

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  3. Reviewer #2 (Public Review):

    The authors have conducted an interesting study looking at the brain mechanisms of speech comprehension in cochlear implant users. This is a relatively under-explored area, due to difficulties in neuroimaging in this population, and so further data are welcome additions to the field. The study employs a technically challenging technique that allows the measurement of blood flow that overcomes some of these difficulties. The experimental approach is powerful, and is hypothesis-driven with respect to exploration of brain mechanisms beyond a focus on assumed recruitment of a language network, and adds a cognitive measure of working memory to create a functional ROI upon which to determine the shared recruitment of this mechanism in more difficult speech understanding that exists in the cochlear implant population. The addition of a well-matched control group allows for stronger conclusions with respect to the findings, which demonstrated that a working memory task and a word listening task shared activation in a similar region in the frontal cortex, which was greater in the cochlear implant group. This finding supports the authors' hypothesis that additional cognitive mechanisms are recruited in the cochlear implant population in order to understand speech. Research with the cochlear implant population is difficult and the authors do a good job to limit the recruitment to a relatively homogeneous population to try and decrease variance related to population characteristics.

    There are some limitations that influence the conclusions that are drawn in the paper currently. Notably, the authors hypothesize the recruitment of an anatomically defined brain region, yet the study uses a functional ROI definition. Further, this functional ROI is defined by a spatial working memory task, which is presumably used so as to be a non-linguistic task to strengthen the conclusion that general cognitive processes, like spatial working memory, are involved in difficult speech understanding in cochlear implantees. However, based on the findings the authors conclude that the brain region dorsolateral prefrontal cortex (DLPFC) is recruited in this case. Scrutiny of the DLPFC ROI shows that much of the functional activation includes the inferior frontal gyrus, which is not classically considered part of the DLPFC, inviting speculation that the spatial working memory task included cognitive mechanisms that might be assigned to the inferior frontal gyrus, for example, speech processing. Notably, the group difference in activation is circumscribed to the inferior frontal gyrus. The point here is not to debate about the localization of function to specific brain regions, rather it is to invite the authors to change their conclusions about the involvement of a brain region that seems to be minimally indicated in the results which statistically contrast the cochlear implant and control groups, and instead comment with respect to the task used.

    Another difficulty relates to the brain imaging technique employed. While there is considerable difficulty in achieving the excellent quality of data demonstrated, some methodological limitations may impact the conclusions. These relate to the extent of the field of view to cover the extent of the DLPFC, which is minimal in this case. Further, the coverage is on the edge of the field of view, where the method may have limitations in signal, and the inherent resolution of the technique and patterns of the data do not allow a strong conclusion about the exclusion of one brain region in preference for an adjacent one that is hypothesized, i.e., inferior frontal gyrus and DLPFC. Finally, the measurement from areas that overlie the cochlear implant transducer is missed, and so has the potential to influence conclusions about activation in this area. Indeed the pattern of results may indicate a finding of signal loss in the right auditory cortex.

    Findings in this study will help expand our understanding of the difficulties faced in speech understanding in the cochlear implant population, and how additional brain mechanisms may be recruited to complete this task.

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  4. Reviewer #3 (Public Review):

    Sherafati et al. investigated the brain networks used for speech perception (words in quiet) in a group of cochlear implant (CI) recipients and a control group (matched for age and gender) using high-density diffuse optical tomography (HD-DOT). Based on region-of-interest (ROI) analyses, the authors reported that the CI group showed reduced brain activity in the right auditory cortex and increased activity in the left dorsolateral prefrontal cortex (DLPFC), in comparison to the control group.

    As more common imaging methods (e.g. fMRI, EEG) are not suitable for imaging CI recipients, the use of HD-DOT is a strength of this study. The authors have been open in the interpretation of their results and acknowledged that additional data are required to support some of their arguments. The manuscript has been prepared to a high standard, in particular, the figures are clear and helpful. The authors have included a lot of supplementary materials to help readers understand and evaluate their study.

    Limitations of the study include:

    1. The rationale for some aspects of study design are missing
    For example, the 'critical' result of increased left DLPFC activation in the CI group was based on a ROI analysis, which was not well-motivated.

    Different brain regions support speech perception, including some domain-general brain areas. Fig. 4C suggests that CI > controls contrast identified quite a few group differences. It is unclear why the authors decided to focus on DLPFC as the domain-general brain region. Furthermore, why left DLPFC only (the authors decided on this focus by defining functional ROIs that included bilateral auditory ROIs and an ROI in left DLPFC)?

    As noted by the authors (Discussion, page 13), previous work has identified differences in activation levels between CI users and NH listeners in the right anterior temporal lobe and left middle superior temporal lobe (Zhou et al. 2018b).

    2. Results of t-tests and correlation analyses do not appear to have been corrected for multiple comparisons
    The authors report 3 ROI analyses and 4 correlation analyses but the associated p-values appear not to have been corrected for multiple comparisons. This issue is important because the p-value reported for the 'main' ROI result (increased DLPFC activation in CI users) is p = 0.03 (page 11).

    3. No behavioral measures were collected during the HD-DOT data acquisition
    The mean speech perception score (as measured by AzBio sentences) was significantly poorer in CI group relative to controls. However, this speech measure is not necessarily representative of speech perception during the HD-DOT scan (AzBio sentences vs. 15-s blocks of words in quiet). Ideally some behavioral data would have been collected during the HD-DOT scan, which could then be used to help interpret differences in brain activity

    4. Results are discussed in the context of listening effort but the authors did not measure listening effort
    The authors explain some of their results (increased DLPFC activation in CI users) in terms of increased listening effort (e.g. Page 14, Conclusions "...and provide a potential framework for the effort that many CI users need to expend during speech perception..."). As the authors did not include any measures of listening effort, it is not clear that increased listening effort is the correct explanation for the increased activation in the left DLPFC.

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