Speech perception under the tent: A domain-general predictive role for the cerebellum

  1. Jeremy I Skipper
  2. Daniel R Lametti

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Abstract

The role of the cerebellum in speech perception remains a mystery. Given its uniform architecture, we tested the hypothesis that it implements a domain-general mechanism whose role in speech is determined by connectivity. We collated all neuroimaging studies reporting cerebellar activity in the Neurosynth database (n = 8,206). From this set, we found all studies involving passive speech and sound perception (n = 72, 64% speech, 12.5% sounds, 12.5% music, and 11% tones) and speech production and articulation (n = 175). Standard and coactivation neuroimaging meta-analyses were used to compare cerebellar and associated cortical activations between passive perception and production. We found distinct regions of perception-and production-related activity in the cerebellum and regions of perception-production overlap. Each of these regions had distinct patterns of cortico-cerebellar connectivity. To test for domain generality versus specificity, we identified all psychological and task-related terms in the Neurosynth database that predicted activity in cerebellar regions associated with passive perception and production. Regions in the cerebellum activated by speech perception were associated with domain-general terms related to prediction. One hallmark of predictive processing is metabolic savings (i.e., decreases in neural activity when events are predicted). To test the hypothesis that the cerebellum plays a predictive role in speech perception, we examined cortical activation between studies reporting cerebellar activation and those without cerebellar activation during speech perception. When the cerebellum was active during speech perception there was far less cortical activation than when it was inactive. The results suggest that the cerebellum implements a domain-general mechanism related to prediction during speech perception.

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  1. eLife

    ###Reviewer #2:

    The authors set out to investigate whether the cerebellum plays a domain-general and predictive role in speech perception. They leveraged the online platform, Neurosynth to conduct a meta-analysis of fMRI studies to compare the activation results between speech perception and speech production studies. They find that there are distinct as well as overlapping regions of perception- and production-related activity in the cerebellum, and that each of these regions has a distinct connectivity fingerprint with the cerebral cortex. They mined text data from thousands of studies in Neurosynth to determine which labels best explain these speech-perception and speech-production activity patterns. They find that cerebellar regions activated by speech-perception, speech production, and their overlap, are also associated with cognitive and motor processes beyond the domain of speech and language. On the basis of these results, they argue for a domain-general view of cerebellar processing.

    One of the most interesting findings in this paper is that speech-perception and speech-production tasks elicit both distinct and overlapping activity patterns in the cerebellum. It has long been known that the cerebellum is activated by speech processing, however, it has been less clear to what extent these two processes (perception and production) differ in their activation patterns. Importantly, the authors also show that these distinct and overlapping networks in the cerebellum display connectivity patterns with corresponding regions of the cerebral cortex. However, there are some major concerns.

    One of the central take-aways from this study is that prediction is a domain-general mechanism that supports speech perception in the cerebellum. The authors argue for domain-generality on the basis that regions activated by speech perception and production in the cerebellum are also activated by a wide range of non-speech tasks. However, I was a bit confused by this argument. It is my understanding that the same region of the cerebellum can be activated by many different tasks, and that each task will demand its own computational description. However, that does not necessarily provide evidence for domain-generality. What could point to domain-generality is a function/computation that explains the diverse set of computations required by the tasks. That speech-related regions of the cerebellum are also activated by a range of non-speech tasks does not (in my opinion) support a domain-general view of cerebellar processing.

    Another take-away from this study is that the cerebellum plays a predictive role in speech processing. Prediction is at the core of many theories of cerebellar function (e.g., internal models, error-based learning), of course, it is a very broad term that is not necessarily unique to the cerebellum. The authors hypothesize that, "if the cerebellum is involved in prediction during natural speech perception, there should be a greater amount of activity throughout the brain when the cerebellum is not active during this task". The authors compare two different sets of speech perception studies, those that report cerebellar activation and those that do not. They then compare the level of activation in cortex versus cerebellum for both of these study types. They find that cortical activation in the "no cerebellum" studies is increased relative to cortical activation in the "cerebellum active" studies. On the basis of these results, they infer that the cerebellum must be involved in prediction and that prediction results in metabolic savings (i.e. decreased activity in cortex). However, why did the speech perception tasks in the "no cerebellum" studies not activate the cerebellum. Did they not involve prediction in some capacity? There are likely other reasons that there was increased cortical activation in the "no cerebellum" studies that are unrelated to the absence of cerebellar activation.

    It is also not clear to me why speech perception studies that involved passive sound and music perception were included. How are tones related to speech perception? It would have been helpful if the authors had shown consistency across the different modalities (i.e. speech, sounds, instrumental music, and tones). I'm also assuming that the speech production studies were not matched across these four groups. Couldn't differences in activity patterns arising between the two study types potentially be attributed to sounds, instrumental music, and tones present in the speech perception studies?

  2. eLife

    ###Reviewer #1:

    I have very much enjoyed reading this piece of work, investigating the role of the cerebellum in non-motor functions using a meta-analysis and focusing especially on speech perception and predictive processing. I believe that this work is highly relevant to the field and will contribute considerably to the understanding of cerebellar functioning.

    I appreciate the careful description of the methods and the aim to challenge the hypotheses through additional testing. However I have only very few major concerns, which however I believe are all addressable:

    1. From page 8, but mainly throughout the whole paper: I am concerned with the inclusion of 22.5% of instrumental music or tone studies. The paper's overall focus is on speech perception and production, and the authors always only refer to "speech" throughout the manuscript. Whereas the inclusion of speech sound perception studies can be easily justified, the inclusion of tone perception is highly different if the focus lies on speech, e.g. due to the varying complexity of the input signal.

    Although the authors address this issue in the limitation section, it weakens the overall impact of the findings (as they also state, but downplay). For consistency the authors should exclude tone processing studies from their analysis; as the role of cerebellum in contributing to processing of time and potential motor sequencing is widely discussed in the literature (see Gordon et al 2018, PLoSOne, https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6242316/ ). As I very much support the ideas presented in the paper I believe a clear differentiation between perception of speech and perception of music is crucial for making a convincing argument regarding the role of the cerebellum in "passive" predictive language perception, if that is the focus of the paper. It would be interesting, however, if the regions for perception differ when including music studies compared to speech studies only. A separate analysis of the tone studies might not be feasible for 20 or so studies.

    Generally, the authors should either refrain from setting the focus on "speech perception" when the paper clearly focuses on "speech and tone perception" (or more generally "non-motor auditory perception", which is, by the way, not problematic at all, as the findings support a domain-general function of cerebellum. In that case speech perception should not be mentioned singularly in the title. However, if the authors wish to make a statement on speech perception, then they should exclude the tone perception studies from the analysis.

    1. Relatedly, page 5 last sentence, whereas I do agree with this approach and appreciate effort to test the own hypothesis, this approach is missing the testing of an alternative hypothesis: Could the decrease of general cortical activation be linked to the greater activity of a different region, other than the cerebellum. This should be at least discussed.

    2. Page 16/20: To test their hypothesis the authors compare the cortical activation of studies that report cerebellar activity and those that don't. If the cerebellum had this domain general function in predictive processing why would it not be active in some studies? Was there a systematic difference between the two sets of studies, and, as furthermore argued, did those studies that did not activate the cerebellum use indeed speech in novel contexts? A further investigation of the difference between the two sets of studies would be helpful in support of the argumentation.

  3. eLife

    ##Preprint Review

    This preprint was reviewed using eLife’s Preprint Review service, which provides public peer reviews of manuscripts posted on bioRxiv for the benefit of the authors, readers, potential readers, and others interested in our assessment of the work. This review applies only to version 1 of the manuscript.

    ###Summary:

    The importance of cerebellum in cognition generally, and in speech processing more specifically, are timely and interesting questions, and metaanalysis is a helpful tool. The paper is clearly written. However, in the opinion of at least one reviewer and the Reviewing Editor, neither of the two stated aims of the paper were satisfactorily achieved.

    The stated aims were to demonstrate:

    1. "that the cerebellum plays a domain-general role in speech perception-that is, a role that is not inherently speech specific." However, just showing coactivation with other tasks does not indicate domain-generality; for a variety of reasons. First, this conclusion is not supported because of the computational specificity issue raised by Reviewer 2, and second, coactivation in brain imaging can be an artifact of the spatial resolution of BOLD, and of preprocessing -- it does not necessarily imply coactivation at a neural level.

    2. "that the domain-general role played by the cerebellum and its connections during speech perception is related to prediction." Two lines of evidence are offered for this. 1) the reverse inference that regions identified in the paper are associated in Neurosynth with the term 'prediction'; and 2) that there was more cortical activity when the cerebellum was inactive. Just because accurate prediction should reduce activity, doesn't mean that a reduction in activity signifies prediction.

  4. Version published to 10.1101/2020.06.05.136804 on bioRxiv