Temporo-cerebellar connectivity underlies timing constraints in audition

  1. Anika Stockert
  2. Michael Schwartze
  3. David Poeppel
  4. Alfred Anwander
  5. Sonja Kotz  Is a corresponding author
  1. University of Leipzig, Germany
  2. Maastricht University, Netherlands
  3. Max Planck Institute for Empirical Aesthetics, Germany
  4. Max Planck Institute for Human Cognitive and Brain Sciences, Germany

Abstract

The flexible and efficient adaptation to dynamic, rapid changes in the auditory environment likely involves generating and updating of internal models. Such models arguably exploit connections between the neocortex and the cerebellum, supporting proactive adaptation. Here we tested whether temporo-cerebellar disconnection is associated with the processing of sound at short-timescales. First, we identify lesion-specific deficits for the encoding of short timescale spectro-temporal non-speech and speech properties in patients with left posterior temporal cortex stroke. Second, using lesion- guided probabilistic tractography in healthy participants, we revealed bidirectional temporo-cerebellar connectivity with cerebellar dentate nuclei and crura I/II. These findings support the view that the encoding and modeling of rapidly modulated auditory spectro-temporal properties can rely on a temporo-cerebellar interface. We discuss these findings in view of the conjecture that proactive adaptation to a dynamic environment via internal models is a generalizable principle.

Data availability

There is restricted access to the data due to German legal regulations of patient protection.We have made all data which we can legally share accessible via figure share (link is included in the resource statement). We have provided all data (lesion data, scripts, behavioral data that allowed lesion-symptom mapping) in our figure share account for reproduction of the critical seed region for a tracking analysis.Anonymisation of MRI/DTI data is not allowed either through the ethics agreement nor the participants' consent. We cannot do anything about this as these are the legal regulations that we have to deal with. We have made a clear statement that we seek open dialogue about how we have analysed our data. Further, given the data that we have provided, any interested researcher can (1) approach us about our analysis, (2) can take a set of open source age-matched structural MRI/DTI data to replicated our results

Article and author information

Author details

  1. Anika Stockert

    Department of Neurology, University of Leipzig, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Michael Schwartze

    Neuropsyhology and Psychopharmacology, Maastricht University, Maastricht, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  3. David Poeppel

    Neuroscience, Max Planck Institute for Empirical Aesthetics, Frankfurt, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Alfred Anwander

    Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4861-4808
  5. Sonja Kotz

    Neuropsychology and Psychopharmacology, Maastricht University, Maastricht, Netherlands
    For correspondence
    sonja.kotz@maastrichtuniversity.nl
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5894-4624

Funding

Deutsche Forschungsgemeinschaft (DFG KO 2268/6-1)

  • Sonja Kotz

Dissertation award University of Leipzig (none)

  • Anika Stockert

Max-Planck-Gesellschaft (none)

  • Sonja Kotz

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Human subjects: The protocol of the current research was approved by the ethics committee of the University of Leipzig, Germany (Protocol Number: 953). All participants provided written, informed consent before the start of data collection.

Reviewing Editor

  1. Timothy D Griffiths, University of Newcastle, United Kingdom

Publication history

  1. Preprint posted: February 7, 2021 (view preprint)
  2. Received: February 7, 2021
  3. Accepted: September 9, 2021
  4. Accepted Manuscript published: September 20, 2021 (version 1)
  5. Version of Record published: September 29, 2021 (version 2)
  6. Version of Record updated: September 30, 2021 (version 3)

Copyright

© 2021, Stockert et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 643
    Page views
  • 104
    Downloads
  • 1
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Anika Stockert
  2. Michael Schwartze
  3. David Poeppel
  4. Alfred Anwander
  5. Sonja Kotz
(2021)
Temporo-cerebellar connectivity underlies timing constraints in audition
eLife 10:e67303.
https://doi.org/10.7554/eLife.67303

Further reading

    1. Neuroscience
    Payel Chatterjee et al.
    Research Article

    During flight maneuvers, insects exhibit compensatory head movements which are essential for stabilizing the visual field on their retina, reducing motion blur, and supporting visual self-motion estimation. In Diptera, such head movements are mediated via visual feedback from their compound eyes that detect retinal slip, as well as rapid mechanosensory feedback from their halteres - the modified hindwings that sense the angular rates of body rotations. Because non-Dipteran insects lack halteres, it is not known if mechanosensory feedback about body rotations plays any role in their head stabilization response. Diverse non-Dipteran insects are known to rely on visual and antennal mechanosensory feedback for flight control. In hawkmoths, for instance, reduction of antennal mechanosensory feedback severely compromises their ability to control flight. Similarly, when the head movements of freely-flying moths are restricted, their flight ability is also severely impaired. The role of compensatory head movements as well as multimodal feedback in insect flight raises an interesting question: in insects that lack halteres, what sensory cues are required for head stabilization? Here, we show that in the nocturnal hawkmoth Daphnis nerii, compensatory head movements are mediated by combined visual and antennal mechanosensory feedback. We subjected tethered moths to open-loop body roll rotations under different lighting conditions, and measured their ability to maintain head angle in the presence or absence of antennal mechanosensory feedback. Our study suggests that head stabilization in moths is mediated primarily by visual feedback during roll movements at lower frequencies, whereas antennal mechanosensory feedback is required when roll occurs at higher frequency. These findings are consistent with the hypothesis that control of head angle results from a multimodal feedback loop that integrates both visual and antennal mechanosensory feedback, albeit at different latencies. At adequate light levels, visual feedback is sufficient for head stabilization primarily at low frequencies of body roll. However, under dark conditions, antennal mechanosensory feedback is essential for the control of head movements at high of body roll.

    1. Developmental Biology
    2. Neuroscience
    Ashtyn T Wiltbank et al.
    Research Article

    Efficient neurotransmission is essential for organism survival and is enhanced by myelination. However, the genes that regulate myelin and myelinating glial cell development have not been fully characterized. Data from our lab and others demonstrates that cd59, which encodes for a small GPI-anchored glycoprotein, is highly expressed in developing zebrafish, rodent, and human oligodendrocytes (OLs) and Schwann cells (SCs), and that patients with CD59 dysfunction develop neurological dysfunction during early childhood. Yet, the function of Cd59 in the developing nervous system is currently undefined. In this study, we demonstrate that cd59 is expressed in a subset of developing SCs. Using cd59 mutant zebrafish, we show that developing SCs proliferate excessively and nerves may have reduced myelin volume, altered myelin ultrastructure, and perturbed node of Ranvier assembly. Finally, we demonstrate that complement activity is elevated in cd59 mutants and that inhibiting inflammation restores SC proliferation, myelin volume, and nodes of Ranvier to wildtype levels. Together, this work identifies Cd59 and developmental inflammation as key players in myelinating glial cell development, highlighting the collaboration between glia and the innate immune system to ensure normal neural development.