IDEAS home Printed from https://ideas.repec.org/a/plo/pbio00/3001803.html
   My bibliography  Save this article

Differences in temporal processing speeds between the right and left auditory cortex reflect the strength of recurrent synaptic connectivity

Author

Listed:
  • Demetrios Neophytou
  • Diego M Arribas
  • Tushar Arora
  • Robert B Levy
  • Il Memming Park
  • Hysell V Oviedo

Abstract

Brain asymmetry in the sensitivity to spectrotemporal modulation is an established functional feature that underlies the perception of speech and music. The left auditory cortex (ACx) is believed to specialize in processing fast temporal components of speech sounds, and the right ACx slower components. However, the circuit features and neural computations behind these lateralized spectrotemporal processes are poorly understood. To answer these mechanistic questions we use mice, an animal model that captures some relevant features of human communication systems. In this study, we screened for circuit features that could subserve temporal integration differences between the left and right ACx. We mapped excitatory input to principal neurons in all cortical layers and found significantly stronger recurrent connections in the superficial layers of the right ACx compared to the left. We hypothesized that the underlying recurrent neural dynamics would exhibit differential characteristic timescales corresponding to their hemispheric specialization. To investigate, we recorded spike trains from awake mice and estimated the network time constants using a statistical method to combine evidence from multiple weak signal-to-noise ratio neurons. We found longer temporal integration windows in the superficial layers of the right ACx compared to the left as predicted by stronger recurrent excitation. Our study shows substantial evidence linking stronger recurrent synaptic connections to longer network timescales. These findings support speech processing theories that purport asymmetry in temporal integration is a crucial feature of lateralization in auditory processing.This study uses the mouse as a model system that captures relevant features of human lateralized processing of speech and music, revealing a novel mechanism whereby stronger recurrent activity in the Right Auditory Cortex led to longer temporal integration compared to the Left (consistent with the temporal scales of syllabic and supra-syllabic processing).

Suggested Citation

  • Demetrios Neophytou & Diego M Arribas & Tushar Arora & Robert B Levy & Il Memming Park & Hysell V Oviedo, 2022. "Differences in temporal processing speeds between the right and left auditory cortex reflect the strength of recurrent synaptic connectivity," PLOS Biology, Public Library of Science, vol. 20(10), pages 1-20, October.
  • Handle: RePEc:plo:pbio00:3001803
    DOI: 10.1371/journal.pbio.3001803
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3001803
    Download Restriction: no

    File URL: https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.3001803&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pbio.3001803?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. József Fiser & Chiayu Chiu & Michael Weliky, 2004. "Small modulation of ongoing cortical dynamics by sensory input during natural vision," Nature, Nature, vol. 431(7008), pages 573-578, September.
    2. Tomáš Hromádka & Michael R DeWeese & Anthony M Zador, 2008. "Sparse Representation of Sounds in the Unanesthetized Auditory Cortex," PLOS Biology, Public Library of Science, vol. 6(1), pages 1-14, January.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Anthony Randal McIntosh & Natasa Kovacevic & Roxane J Itier, 2008. "Increased Brain Signal Variability Accompanies Lower Behavioral Variability in Development," PLOS Computational Biology, Public Library of Science, vol. 4(7), pages 1-9, July.
    2. Oren Amsalem & Hidehiko Inagaki & Jianing Yu & Karel Svoboda & Ran Darshan, 2024. "Sub-threshold neuronal activity and the dynamical regime of cerebral cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Corentin Massot & Adam D Schneider & Maurice J Chacron & Kathleen E Cullen, 2012. "The Vestibular System Implements a Linear–Nonlinear Transformation In Order to Encode Self-Motion," PLOS Biology, Public Library of Science, vol. 10(7), pages 1-20, July.
    4. Michael A Carlin & Mounya Elhilali, 2013. "Sustained Firing of Model Central Auditory Neurons Yields a Discriminative Spectro-temporal Representation for Natural Sounds," PLOS Computational Biology, Public Library of Science, vol. 9(3), pages 1-18, March.
    5. repec:plo:pcbi00:1002354 is not listed on IDEAS
    6. Gabriel D Puccini & Albert Compte & Miguel Maravall, 2006. "Stimulus Dependence of Barrel Cortex Directional Selectivity," PLOS ONE, Public Library of Science, vol. 1(1), pages 1-6, December.
    7. repec:plo:pone00:0078917 is not listed on IDEAS
    8. repec:plo:pcbi00:1000551 is not listed on IDEAS
    9. Benjamin R Cowley & Matthew A Smith & Adam Kohn & Byron M Yu, 2016. "Stimulus-Driven Population Activity Patterns in Macaque Primary Visual Cortex," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-31, December.
    10. Yifan Gu & Yang Qi & Pulin Gong, 2019. "Rich-club connectivity, diverse population coupling, and dynamical activity patterns emerging from local cortical circuits," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-34, April.
    11. Yang Yiling & Katharine Shapcott & Alina Peter & Johanna Klon-Lipok & Huang Xuhui & Andreea Lazar & Wolf Singer, 2023. "Robust encoding of natural stimuli by neuronal response sequences in monkey visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    12. Márton Albert Hajnal & Duy Tran & Michael Einstein & Mauricio Vallejo Martelo & Karen Safaryan & Pierre-Olivier Polack & Peyman Golshani & Gergő Orbán, 2023. "Continuous multiplexed population representations of task context in the mouse primary visual cortex," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    13. Perla González-Pereyra & Oswaldo Sánchez-Lobato & Mario G. Martínez-Montalvo & Diana I. Ortega-Romero & Claudia I. Pérez-Díaz & Hugo Merchant & Luis A. Tellez & Pavel E. Rueda-Orozco, 2024. "Preconfigured cortico-thalamic neural dynamics constrain movement-associated thalamic activity," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    14. Lars Buesing & Johannes Bill & Bernhard Nessler & Wolfgang Maass, 2011. "Neural Dynamics as Sampling: A Model for Stochastic Computation in Recurrent Networks of Spiking Neurons," PLOS Computational Biology, Public Library of Science, vol. 7(11), pages 1-22, November.
    15. Miguel Maravall & Rasmus S Petersen & Adrienne L Fairhall & Ehsan Arabzadeh & Mathew E Diamond, 2007. "Shifts in Coding Properties and Maintenance of Information Transmission during Adaptation in Barrel Cortex," PLOS Biology, Public Library of Science, vol. 5(2), pages 1-12, January.
    16. Rong J. B. Zhu & Xue-Xin Wei, 2023. "Unsupervised approach to decomposing neural tuning variability," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    17. Cheng Ly & Brent Doiron, 2009. "Divisive Gain Modulation with Dynamic Stimuli in Integrate-and-Fire Neurons," PLOS Computational Biology, Public Library of Science, vol. 5(4), pages 1-12, April.
    18. Gonzalo H Otazu & Christian Leibold, 2011. "A Corticothalamic Circuit Model for Sound Identification in Complex Scenes," PLOS ONE, Public Library of Science, vol. 6(9), pages 1-15, September.
    19. Jean-Pierre Rospars & Alexandre Grémiaux & David Jarriault & Antoine Chaffiol & Christelle Monsempes & Nina Deisig & Sylvia Anton & Philippe Lucas & Dominique Martinez, 2014. "Heterogeneity and Convergence of Olfactory First-Order Neurons Account for the High Speed and Sensitivity of Second-Order Neurons," PLOS Computational Biology, Public Library of Science, vol. 10(12), pages 1-16, December.
    20. repec:plo:pcbi00:1002395 is not listed on IDEAS
    21. Teppei Matsui & Takayuki Hashimoto & Tomonari Murakami & Masato Uemura & Kohei Kikuta & Toshiki Kato & Kenichi Ohki, 2024. "Orthogonalization of spontaneous and stimulus-driven activity by hierarchical neocortical areal network in primates," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    22. Rava Azeredo da Silveira & Michael J Berry II, 2014. "High-Fidelity Coding with Correlated Neurons," PLOS Computational Biology, Public Library of Science, vol. 10(11), pages 1-25, November.
    23. Disheng Tang & Joel Zylberberg & Xiaoxuan Jia & Hannah Choi, 2024. "Stimulus type shapes the topology of cellular functional networks in mouse visual cortex," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    24. Ryan C Williamson & Benjamin R Cowley & Ashok Litwin-Kumar & Brent Doiron & Adam Kohn & Matthew A Smith & Byron M Yu, 2016. "Scaling Properties of Dimensionality Reduction for Neural Populations and Network Models," PLOS Computational Biology, Public Library of Science, vol. 12(12), pages 1-27, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:plo:pbio00:3001803. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: plosbiology (email available below). General contact details of provider: https://journals.plos.org/plosbiology/ .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.