Rhythmic modulation of prediction errors: A top-down gating role for the beta-range in speech processing

被引:2
作者
Hovsepyan, Sevada [1 ]
Olasagasti, Itsaso [1 ]
Giraud, Anne-Lise [1 ,2 ]
机构
[1] Univ Geneva, Dept Basic Neurosci, Biotech Campus, Geneva, Switzerland
[2] Univ Paris Cite, Inst Pasteur, Inst Audit, INSERM, Paris, France
基金
瑞士国家科学基金会;
关键词
BRAIN OSCILLATIONS; NEURAL ACTIVITY; VISUAL-CORTEX; GAMMA RHYTHMS; MODEL; THETA; FEEDBACK; BAND; FEEDFORWARD; SHORTLIST;
D O I
10.1371/journal.pcbi.1011595
中图分类号
Q5 [生物化学];
学科分类号
071010 ; 081704 ;
摘要
Natural speech perception requires processing the ongoing acoustic input while keeping in mind the preceding one and predicting the next. This complex computational problem could be handled by a dynamic multi-timescale hierarchical inferential process that coordinates the information flow up and down the language network hierarchy. Using a predictive coding computational model (Precoss-beta) that identifies online individual syllables from continuous speech, we address the advantage of a rhythmic modulation of up and down information flows, and whether beta oscillations could be optimal for this. In the model, and consistent with experimental data, theta and low-gamma neural frequency scales ensure syllable-tracking and phoneme-level speech encoding, respectively, while the beta rhythm is associated with inferential processes. We show that a rhythmic alternation of bottom-up and top-down processing regimes improves syllable recognition, and that optimal efficacy is reached when the alternation of bottom-up and top-down regimes, via oscillating prediction error precisions, is in the beta range (around 20-30 Hz). These results not only demonstrate the advantage of a rhythmic alternation of up- and down-going information, but also that the low-beta range is optimal given sensory analysis at theta and low-gamma scales. While specific to speech processing, the notion of alternating bottom-up and top-down processes with frequency multiplexing might generalize to other cognitive architectures. During speech perception, our brain achieves continuous acoustic analysis of the ongoing speech signal, its transformation into linguistic representations, and the prediction of the most likely next words or syllables. In this computational study, we address the biological mechanisms underpinning the coordination of these operations during natural speech processing. Using a model that recognizes on-line syllables in natural sentences, we show that neural activity at specific rhythms is dedicated to specific operations, and that while the theta and low-gamma rhythms are engaged in speech features signaling and encoding, the more endogenous low-beta rhythm drives the rhythmic and coordinated modulation of prediction errors across levels of hierarchy.
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页数:29
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共 97 条
  • [1] Beta-band oscillations play an essential role in motor-auditory interactions
    Abbasi, Omid
    Gross, Joachim
    [J]. HUMAN BRAIN MAPPING, 2020, 41 (03) : 656 - 665
  • [2] Amodei D, 2016, PR MACH LEARN RES, V48
  • [3] Delta-Beta Coupled Oscillations Underlie Temporal Prediction Accuracy
    Arnal, Luc H.
    Doelling, Keith B.
    Poeppel, David
    [J]. CEREBRAL CORTEX, 2015, 25 (09) : 3077 - 3085
  • [4] Cortical oscillations and sensory predictions
    Arnal, Luc H.
    Giraud, Anne-Lise
    [J]. TRENDS IN COGNITIVE SCIENCES, 2012, 16 (07) : 390 - 398
  • [5] Layer and rhythm specificity for predictive routing
    Bastos, Andre M.
    Lundqvist, Mikael
    Waite, Ayan S.
    Kopell, Nancy
    Miller, Earl K.
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2020, 117 (49) : 31459 - 31469
  • [6] Canonical Microcircuits for Predictive Coding
    Bastos, Andre M.
    Usrey, W. Martin
    Adams, Rick A.
    Mangun, George R.
    Fries, Pascal
    Friston, Karl J.
    [J]. NEURON, 2012, 76 (04) : 695 - 711
  • [7] Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels
    Bastos, Andre Moraes
    Vezoli, Julien
    Bosman, Conrado Arturo
    Schoffelen, Jan-Mathijs
    Oostenveld, Robert
    Dowdall, Jarrod Robert
    De Weerd, Peter
    Kennedy, Henry
    Fries, Pascal
    [J]. NEURON, 2015, 85 (02) : 390 - 401
  • [8] Spontaneous Beta Band Rhythms in the Predictive Coding of Natural Stimuli
    Betti, Viviana
    Della Penna, Stefania
    de Pasquale, Francesco
    Corbetta, Maurizio
    [J]. NEUROSCIENTIST, 2021, 27 (02) : 184 - 201
  • [9] Oscillatory EEG dynamics underlying automatic chunking during sentence processing
    Bonhage, Corinna E.
    Meyer, Lars
    Gruber, Thomas
    Friederici, Angela D.
    Mueller, Jutta L.
    [J]. NEUROIMAGE, 2017, 152 : 647 - 657
  • [10] Shifting the spotlight of attention: evidence for discrete computations in cognition
    Buschman, Timothy J.
    Miller, Earl K.
    [J]. FRONTIERS IN HUMAN NEUROSCIENCE, 2010, 4