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Research ArticleNew Research, Sensory and Motor Systems

Signature Patterns for Top-Down and Bottom-Up Information Processing via Cross-Frequency Coupling in Macaque Auditory Cortex

Christian D. Márton, Makoto Fukushima, Corrie R. Camalier, Simon R. Schultz and Bruno B. Averbeck
eNeuro 28 March 2019, 6 (2) ENEURO.0467-18.2019; https://doi.org/10.1523/ENEURO.0467-18.2019
Christian D. Márton
1Centre for Neurotechnology, and Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
2Section on Learning and Decision Making, Laboratory of Neuropsychology, National Institute of Mental Health/National Institutes of Health, Bethesda, Maryland 20892
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Makoto Fukushima
2Section on Learning and Decision Making, Laboratory of Neuropsychology, National Institute of Mental Health/National Institutes of Health, Bethesda, Maryland 20892
3 RIKEN Center for Brain Science Institute, Saitama 351-0106, Japan
4Consumer Neuroscience, The Nielsen Company, Tokyo 107-0052, Japan
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Corrie R. Camalier
2Section on Learning and Decision Making, Laboratory of Neuropsychology, National Institute of Mental Health/National Institutes of Health, Bethesda, Maryland 20892
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Simon R. Schultz
1Centre for Neurotechnology, and Department of Bioengineering, Imperial College London, London SW7 2AZ, United Kingdom
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Bruno B. Averbeck
2Section on Learning and Decision Making, Laboratory of Neuropsychology, National Institute of Mental Health/National Institutes of Health, Bethesda, Maryland 20892
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Figures

  • Extended Data
  • Figure 1.
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    Figure 1.

    Coupling analysis overview: recordings were made from four µECoG arrays spanning auditory cortex while monkeys listened to 1 of 20 natural VOCs, 20 synthetic EPSs, or 20 synthetic SPSs. Electrodes were partitioned into four sectors along the caudorostral axis (S1, A1/ML; S2, R/AL; S3, RTL; S4, RTp). We decomposed the signal into its time–frequency representation, and obtained amplitude and phase components for each sector. Plots of signal amplitude (in dB) are normalized to the baseline activity before stimulus onset. We investigated two types of coupling across sectors: amplitude–amplitude and phase–amplitude coupling. We computed both types of coupling in the bottom-up and top-down directions. Top-down coupling was defined as coupling in which the source electrode came from a sector of higher order than the target electrode, and vice versa for bottom-up coupling.

  • Figure 2.
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    Figure 2.

    Top-down vs bottom-up phase–amplitude and amplitude–amplitude coupling in natural vocalizations (VOC). A, B, Phase-amplitude coupling (PAC) strength in the top-down (A) and bottom-up (B) directions. Depicted are canonical correlation-derived coupling coefficients (see Materials and Methods). C, Difference in top-down and bottom-up in PAC strength. Significant differences are enclosed by black rectangles (p ≤ 0.01, cluster-corrected). D, E, Amplitude-amplitude coupling (AAC) strength in the top-down (D) and bottom-up (E) directions. Depicted are canonical correlation-derived coupling coefficients. F, Difference between top-down and bottom-up in AAC strength. Significant differences are marked by black outlines (p ≤ 0.01, cluster corrected). Results are depicted averaged across all channels, cross-regional pairs, and animals. See Extended Data Figure 2-1, Extended Data Figure 2-2, and Extended Data Figure 2-3.

  • Figure 3.
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    Figure 3.

    Top-down vs bottom-up PAC strength across the auditory hierarchy in natural stimuli. A–F, Difference in top-down and bottom-up PAC strength for CFC between sectors 1 (A1/ML) and 2 (R/AL; A), sectors 1 (A1/ML) and 3 (RTL; B), sectors 1 (A1/ML) and 4 (RTp; C), sectors 2 and 3 (D), sectors 2 and 4 (E), and sectors 3 and 4 (F; for sector definitions, see Data preprocessing, in Materials and Methods ). Interactions between sector 1 (A1/ML) and higher-order sectors show strong asymmetries in bottom-up and top-down coupling strength across the frequency spectrum; interactions among higher-order sectors (S2–S4) show less widespread asymmetries. Significant differences are marked by black outlines (p ≤ 0.01, cluster corrected). Results are depicted averaged across all channels and animals. See Extended Data Figure 3-1.

  • Figure 4.
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    Figure 4.

    Top-down vs bottom-up phase–amplitude and amplitude–amplitude coupling in synthetic envelope-preserved stimuli (EPSs) and synthetic spectrum-preserved stimuli (SPSs) A, Difference in top-down and bottom-up PAC strength in EPS stimuli. B, Difference in top-down and bottom-up AAC strength in EPS stimuli. C, Difference in top-down and bottom-up PAC strength in SPS stimuli. D, Difference in top-down and bottom-up AAC strength in SPS stimuli. Significant differences are marked by black outlines (p ≤ 0.01, cluster corrected). Results are depicted averaged across all channels, cross-regional pairs, and animals. See Extended Data Figure 4-1, Extended Data Figure 4-2, Extended Data Figure 4-3, Extended Data Figure 4-4, Extended Data Figure 4-5, and Extended Data Figure 4-6.

  • Figure 5.
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    Figure 5.

    Phase-amplitude (PAC) and amplitude-amplitude (AAC) coupling strength in natural vocalizations (VOC) compared with synthetic envelope-preserved sounds (EPS) and synthetic spectrum-preserved sounds (SPS). A–D Difference in PAC strength between natural vocalizations and synthetic sounds. The difference between VOC and EPS stimuli (A–B) and between VOC and SPS (C–D) stimuli is depicted separately in the top-down and bottom-up direction. E–H Difference in AAC strength between natural vocalizations and synthetic sounds. The difference between VOC and EPS stimuli (E–F) and between VOC and SPS (G–H) stimuli is again depicted separately in the top-down and bottom-up direction. Significant differences are marked by black outlines (p ≤ 0.01, cluster corrected). Results are depicted averaged across all channels, cross-regional pairs, and animals. See Extended Data Figure 5-1.

Extended Data

  • Figures
  • Extended Data Figure 2-1

    (A) Power vs. frequency of neural signal and (B) regression line fit. The amplitude of the neural recording signal peaks in the alpha (7.5-12.5 Hz) frequency range and shows the typical 1/f decay pattern thereafter. The signal depicted here is from stimulus onset (time=0) for presentation of the intact stimulus (VOC), averaged across all variables. Standard deviation across all variables is depicted by the red shaded region. The regression line fit to the neural signal confirms a 1/f decay pattern (B). The delta frequency band (0-2.5 Hz) was excluded from analyses (see Methods and Materials). Download Figure 2-1, EPS file.

  • Extended Data Figure 2-2

    Distribution of differences in PAC coupling strength for select CFC pairs in natural stimuli (VOC) (A) theta (5Hz) to beta (20Hz) PAC (B) theta (5Hz) to high gamma (90Hz) PAC (C) beta (20Hz) to low gamma (55Hz) PAC. Download Figure 2-2, EPS file.

  • Extended Data Figure 2-3

    Distribution of differences in AAC coupling strength for select CFC pairs in natural stimuli (VOC) (A) theta (5Hz) to beta (20Hz) PAC (B) theta (5Hz) to high gamma (90Hz) PAC (C) beta (20Hz) to low gamma (55Hz) PAC. Download Figure 2-3, EPS file.

  • Extended Data Figure 3-1

    Top-down versus bottom-up amplitude-amplitude coupling strength (AAC) across the auditory hierarchy in natural stimuli (VOC) Difference in top-down and bottom-up amplitude-amplitude coupling (AAC) strength for CFC between sectors 1 (A1/ML) and 2 (R/AL) (A), sectors 1 (A1/ML) and 3 (RTL) (B), sectors 1 (A1/ML) and 4 (RTp) (C), sectors 2 and 3 (D), sectors 2 and 4 (E) and sectors 3 and 4 (F) (see Methods and Materials 3.5 for sector definitions). Interactions between sector 1 (A1/ML) and higher order sectors show strong asymmetries in bottom-up and top-down coupling strength across the frequency spectrum; interactions among higher-order sectors (S2-S4) show less widespread asymmetries. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). Results are depicted averaged across all channels and animals. Download Figure 3-1, EPS file.

  • Extended Data Figure 4-1

    Top-down vs. bottom-up phase-amplitude and amplitude-amplitude coupling in synthetic envelope-preserved vocalizations (EPS). (A-B) Phase-amplitude coupling (PAC) strength in the top-down (A) and bottom-up direction (B). Depicted are canonical correlation-derived coupling coefficients (see Methods and Materials). (C) Difference in top-down and bottom-up in PAC strength. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). (D-E) Amplitude-amplitude coupling (AAC) strength in the top-down (D) and bottom-up direction (E). Depicted are canonical correlation-derived coupling coefficients. (F) Difference between top-down and bottom-up in AAC strength. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). Results are depicted averaged across all channels, cross-regional pairs, and animals. Download Figure 4-1, EPS file.

  • Extended Data Figure 4-2

    Top-down versus bottom-up phase-amplitude coupling strength (PAC) across the auditory hierarchy in synthetic envelop-preserved stimuli (EPS) Difference in top-down and bottom-up phase-amplitude coupling (PAC) strength for CFC between sectors 1 (A1/ML) and 2 (R/AL) (A), sectors 1 (A1/ML) and 3 (RTL) (B), sectors 1 (A1/ML) and 4 (RTp) (C), sectors 2 and 3 (D), sectors 2 and 4 (E) and sectors 3 and 4 (F) (see Methods and Materials 3.5 for sector definitions). Interactions between sector 1 (A1/ML) and higher order sectors show strong asymmetries in bottom-up and top-down coupling strength across the frequency spectrum; interactions among higher-order sectors (S2-S4) show less widespread asymmetries. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). Results are depicted averaged across all channels and animals. Download Figure 4-2, EPS file.

  • Extended Data Figure 4-3

    Top-down versus bottom-up amplitude-amplitude coupling strength (AAC) across the auditory hierarchy in synthetic envelope-preserved stimuli (EPS) Difference in top-down and bottom-up amplitude-amplitude coupling (AAC) strength for CFC between sectors 1 (A1/ML) and 2 (R/AL) (A), sectors 1 (A1/ML) and 3 (RTL) (B), sectors 1 (A1/ML) and 4 (RTp) (C), sectors 2 and 3 (D), sectors 2 and 4 (E) and sectors 3 and 4 (F) (see Methods and Materials 3.5 for sector definitions). Interactions between sector 1 (A1/ML) and higher order sectors show strong asymmetries in bottom-up and top-down coupling strength across the frequency spectrum; interactions among higher-order sectors (S2-S4) show less widespread asymmetries. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). Results are depicted averaged across all channels and animals. Download Figure 4-3, EPS file.

  • Extended Data Figure 4-4

    Top-down vs. bottom-up phase-amplitude and amplitude-amplitude coupling in synthetic spectrum-preserved vocalizations (SPS). (A-B) Phase-amplitude coupling (PAC) strength in the top-down (A) and bottom-up direction (B). Depicted are canonical correlation-derived coupling coefficients (see Methods and Materials). (C) Difference in top-down and bottom-up in PAC strength. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). (D-E) Amplitude-amplitude coupling (AAC) strength in the top-down (D) and bottom-up direction (E). Depicted are canonical correlation-derived coupling coefficients. (F) Difference between top-down and bottom-up in AAC strength. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). Results are depicted averaged across all channels, cross-regional pairs, and animals. Download Figure 4-4, EPS file.

  • Extended Data Figure 4-5

    Top-down versus bottom-up phase-amplitude coupling strength (PAC) across the auditory hierarchy in synthetic spectrum-preserved stimuli (SPS) Difference in top-down and bottom-up phase-amplitude coupling (PAC) strength for CFC between sectors 1 (A1/ML) and 2 (R/AL) (A), sectors 1 (A1/ML) and 3 (RTL) (B), sectors 1 (A1/ML) and 4 (RTp) (C), sectors 2 and 3 (D), sectors 2 and 4 (E) and sectors 3 and 4 (F) (see Methods and Materials 3.5 for sector definitions). Interactions between sector 1 (A1/ML) and higher order sectors show strong asymmetries in bottom-up and top-down coupling strength across the frequency spectrum; interactions among higher-order sectors (S2-S4) show less widespread asymmetries. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). Results are depicted averaged across all channels and animals. Download Figure 4-5, EPS file.

  • Extended Data Figure 4-6

    Top-down versus bottom-up amplitude-amplitude coupling strength (AAC) across the auditory hierarchy in synthetic spectrum-preserved stimuli (SPS) Difference in top-down and bottom-up amplitude-amplitude coupling (AAC) strength for CFC between sectors 1 (A1/ML) and 2 (R/AL) (A), sectors 1 (A1/ML) and 3 (RTL) (B), sectors 1 (A1/ML) and 4 (RTp) (C), sectors 2 and 3 (D), sectors 2 and 4 (E) and sectors 3 and 4 (F) (see Methods and Materials 3.5 for sector definitions). Interactions between sector 1 (A1/ML) and higher order sectors show strong asymmetries in bottom-up and top-down coupling strength across the frequency spectrum; interactions among higher-order sectors (S2-S4) show less widespread asymmetries. Significant differences are marked by black outlines (p≤0.01, cluster-corrected). Results are depicted averaged across all channels and animals. Download Figure 4-6, EPS file.

  • Extended Data Figure 5-1

    Phase-amplitude and amplitude-amplitude coupling strength in synthetic envelope-preserved sounds (SPS) compared to envelope-preserved sounds (EPS) (A-B) Difference in PAC strength between synthetic spectrum-preserved (SPS) and synthetic envelope-preserved sounds (EPS), separately in the top-down (B) and bottom-up direction (C). (C-D) Difference in AAC strength between SPS and EPS, separately in the top-down (C) and bottom-up direction (D). Significant differences are marked by black outlines (p≤0.01, cluster-corrected). Results are depicted averaged across all channels, cross-regional pairs, and animals. Download Figure 5-1, EPS file.

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Signature Patterns for Top-Down and Bottom-Up Information Processing via Cross-Frequency Coupling in Macaque Auditory Cortex
Christian D. Márton, Makoto Fukushima, Corrie R. Camalier, Simon R. Schultz, Bruno B. Averbeck
eNeuro 28 March 2019, 6 (2) ENEURO.0467-18.2019; DOI: 10.1523/ENEURO.0467-18.2019

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Signature Patterns for Top-Down and Bottom-Up Information Processing via Cross-Frequency Coupling in Macaque Auditory Cortex
Christian D. Márton, Makoto Fukushima, Corrie R. Camalier, Simon R. Schultz, Bruno B. Averbeck
eNeuro 28 March 2019, 6 (2) ENEURO.0467-18.2019; DOI: 10.1523/ENEURO.0467-18.2019
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Keywords

  • auditory cortex
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