Research ArticleNEUROSCIENCE

Context-specific modulation of intrinsic coupling modes shapes multisensory processing

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Science Advances  10 Apr 2019:
Vol. 5, no. 4, eaar7633
DOI: 10.1126/sciadv.aar7633
  • Fig. 1 Effects of multisensory stimulation on response timing and power.

    (A) Map of functional areas. A1, primary auditory cortex; AAF, anterior auditory field; PPF, posterior pseudosylvian field; PSF, posterior suprasylvian field; ADF, anterior dorsal field; AVF, anterior ventral field; VP, ventroposterior area; 3b, primary somatosensory cortex; S2, secondary somatosensory cortex; S3, tertiary somatosensory cortex; PPc, posterior parietal caudal; PPr, posterior parietal rostral; SSY, suprasylvian visual areas. (B) Schematic of the ECoG array placed on the left hemisphere of the ferret brain, covering most of the occipital, temporal, and parietal cortex. Red dots represent recording sites, and white circles represent the holes in the foil. lat, lateral sulcus; sss, suprasylvian sulcus; ps, pseudosylvian sulcus. (C) Topographic distribution of response amplitudes with unimodal (A: clicks and V: flashes) and bimodal (AV: simultaneous clicks and flashes) stimuli. Dark colors represent the amplitude of the strongest deflection in the event-related potential (ERP) within the first 80 ms after stimulus onset. (D) Topographic distribution of changes of total power in the alpha band in response to auditory (left), visual (middle), and audiovisual (right) stimuli. Power change was averaged over a stimulus time window (100 to 600 ms, relative to stimulus onset) and normalized to the prestimulus interval (−600 to −100 ms). (E) Latency reduction. Scatterplot of latencies of responses to unimodal versus bimodal stimulation. Blue circles represent data from electrodes that responded to unimodal visual stimuli but not unimodal auditory stimuli; red circles indicate electrodes that responded in the unimodal condition only to auditory stimuli. Sites that responded to both unimodal visual and unimodal auditory stimuli were not included. Top right: Probability distribution of the variation index (difference between latencies with unimodal and bimodal stimuli). Elements with low variation index are located along the diagonal. Bottom: Probability distribution of unimodal latencies. Left: Probability distribution of bimodal latencies. (F) Scatterplot of power enhancement (z score) during unimodal (ripples or drifting Gabor patches) and bimodal stimulation across responsive electrodes for theta band (4 to 8 Hz, green circles) and alpha band (8 to 16 Hz, black circles) for sustained stimuli. Continuous lines and filled diamonds correspond to visual areas, while dashed lines and open circles correspond to auditory areas. Top right: Normalized probability distribution of the variation index (difference between unimodal and bimodal power enhancements). Bottom and left: Panels showing probability distributions of power enhancement during unimodal and bimodal stimuli, respectively.

  • Fig. 2 Stimulus-related modulation of envelope ICMs.

    Coupling matrices represent the strength of amplitude envelope correlations between functional areas. The labeling of rows and columns, as shown in the top left in (A), applies to all matrices in the figure. On the basis of the anatomical regions (abbreviations as in Fig. 1), these can be grouped in three modalities: visual, somatosensory parietal, and auditory regions (black dark squares in top left matrix). (A) Connectivity during stimulation with ripples (left column, A), drifting Gabor patches (second column, V), and simultaneous presentation of ripples and Gabor patches (third column, AV). Different rows represent different frequency bands. Note that matrices for the high gamma and the high frequency bands are not shown. (B) Connectivity during unimodal (A, V) and bimodal (AV) stimulation with clicks and flashes for different frequency bands (rows). Connections that were not significantly different from the shuffle controls are marked with an “x.” (C) Normalized degree (left) and betweenness (right) for connectivity matrices shown in (A). Each subplot represents the mean and standard error of the respective graph measure associated with auditory (red), visual (blue), and audiovisual (green) stimulation. *P < 0.05; ***P < 0.001. (D) Normalized degree and betweenness for connectivity matrices shown in (B).

  • Fig. 3 Stimulus-related modulation of phase ICMs.

    (A) Matrices from the first to the third column represent the mean imaginary coherence between areas during stimulation with auditory ripples (A), drifting Gabors (V), or both (AV). (B) Connectivity during unimodal (A, V) and bimodal (AV) stimulation with clicks and flashes. In (A) and (B), connections that were not significantly different from the shuffle controls are marked with an “x” in the coupling matrices. (C) Normalized degree and betweenness connectivity matrices shown in (A). **P < 0.01; ***P < 0.001. (D) Normalized degree and betweenness for connectivity matrices shown in (B).

  • Fig. 4 Prestimulus connectivity matrices.

    (A) Envelope ICMs. Left column shows the average matrix across animals of the prestimulus connectivity obtained during the sustained stimulation blocks (pre–R-G). Middle column shows the prestimulus connectivity matrix for the blocks with clicks and flashes (pre–C-F). Right column: Connectivity in the ongoing condition, i.e., in a recording block without intermittent sensory stimulation. Rows represent the frequency bands as defined in Materials and Methods. (B) Phase ICMs. Matrices show imaginary coherence in pre–R-G, pre–C-F, and ongoing activity blocks for the same recordings epochs as in (A).

  • Fig. 5 Graph theoretical analysis of prestimulus connectivity.

    Mean degree, betweenness, and clustering coefficient were used to characterize the ICMs in intervals before stimulus onset. (A to C) Three measures for envelope ICMs during R-G stimuli (orange) and C-F blocks (blue) across frequency bands. Significant differences occur at low frequencies, in particular, theta, alpha, and beta bands. Asterisks represent P < 0.001. (D to F) The graph theoretical measures characterizing the prestimulus intervals in C-F and R-G blocks. The data presented are the means ± SD across animals.

  • Fig. 6 Prestimulus connectivity predicts multisensory effects on response timing and power.

    (A) Correlation between envelope coupling and change in latencies (latV-latAV) for visually responsive sites in the R-G (orange) and C-F (blue) stimulation blocks. Asterisks represent significant correlations (P < 0.01), and error bars represent the standard error of the correlation. (B) Correlation of differences in latency with phase coupling. (C) Correlation between prestimulus envelope coupling and multisensory power enhancement observed with ripples and Gabor patches (R-G). Each element in the matrix represents the strength of the correlation between the prestimulus connectivity in a certain band and the stimulus-related power enhancement in a specific band. Hot colors represent positive correlations, and cold colors represent negative correlations. Nonsignificant correlations (P > 0.01) are masked. (D) Correlation matrix between prestimulus phase coupling and stimulus-related power changes with R-G. (E and F) Same analyses of the relation between prestimulus connectivity and multisensory power enhancement for the stimulation blocks with clicks and flashes (C-F).

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/5/4/eaar7633/DC1

    Fig. S1. Recording approach in the anesthetized ferret.

    Fig. S2. Spectral properties of ongoing and stimulus-related activity.

    Fig. S3. Fraction of responsive sites and multisensory responses.

    Fig. S4. Topography of response power changes for sustained and transient stimuli.

    Fig. S5. Clustering coefficient for stimulus-related connectivity.

    Fig. S6. Contrast index of connectivity matrices during prestimulus conditions.

    Fig. S7. Relation between prestimulus functional connectivity and multisensory effects.

    Fig. S8. Grand mean of connectivity measures as a function of frequency.

  • Supplementary Materials

    This PDF file includes:

    • Fig. S1. Recording approach in the anesthetized ferret.
    • Fig. S2. Spectral properties of ongoing and stimulus-related activity.
    • Fig. S3. Fraction of responsive sites and multisensory responses.
    • Fig. S4. Topography of response power changes for sustained and transient stimuli.
    • Fig. S5. Clustering coefficient for stimulus-related connectivity.
    • Fig. S6. Contrast index of connectivity matrices during prestimulus conditions.
    • Fig. S7. Relation between prestimulus functional connectivity and multisensory effects.
    • Fig. S8. Grand mean of connectivity measures as a function of frequency.

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