Research ArticleNEUROPHYSIOLOGY

Dissociation of broadband high-frequency activity and neuronal firing in the neocortex

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Science Advances  12 Aug 2020:
Vol. 6, no. 33, eabb0977
DOI: 10.1126/sciadv.abb0977
  • Fig. 1 Laminar activity profiles from individual penetrations in V1 and A1.

    Color maps show a CSD superimposed with FPs (left) and a BHA (color map) superimposed with MUA (line plots) profiles (right) in V1 (A) and A1 (C) from a representative session. (A) presents data from V1 recordings during diffuse flash stimulation. (C) shows data from A1 recordings during presentation of broadband noise (100-ms duration). x axes indicate time relative to stimulus onset. y axes represent cortical depth with increasing numbers from superficial to deep layers. Vertical lines indicate sensory events. (B and D) Line plots show the distribution of MUA-BHA cross-correlation coefficients calculated across trials for each penetration of V1 (B) and A1 (D). Box plot presents distribution of the lags obtained from the cross-correlations. Positive values indicate that MUA leads BHA. Shading in the line plot reflects SEM. Central mark and edges in box plots show median and 25th and 75th percentiles. (E and F) show maps of z statistics calculated across trials (n = 137 and 84) for individual V1 (E) and A1 (F) penetration. The statistics values are obtained from a nonparametric pairwise test on MUA (left) and BHA (middle) relative to the prestimulus baseline. Nonsignificant time points are masked (P < 0.05; controlled for multiple comparisons across channels and time with the Benjamini and Yekutieli procedure). Right panels show an overlap (yellow) between the BHA (green) and MUA (red) statistic masks.

  • Fig. 2 Differential laminar distribution of BHA and MUA across experiments in V1.

    (A to D) present V1 data from recordings during diffuse flash stimulation (V1-DF; n = 104 experiments in two animals). (E to H) Data from V1 recordings during free-viewing exploration of visual images [V1-FV; n = 49, same two animals as in (A to D)]. Line plots show the time course of BHA (A and E) and MUA (C and G) response across supragranular, granular, and infragranular (red, green, and blue lines) layers. x axes indicate time relative to stimulus (A, C) or fixation onset (E, G). y axes represent signal change from baseline (i.e., normalized BHA/MUA). Box plots present BHA (B and F) and MUA (D and H) distributions averaged across time after stimulus onset (B and D) and across the entire pre- and postfixation epoch (F and H). Supragranular, granular, and infragranular (S, G, and I) layers are plotted as separate box plots. Box plots indicate 25th percentile, median, and 75th percentile; whiskers extend to extreme values not considered outliers, while outliers are marked with crosses. Shading in line plots reflects SEM. Note the consistently different laminar distributions of BHA and MUA in both experiments. Despite different stimuli, levels of firing, and BHA magnitude across experiments, BHA in the supragranular layers is enhanced relative to that in the granular and infragranular layers, while MUA in supragranular is sparse compared to granular and infragranular. Note also that in the free viewing (E to H), there is substantial saccadic modulations of MUA and BHA across all layers, with a clear pattern of MUA suppression around the time of the saccade (perisaccadic suppression) and MUA increase at the end of the saccade (onset of fixation). Arrows in (A and E) indicate early (solid line) and late (dashed line) BHA components.

  • Fig. 3 Differential laminar distribution of BHA and MUA across experiments in A1.

    (A to D) presents data from A1 recordings during presentation of broadband noise (A1-BBN; duration, 100 ms; n = 26, two animals). (E to H) shows data from A1 recordings during presentation of best frequency tones [A1-BFT; 100-ms duration; n = 26, same two animals as in (A to D)]. Line plots show the time course of BHA (A and E) and MUA (C and G) response across supragranular, granular, and infragranular (red, green, and blue lines) layers. x axes indicate time relative to stimulus (A, C, E, G). y axes represent signal change from baseline (i.e., normalized BHA/MUA). Box plots present BHA (B and F) and MUA (D and H) distributions averaged across time after stimulus onset. Supragranular, granular, and infragranular (S, G, and I) layers are plotted as separate box plots. Box plots indicate 25th percentile, median, and 75th percentile; whiskers extend to extreme values not considered outliers, while outliers are marked with crosses. Shading in line plots reflects SEM. Note the consistently different laminar distributions of BHA and MUA in both experiments. Despite different stimuli (i.e., broadband noise and best frequency tones), BHA in the supragranular layers is enhanced relative to that in the granular and infragranular layers, while MUA in supragranular is sparse compared to granular and infragranular. Arrows in (A and E) indicate early (solid line) and late (dashed line) BHA components.

  • Fig. 4 Laminar contributions to the pial surface BHA signal.

    (A to D) BHA recorded from pial surface, supragranular, granular, and infragranular layers (gray, red, green, and blue, respectively) of (A) V1 during whole-screen flash stimulation (n = 31 experiments). (B) Presentation of broadband noise during A1 recordings (n = 24), (C) free viewing of visual images during V1 recordings (n = 18), and (D) presentation of best frequency pure tones during A1 recordings (n = 24). y axes represent signal change from baseline (i.e., normalized BHA). (E to H) Portions of the amount of variance (adjusted R2) in the pial surface BHA signal explained by each of three different models, containing laminar BHA from either supragranular (red), granular (green), or infragranular (blue) layers as predictors. Colored markers over panels represent cortical depth, which explains most of the variance (KW test across distributions of adjusted R2 values).

  • Fig. 5 Laminar distribution of BHA and MUA in the human prefrontal cortex.

    Line plots show example traces from simultaneous BHA (A and B) and MUA (C and D) recordings during rest in two patients with epilepsy implanted with linear probes in a to-be-resected tissue. Signals were assigned into three a priori depths (1, 150 to 900 μm; 2, 1050 to 1800 μm; and 3, 1950 to 2850 μm) based on known thickness of the cortex (see Materials and Methods). The whole resting data were segmented into 1-s-long intervals (100-ms-long intervals at side of epoch were removed after filtering to avoid contamination of edge effects). The laminar distribution of BHA and MUA was quantified by testing for nonuniformity of BHA and MUA across depths (see Materials and Methods). Box plots present results aggregated across all BHA (A and B) and MUA (C and D) epochs in each patient separately. Box plots indicate 25th percentile, median, and 75th percentile; whiskers extend to extreme values not considered outliers. Outliers are shown as “+” signs.

  • Fig. 6 The effect of PCP on BHA and MUA in the primary auditory cortex.

    (A and B) Box plots present BHA (A) and MUA (B) averaged within the 150-ms-long poststimulus time window before (control) and after systemic administration of PCP (n = 8). Box plots indicate 25th percentile, median, and 75th percentile; whiskers extend to extreme values not considered outliers. (C to F) Line plots show the time course of BHA (C and E) recorded from supragranular, granular, and infragranular (red, green, and blue lines) layers of A1 before (C) and after (E) systemic administration of PCP. (D and F) Concomitant MUA recordings from the same supragranular, granular, and infragranular (red, green, and blue lines) layers before (D) and after (F) systemic administration of PCP. x axis indicates time relative to stimulus onset. y axis represents signal change from baseline, averaged over the 50-ms interval before the stimulus (normalized BHA/MUA). Shading reflects SEM.

Supplementary Materials

  • Supplementary Materials

    Dissociation of broadband high-frequency activity and neuronal firing in the neocortex

    Marcin Leszczyński, Annamaria Barczak, Yoshinao Kajikawa, Istvan Ulbert, Arnaud Y. Falchier, Idan Tal, Saskia Haegens, Lucia Melloni, Robert T. Knight, Charles E. Schroeder

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