Brett L. Foster, Vinitha Rangarajan, William R. Shirer, Josef Parvizi 

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Intrinsic and Task-Dependent Coupling of Neuronal Population Activity in Human Parietal Cortex  Brett L. Foster, Vinitha Rangarajan, William R. Shirer, Josef Parvizi  Neuron  Volume 86, Issue 2, Pages 578-590 (April 2015) DOI: 10.1016/j.neuron.2015.03.018 Copyright © 2015 Elsevier Inc. Terms and Conditions

Figure 1 Parietal Subregions, Electrode Locations, Experimental Task, and Task Responses (A) Lateral and medial parietal lobe was divided into seven putative subregions. Lateral subregions were: supramarginal gyrus (SMG), angular gyrus (AG), intraparietal sulcus (IPS), and superior parietal lobule (SPL). Medial subregions were: precuneus cortex (PrCC), posterior cingulate cortex (PCC), and retrosplenial cortex (RSC). For group analyses, we combined PCC and RSC recording sites (RSC/PCC; see Supplemental Experimental Procedures). Sulci shown are: post-central sulcus (pcs), intra-parietal sulcus (ips), transverse occipital sulcus (tos), marginal branch (mg), cingulate sulcus (cgs), parieto-occipital sulcus (pos), and calcarine sulcus (cs). (B) Lateral and medial views of electrode locations in left parietal cortex for all subjects normalized to a common brain (MNI). Highlighted boundaries demarcate left lateral and medial posterior parietal cortex. (C) Subjects performed a simple task requiring true/false judgments of visually presented statements or equations as previously employed (Foster et al., 2012). Bar graphs show mean HFB response (with SEM) across conditions for each parietal region of interest (D, lateral; E, medial) across all subjects. While dorsal parietal regions (IPS and SPL) display some similarity, most striking is the similar profile of HFB response between RSC/PCC and AG across conditions. See also Figures S1 and S2. Neuron 2015 86, 578-590DOI: (10.1016/j.neuron.2015.03.018) Copyright © 2015 Elsevier Inc. Terms and Conditions

Figure 2 Correlated HFB Trial Responses between PCC and AG (A) Medial view of electrode sites for S3, with a PCC seed electrode highlighted. (B) Lateral view of electrode sites in S3, where color indicates the correlation value of task responses with respect to the PCC seed electrode in (A). (C) HFB responses for all trials (n = 178) across a single experimental run for the PCC electrode in (A). Each trial response reflects the mean HFB response for the time window 400–900 ms post-stimulus presentation. Right panel shows all trials for each condition, recapitulating the response profile of group data in Figure 1. (D) Single-trial HFB responses for the AG electrode in (B) from the same experimental data as in (C). (E) Time series of trial responses from (C) and (D) reflecting PCC and AG, respectively, display a strong positive correlation. Scatter plot displays all trial responses for PCC versus AG. See also Figure S3. Neuron 2015 86, 578-590DOI: (10.1016/j.neuron.2015.03.018) Copyright © 2015 Elsevier Inc. Terms and Conditions

Figure 3 Consistent Subregional Correlation across Subjects and Task Runs (A) Task correlation matrices for all parietal electrode pairs are shown for each subject (correlations averaged across two task runs). (B) Mean task correlation values between parietal subregions across subjects are shown for the first (left) and second (right) task runs. Correlation matrices for each task run show a highly similar pattern of correlation between regions (Run-1 versus Run-2 matrix similarity, r = 0.91, p < 0.001, n = 21), whereby correlations are most pronounced between RSC/PCC and AG. (C) Mean RSC/PCC-AG correlation (with SEM) across subjects is shown for each task condition. Mean condition correlations suggest that all task conditions comodulated RSC/PCC and AG HFB responses, with the self-episodic condition producing the greatest correlation values (main effect of condition on RSC/PCC-AG correlation F(5, 405) = 9.11, p < 0.001). See also Figure S6. Neuron 2015 86, 578-590DOI: (10.1016/j.neuron.2015.03.018) Copyright © 2015 Elsevier Inc. Terms and Conditions

Figure 4 Relative Timing of HFB Response Onset during Episodic Retrieval (A) Histograms display the distribution of HFB ROL difference latencies (i.e., ROL delay), where each region of interest is compared to RSC/PCC, for the self-episodic condition. Each observation is therefore the HFB ROL difference, for a single trial, between a given RSC/PCC site and a given AG (top left), SPL (top right), visual (bottom left), or motor (bottom right) site. (B) Probability density functions for each ROL difference distribution. These distributions suggest that compared to RSC/PCC, AG showed no lag or lead bias (delay) in response onset timing, unlike other control regions. (C) Schematic representation of latency distributions (A and B), which suggest a sequence of HFB response onsets during episodic retrieval, where visual regions closely precede the near simultaneous onset of RSC/PCC and AG, followed by the engagement of SPL and finally motor cortex. See also Figures S1, S4, S5, and S6. Neuron 2015 86, 578-590DOI: (10.1016/j.neuron.2015.03.018) Copyright © 2015 Elsevier Inc. Terms and Conditions

Figure 5 Resting-State Analysis of Spontaneous ECoG Data (A–C) To obtain a slow time-varying HFB signal the raw time series (A) is filtered in the HFB range (70–180 Hz) and the amplitude is extracted (B). The spontaneous HFB amplitude is then low-pass filtered below 1 Hz to obtain a slow time-varying HFB signal (C, example of 60 s time series from a larger 5 min dataset). (D) Medial and lateral view of electrode sites in S2, with a medial PCC seed electrode highlighted, and the corresponding correlation values in lateral parietal cortex (only) interpolated onto the cortical surface. For the PCC seed, there is a selective and significant correlation with AG. (E) The slow modulation of other canonical frequency bands was also studied for the same seed region. Only the low beta range (Beta-1) displayed similar, though less focal, significant correlation with AG. The significance of correlations was determined by time series permutation testing and was corrected for multiple comparisons using false discovery rate (p < 0.01). See also Figure S7. Neuron 2015 86, 578-590DOI: (10.1016/j.neuron.2015.03.018) Copyright © 2015 Elsevier Inc. Terms and Conditions

Figure 6 Similarity of ECoG Correlation Patterns across Task, Rest, and Sleep States (A) Correlation values for task, rest, and sleep states are shown for all subjects on a shared cortical surface. Correlations are relative to a consistent RSC/PCC seed location in each subject (seed). Task data reflect trial-based correlation of HFB amplitude response, whereas rest and sleep data reflect correlation of spontaneous slow (<1 Hz) fluctuations of HFB amplitude. Across all three states, a strikingly similar pattern of correlation with the AG is observed. (B) Mean HFB amplitude response (400–900 ms post stimulus onset) in LPC across all subjects during the self-episodic condition also displays a similar pattern of activation. (C) To directly compare the pattern of connectivity among task, rest, and sleep states, we computed the similarity between correlation matrices across each state for each subject. Example correlation matrices are shown for S3 (note outlined column in each reflects the data used for (B); i.e., a medial seed location and all lateral site correlations). (D) Scatter plots show the similarity (correlation) between states for the data shown in (C) (note: to control for correlations being driven by local within region similarity, we only included the medial-lateral correlation pairs [n = 187], e.g., AG-AG or PCC-PCC pairs excluded and PCC-AG or RSC-SPL included; see Figure S8 for all pairs). Across comparisons we see a striking positive correlation between states, which is most pronounced between rest and sleep. (E) Across subjects the similarity of connectivity between states is remarkably consistent. Plot shows the between-state similarity (correlation value with 95% CI) for each subject and the associated correlation value for p = 0.01 based on permutation testing (S1-S3 pairs n = 196, 180, 187). See also Figures S7 and S8. Neuron 2015 86, 578-590DOI: (10.1016/j.neuron.2015.03.018) Copyright © 2015 Elsevier Inc. Terms and Conditions

Figure 7 Similarity of ECoG and fMRI Resting-State Connectivity (A) Resting-state ECoG data are shown for an example PCC seed electrode in S3. Based on the seed region in PCC, slow (<1 Hz) HFB amplitude is correlated significantly and selectively with AG (significant electrodes show white fill color). (B) Resting-state fMRI data for S3 is shown for the same seed location but with full brain voxel-wise correlation. ECoG electrode locations are overlaid to show correspondence between modalities, whereby significantly correlated electrodes co-locate with significantly correlated voxel clusters. (C) For a more comprehensive and quantitative comparison, we correlated parietal connectivity matrices for rsECoG and rsfMRI data. Plot shows the correlation value and 95% confidence interval for connectivity comparisons between rsECoG and rsfMRI in each subject (gray boxes show significance level p = 0.01 based on permutation testing). Modalities were matched by extracting fMRI time series from ROI defined by each subject’s electrode locations (S1-S3 pairs n = 595, 351, 378). Neuron 2015 86, 578-590DOI: (10.1016/j.neuron.2015.03.018) Copyright © 2015 Elsevier Inc. Terms and Conditions

Figure 8 Similar Parcellation Boundaries in rsECoG and rsfMRI (A) Electrode locations for the medial and lateral surface are shown for S1 (note: electrodes beyond parietal lobe are shown for completeness). Seed electrodes of interest are highlighted for PCC (medial, white fill), SMG (lateral, blue fill), and AG (lateral, red fill). To capture an example of regional and network parcellation for both modalities, we show local and distal correlation profiles for the inferior parietal lobule (IPL, SMG→AG). (B) Emulating the approach of Cohen et al. (2008) and more recently Wig et al. (2014), top panels show the correlation value between each seed region (1–6) for rsECoG (left) and rsfMRI (right) data, based on the same seed locations. Both modalities display a shift in connectivity that reflects a lack of correlation (boundary) between SMG and AG, consistent with DMN organization. In addition, when comparing each IPL seed region to the target seed in PCC (bottom), there is a strong increase in correlation values for both modalities (ECoG, left; fMRI, right) as the IPL seed location transitions into the AG, consistent with DMN organization. Neuron 2015 86, 578-590DOI: (10.1016/j.neuron.2015.03.018) Copyright © 2015 Elsevier Inc. Terms and Conditions