Cortical localization of phase and amplitude dynamics predicting access to somatosensory awareness

Abstract

Neural dynamics leading to conscious sensory perception have remained enigmatic in despite of large interest. Human functional magnetic resonance imaging (fMRI) studies have revealed that a co-activation of sensory and frontoparietal areas is crucial for conscious sensory perception in the several second time-scale of BOLD signal fluctuations. Electrophysiological recordings with magneto- and electroencephalography (MEG and EEG) and intracranial EEG (iEEG) have shown that event related responses (ERs), phase-locking of neuronal activity, and oscillation amplitude modulations in sub-second timescales are greater for consciously perceived than for unperceived stimuli. The cortical sources of ER and oscillation dynamics predicting the conscious perception have, however, remained unclear because these prior studies have utilized MEG/EEG sensor-level analyses or iEEG with limited neuroanatomical coverage. We used a somatosensory detection task, magnetoencephalography (MEG), and cortically constrained source reconstruction to identify the cortical areas where ERs, local poststimulus amplitudes and phase-locking of neuronal activity are predictive of the conscious access of somatosensory information. We show here that strengthened ERs, phase-locking to stimulus onset (SL), and induced oscillations amplitude modulations all predicted conscious somatosensory perception, but the most robust and widespread of these was SL that was sustained in low-alpha (6-10 Hz) band. The strength of SL and to a lesser extent that of ER predicted conscious perception in the somatosensory, lateral and medial frontal, posterior parietal, and in the cingulate cortex. These data suggest that a rapid phase-reorganization and concurrent oscillation amplitude modulations in these areas play an instrumental role in the emergence of a conscious percept.

Keywords: MEG; conscious; cortex; oscillation; perception; somatosensory; source.

Figure 1

Evoked responses (ER) of broad‐band (1–45 Hz) filtered MEG data differ for perceived (Hit) and unperceived (Miss) stimuli. A) A fraction of the 400 brain areas (parcels) in which the ER was stronger (P+) than in the prestimulus baseline (BL) period separately for perceived stimuli (Hits (blue)) and unperceived stimuli (Misses (red)) as well as for their difference (Cyan) (Wilcoxon signed rank test, P < 0.05, corrected). The stimulus onset is at 0 ms. B) The cortical areas in which ER was stronger for Hits compared with Misses (Wilcoxon signed rank test, P < 0.05, FDR corrected) displayed in inflated cortical surface. Colors of the parcels indicate average strength of the ER over a selected time‐window. Primary somatosensory (SI), secondary somatosensory (SII), supplementary motor area (SMA), and primary motor area (MI) are shown with bold text. Boundaries depict functional connectivity networks as identified from fMRI based functional connectivity network [Yeo et al., 2011]; frontoparietal together with dorsal attentional network (FP/DAN, blue), ventral attentional network (VAN, purple) and sensorimotor network (SM, green). Parcels are indicated with acronyms. Template brain points to the positions of functional systems and important parcels. Acronyms for the brain areas are: aCi = anterior cingulate, iprCS = inferior precentral sulcus, iFG = inferior frontal gyrus, iFS = inferior frontal sulcus, INS = insula, iTG = inferior temporal gyrus, intPS = intaparietal sulcus, mCi = middle‐cingulate, mFG = middle‐frontal gyrus, mFS= middle frontal sulcus, sPG = superior parietal gyrus, sTS = superior temporal sulcus, pCi = posterior cingulate, poCS = postcentral sulcus, sFG = superior frontal sulcus, sprCS = superior precentral sulcus, sPG = superior parietal gyrus, sTS = superior temporal sulcus. C) The relative strength of ER compared with baseline separately for Hits (solid line) and Misses (dashed line) averaged over contralateral SM (green), FP/DAN (blue), and VAN (purple). The lines above indicate significant difference between the Hit and Miss trials (Wilcoxon signed rank test, P < 0.05, FDR corrected).

Figure 2

Broad‐band amplitude (A) and stimulus‐locking (SL) are stronger for Hits than for Misses. A) Fraction of brain areas (parcels) in which the amplitude of broad‐band activity was stronger (P+) or weaker (P−) than in the prestimulus baseline separately for Hits (blue), Misses (red) and for their difference (cyan) (Wilcoxon signed rank test, P < 0.05, corrected). B) Fraction of brain areas (parcels) in which the phase‐locking of broad‐band activity to stimulus onset (stimulus‐locking, SL) was stronger (P+) than in the prestimulus baseline. C) The cortical areas in which the broad‐band amplitude was stronger for Hits than for Misses (Wilcoxon signed rank test, P < 0.05, FDR corrected) displayed in inflated cortical surface. Color indicates the average amplitude values in the selected time‐window for the current parcel. Labels and acronyms as in Figure 1B. D) The cortical areas in which SL was stronger for Hits than Misses displayed in inflated cortical surface. Color indicates the average PLF values in the selected time‐window for the current parcel. Acronyms for the brain areas: prCN = precuneus, subPS = subparietal sulcus. Borders and rest of the acronyms as in Figure 1B.

Figure 3

The strength of ER and SL are not dependent on the position in the Hit‐Miss behavioral series. A) Behavioral data of 2.5 min from a representative subject showing that behavioral performance is temporally clustered into sequences of Hits (blue) and Misses (red). Different Colors indicate stimulus positions in the behavioral sequence. The last Miss before Hit is indicated with magenta and the first Hit after Miss with cyan. The rest of the Hits are indicated with blue and rest of the Misses with red. B) Temporal autocorrelations in the behavioral series as estimated with DFA exponent α displayed separately for each subject as well as exponents for the surrogate data. C) The relative strength of ER in the contralateral SI for Hits and Misses separately for stimuli in the different positions in the behavioral sequence. Colors as in A. Black lines indicate statistically significant difference between Hits and Misses in the middle of the sequence and grey lines between the first Hits and last Misses (P < 0.05, Wilcoxon signed rank test, FDR corrected). D) The relative strengths of SL for Hits and Misses in different positions in the behavioral series as displayed in C.

Figure 4

The strengths of broad‐band amplitude and SL are correlated with RTs. A) Oscillation amplitudes averaged over SM, FP/DAN, and VAN separately for trials with fast, intermediate, and slow RTs. Lines above indicate significant difference between fast and slow RT trials (Wilcoxon signed ranked test, P < 0.05, corrected) B) SL as in A.

Figure 5

Spectral characteristics of SL. A) Time‐frequency representation (TFR) of narrow‐band SL. The color scale shows the fraction of brain parcels that were positively (P⁺ _P) modulated (Wilcoxon signed rank test, P < 0.01, FDR corrected) as the function of time and frequency for Hits (left), Misses (middle) and for their difference (right). B) The cortical regions in which SL was significantly stronger for Hits than for Misses in the selected TF‐ROI. The color indicates the positive fraction (P⁺ _TF) of time‐frequency elements in which modulation was observed in the selected ROI (Wilcoxon signed rank test, P < 0.01, FDR corrected). For labels, borders, and acronyms see Figure 1B.

Figure 6

Spectral characteristics of induced amplitude modulations. A) TFR of the oscillation amplitude modulations for Hits, Misses and for their difference. The color scale shows the fraction of brain areas in which amplitudes were positively (P⁺ _P) or negatively ( $P_{\mathrm{P}}^{-}$) modulated (Wilcoxon signed rank test, P < 0.05, corrected). B) The cortical areas in which oscillation amplitudes were stronger for Hits than for Misses. Color indicates positive ( $P_{\text{TF}}^{+}$) or negative ( $P_{\text{TF}}^{-}$) fraction of time‐frequency elements in which modulation was observed in the selected TF‐ROI (Wilcoxon signed rank test, P < 0.05, FDR corrected). For labels, borders, and acronyms see Figure 1B.