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.

Brain networks underlying conscious tactile perception of textures as revealed using the velvet hand illusion

“…The statistical threshold for the spatial extent test was set at p < .05, family-wise error (FWE)-corrected for multiple comparisons over the whole brain when the height threshold was set at p < .001 The human S1 is involved in various aspects of conscious tactile perception, such as the detection and localization of stimuli (Auksztulewicz et al, 2012;Blankenburg et al, 2006;Hirvonen & Palva, 2016;Meador et al, 2002). Brain activation during the velvet hand illusion (strong illusion relative to weak illusion, Si -Wi) in the group analysis.…”

“…As activity in the PO is associated with the magnitude of the texture percept (Eck et al, 2016;Kitada et al, 2005), the bottom-up processing of texture information from the S1 to PO may occur (Hsiao, Johnson, & Twombly, 1993;James, Kim, & Fisher, 2007;Sathian, 2016;Sathian et al, 2011). Other studies have also examined the neural substrates associated with conscious detection of tactile stimuli (Auksztulewicz, Spitzer, & Blankenburg, 2012;Hirvonen & Palva, 2016;Linkenkaer-Hansen, Nikulin, Palva, Ilmoniemi, & Palva, 2004;Meador et al, 2017;Meador, Ray, Echauz, Loring, & Vachtsevanos, 2002;Monto, Palva, Voipio, & Palva, 2008). Previous studies regarding tactile illusions have demonstrated that S1 is associated with illusory mislocalization of tactile sensations (Blankenburg et al, 2006;Bufalari, Di Russo, & Aglioti, 2014;Chen, Friedman, & Roe, 2003).…”

The Role of Local and Large-Scale Neuronal Synchronization in Human Cognition

“…Furthermore, sustained phase locking of ongoing neuronal activity to somatosensory stimulus and a transient increase in the strength of oscillation amplitudes predicted also whether weak stimuli presented at the threshold of detection were consciously perceived (Hirvonen and Palva 2016;Palva et al 2005b) (Fig. 1a-b).…”

“…Several methods such as beamformers (Gross et al 2001), low resolution electromagnetic tomography (LORETA) (Pascual-Marqui et al 2011), and minimumnorm estimation (MNE) (Hamalainen and Ilmoniemi 1994;Lin et al 2006) have been developed for source reconstruction. Indeed, a large body of source reconstruction-based MEG studies have shown that the amplitudes of local cortical oscillations, which reflect synchronization in the local neuronal populations, are correlated with attention (Händel et al 2011;Rouhinen et al 2013;Zumer et al 2014), perception (Haegens et al 2011;Hirvonen and Palva 2016), and WM (Bonnefond and Jensen 2012;Honkanen et al 2015;Palva et al 2011;Roux et al 2012) and hence with many distinct cognitive functions.…”

“…(e) Template brain defining different brain systems: SI, primary somatosensory area; SII, secondary somatosensory area; SM, somatomotor system; FP&DAN, fronto-parietal & dorsal attention network. Modified from ref (Hirvonen and Palva 2016) capacity limitations of visual attention ( Fig. 2a) (Rouhinen et al 2013).…”