Neuro-oscillatory phase alignment drives speeded multisensory response times: an electro-corticographic investigation

Abstract

Even simple tasks rely on information exchange between functionally distinct and often relatively distant neuronal ensembles. Considerable work indicates oscillatory synchronization through phase alignment is a major agent of inter-regional communication. In the brain, different oscillatory phases correspond to low- and high-excitability states. Optimally aligned phases (or high-excitability states) promote inter-regional communication. Studies have also shown that sensory stimulation can modulate or reset the phase of ongoing cortical oscillations. For example, auditory stimuli can reset the phase of oscillations in visual cortex, influencing processing of a simultaneous visual stimulus. Such cross-regional phase reset represents a candidate mechanism for aligning oscillatory phase for inter-regional communication. Here, we explored the role of local and inter-regional phase alignment in driving a well established behavioral correlate of multisensory integration: the redundant target effect (RTE), which refers to the fact that responses to multisensory inputs are substantially faster than to unisensory stimuli. In a speeded detection task, human epileptic patients (N = 3) responded to unisensory (auditory or visual) and multisensory (audiovisual) stimuli with a button press, while electrocorticography was recorded over auditory and motor regions. Visual stimulation significantly modulated auditory activity via phase reset in the delta and theta bands. During the period between stimulation and subsequent motor response, transient synchronization between auditory and motor regions was observed. Phase synchrony to multisensory inputs was faster than to unisensory stimulation. This sensorimotor phase alignment correlated with behavior such that stronger synchrony was associated with faster responses, linking the commonly observed RTE with phase alignment across a sensorimotor network.

Keywords: ECoG; EEG; motor; multisensory; oscillations; synchrony.

Figure 1.

Electrode locations and modulation of activity in auditory cortex. A, Projection of the electrodes of interest on MNI brain template for the three subjects. Electrodes over auditory and motor cortices are indicated in dark green and orange, respectively. B, Evoked potentials recorded over auditory cortex. The activity following AV, A, and V stimuli are plotted in red, green, and blue, respectively; the black line depicts the sum of the ERPs evoked in the unisensory conditions (A + V). Ribbon-plot, below ERP traces, represents statistical results [comparison of each condition against baseline and between conditions following the additive model (AV vs (A + V); in black)]. Corrected significant p values are represented as solid color, and uncorrected p values appear transparent. C, PCI following audiovisual (left), auditory (middle), and visual, (right) stimuli. D, Multisensory effects on PCI assessed using the additive model: AV versus (A + V). C, D, Solid colors with black contours represent statistically significant values corrected for multiple comparisons.

Figure 2.

Power modulations in auditory cortex. Power modulation following audiovisual (left), auditory-alone (middle), and visual-alone (right) stimuli. Solid colors with black contours represent statistically significant values corrected for multiple comparisons.

Figure 3.

Behavior and motor-related activations. A, For each participant RT distribution is plotted. Bars represent the amount of trials with RTs included in a 20 ms bin. Red, green, and blue correspond, respectively, to audiovisual, auditory-alone, and visual-alone conditions. B, Motor-related activity in response to AV (left), A (middle), and V (right) stimuli. For each subject the first row depicts single-trial representations of activity, in microvolts, recorded over motor cortex, from −100 to 700 ms. Single trials were sorted per RT (represented by the black line). The second row represents induced power modulation (relative to the entire period) time locked to the response, from −350 to 350 ms, for frequencies ranging from 3 to 50 and 70 to 125 Hz. Corrected significant values are depicted with solid colors and black contours.

Figure 4.

Phase-locking activity between auditory and motor cortices time lock to stimulus onset. A, PLV plot for AV (left), A (middle), and V (right) conditions. B, Multisensory effects on PLV assessed using the additive model: AV versus (A + V). Color bars indicate PLV value (A) and difference in PLV value between AV and (A + V) (B). A, B, Solid contoured colors represent statistically significant values corrected for multiple comparisons.

Figure 5.

Phase-locking activity between auditory and motor cortices time lock to the response. A, PLV plot for AV (left), A (middle), and V (right) conditions. B, Multisensory effects on PLV assessed using the additive model: AV versus (A + V). Color bars indicate PLV value (A) and difference in PLV value between AV and (A + V) (B). A, B, Solid contoured colors represent statistically significant values after correction for multiple comparisons.

Figure 6.

Relationship between phase alignment in auditory cortex, phase locking between auditory and motor cortices, and response times (each row represents a participant). A, Correlation between PCI and PLV. B, Correlation between PLV and RTs. Each point on the x-axis of the scatter plots represents the estimated phase alignment index and/or corresponding RTs for 10% of the trials, binned per RT (audiovisual in red, auditory-alone in green, visual-alone in blue). Fitting lines are plotted plain if statistics on the slopes were significant and/or at trend, dashed otherwise.