Benjamin Morillon

Intrinsic Connectivity Networks, Alpha Oscillations, and Tonic Alertness: A Simultaneous Electroencephalography/Functional Magnetic Resonance Imaging Study

Trial-by-trial variability in perceptual performance on identical stimuli has been related to spontaneous fluctuations in ongoing activity of intrinsic functional connectivity networks (ICNs). In a paradigm requiring sustained vigilance for instance, we previously observed that higher prestimulus activity in a cingulo-insular-thalamic network facilitated subsequent perception. Here, we test our proposed interpretation that this network underpins maintenance of tonic alertness. We used simultaneous acquisition of functional magnetic resonance imaging (fMRI) and electroencephalography (EEG) in the absence of any paradigm to test an ensuing hypothesis, namely that spontaneous fluctuations in this ICN′s activity (as measured by fMRI) should show a positive correlation with the electrical signatures of tonic alertness (as recorded by concurrent EEG). We found in human subjects (19 male, 7 female) that activity in a network comprising dorsal anterior cingulate cortex, anterior insula, anterior prefrontal cortex and thalamus is positively correlated with global field power (GFP) of upper alpha band (10–12 Hz) oscillations, the most consistent electrical index of tonic alertness. Conversely, and in line with earlier findings, alpha band power was negatively correlated with activity in another ICN, the so-called dorsal attention network which is most prominently involved in selective spatial attention. We propose that the cingulo-insular-thalamic network serves maintaining tonic alertness through generalized expression of cortical alpha oscillations. Attention is mediated by activity in other systems, e.g., the dorsal attention network for space, selectively disrupts alertness-related suppression and hence manifests as local attenuation of alpha activity.

Dual Neural Routing of Visual Facilitation in Speech Processing

Viewing our interlocutor facilitates speech perception, unlike for instance when we telephone. Several neural routes and mechanisms could account for this phenomenon. Using magnetoencephalography, we show that when seeing the interlocutor, latencies of auditory responses (M100) are the shorter the more predictable speech is from visual input, whether the auditory signal was congruent or not. Incongruence of auditory and visual input affected auditory responses ∼20 ms after latency shortening was detected, indicating that initial content-dependent auditory facilitation by vision is followed by a feedback signal that reflects the error between expected and received auditory input (prediction error). We then used functional magnetic resonance imaging and confirmed that distinct routes of visual information to auditory processing underlie these two functional mechanisms. Functional connectivity between visual motion and auditory areas depended on the degree of visual predictability, whereas connectivity between the superior temporal sulcus and both auditory and visual motion areas was driven by audiovisual (AV) incongruence. These results establish two distinct mechanisms by which the brain uses potentially predictive visual information to improve auditory perception. A fast direct corticocortical pathway conveys visual motion parameters to auditory cortex, and a slower and indirect feedback pathway signals the error between visual prediction and auditory input.

The contribution of frequency-specific activity to hierarchical information processing in the human auditory cortex

The fact that feed-forward and top-down propagation of sensory information use distinct frequency bands is an appealing assumption for which evidence remains scarce. Here we obtain human depth recordings from two auditory cortical regions in both hemispheres, while subjects listen to sentences, and show that information travels in each direction using separate frequency channels. Bottom-up and top-down propagation dominates in γ- and δ–β (<40 Hz) bands, respectively. The predominance of low frequencies for top-down information transfer is confirmed by cross-regional frequency coupling, which indicates that the power of γ-activity in A1 is modulated by the phase of δ–β activity sampled from association auditory cortex (AAC). This cross-regional coupling effect is absent in the opposite direction. Finally, we show that information transfer does not proceed continuously but by time windows where bottom-up or top-down processing alternatively dominates. These findings suggest that the brain uses both frequency- and time-division multiplexing to optimize directional information transfer.

Alpha-Band Phase Synchrony Is Related to Activity in the Fronto-Parietal Adaptive Control Network

Neural oscillations in the alpha band (8–12 Hz) are increasingly viewed as an active inhibitory mechanism that gates and controls sensory information processing as a function of cognitive relevance. Extending this view, phase synchronization of alpha oscillations across distant cortical regions could regulate integration of information. Here, we investigated whether such long-range cross-region coupling in the alpha band is intrinsically and selectively linked to activity in a distinct functionally specialized brain network. If so, this would provide new insight into the functional role of alpha band phase synchrony. We adapted the phase-locking value to assess fluctuations in synchrony that occur over time in ongoing activity. Concurrent EEG and functional magnetic resonance imaging (fMRI) were recorded during resting wakefulness in 26 human subjects. Fluctuations in global synchrony in the upper alpha band correlated positively with activity in several prefrontal and parietal regions (as measured by fMRI). fMRI intrinsic connectivity analysis confirmed that these regions correspond to the well known fronto-parietal (FP) network. Spectral correlations with this networks activity confirmed that no other frequency band showed equivalent results. This selective association supports an intrinsic relation between large-scale alpha phase synchrony and cognitive functions associated with the FP network. This network has been suggested to implement phasic aspects of top-down modulation such as initiation and change in moment-to-moment control. Mechanistically, long-range upper alpha band synchrony is well suited to support these functions. Complementing our previous findings that related alpha oscillation power to neural structures serving tonic control, the current findings link alpha phase synchrony to neural structures underpinning phasic control of alertness and task requirements.

Neurophysiological origin of human brain asymmetry for speech and language

The physiological basis of human cerebral asymmetry for language remains mysterious. We have used simultaneous physiological and anatomical measurements to investigate the issue. Concentrating on neural oscillatory activity in speech-specific frequency bands and exploring interactions between gestural (motor) and auditory-evoked activity, we find, in the absence of language-related processing, that left auditory, somatosensory, articulatory motor, and inferior parietal cortices show specific, lateralized, speech-related physiological properties. With the addition of ecologically valid audiovisual stimulation, activity in auditory cortex synchronizes with left-dominant input from the motor cortex at frequencies corresponding to syllabic, but not phonemic, speech rhythms. Our results support theories of language lateralization that posit a major role for intrinsic, hardwired perceptuomotor processing in syllabic parsing and are compatible both with the evolutionary view that speech arose from a combination of syllable-sized vocalizations and meaningful hand gestures and with developmental observations suggesting phonemic analysis is a developmentally acquired process.

Motor contributions to the temporal precision of auditory attention

In temporal—or dynamic—attending theory, it is proposed that motor activity helps to synchronize temporal fluctuations of attention with the timing of events in a task-relevant stream, thus facilitating sensory selection. Here we develop a mechanistic behavioural account for this theory by asking human participants to track a slow reference beat, by noiseless finger pressing, while extracting auditory target tones delivered on-beat and interleaved with distractors. We find that overt rhythmic motor activity improves the segmentation of auditory information by enhancing sensitivity to target tones while actively suppressing distractor tones. This effect is triggered by cyclic fluctuations in sensory gain locked to individual motor acts, scales parametrically with the temporal predictability of sensory events and depends on the temporal alignment between motor and attention fluctuations. Together, these findings reveal how top-down influences associated with a rhythmic motor routine sharpen sensory representations, enacting auditory ‘active sensing’.

Predictive motor control of sensory dynamics in auditory active sensing

Neuronal oscillations present potential physiological substrates for brain operations that require temporal prediction. We review this idea in the context of auditory perception. Using speech as an exemplar, we illustrate how hierarchically organized oscillations can be used to parse and encode complex input streams. We then consider the motor system as a major source of rhythms (temporal priors) in auditory processing, that act in concert with attention to sharpen sensory representations and link them across areas. We discuss the circuits that could mediate this audio-motor interaction, notably the potential role of the somatosensory system. Finally, we reposition temporal predictions in the context of internal models, discussing how they interact with feature-based or spatial predictions. We argue that complementary predictions interact synergistically according to the organizational principles of each sensory system, forming multidimensional filters crucial to perception.

Asymmetric Function of Theta and Gamma Activity in Syllable Processing: An Intra-Cortical Study

Low-gamma (25–45 Hz) and theta (4–8 Hz) oscillations are proposed to underpin the integration of phonemic and syllabic information, respectively. How these two scales of analysis split functions across hemispheres is unclear. We analyzed cortical responses from an epileptic patient with a rare bilateral electrode implantation (stereotactic EEG) in primary (A1/BA41 and A2/BA42) and association auditory cortices (BA22). Using time-frequency analyses, we confirmed the dominance of a 5–6 Hz theta activity in right and of a low-gamma (25–45 Hz) activity in left primary auditory cortices (A1/A2), during both resting state and syllable processing. We further detected high-theta (7–8 Hz) resting activity in left primary, but also associative auditory regions. In left BA22, its phase correlated with high-gamma induced power. Such a hierarchical relationship across theta and gamma frequency bands (theta/gamma phase-amplitude coupling) could index the process by which the neural code shifts from stimulus feature- to phonological-encoding, and is associated with the transition from evoked to induced power responses. These data suggest that theta and gamma activity in right and left auditory cortices bear different functions. They support a scheme where slow parsing of the acoustic information dominates in right hemisphere at a syllabic (5–6 Hz) rate, and left auditory cortex exhibits a more complex cascade of oscillations, reflecting the possible extraction of transient acoustic cues at a fast (~25–45 Hz) rate, subsequently integrated at a slower, e.g., syllabic one. Slow oscillations could functionally participate to speech processing by structuring gamma activity in left BA22, where abstract percepts emerge.

Lateralization of Speech Production Starts in Sensory Cortices—A Possible Sensory Origin of Cerebral Left Dominance for Speech

Speech production is a left-lateralized brain function, which could arise from a left dominance either in speech executive or sensory processes or both. Using functional magnetic resonance imaging in healthy subjects, we show that sensory cortices already lateralize when speaking is intended, while the frontal cortex only lateralizes when speech is acted out. The sequence of lateralization, first temporal then frontal lateralization, suggests that the functional lateralization of the auditory cortex could drive hemispheric specialization for speech production.

Impaired auditory sampling in dyslexia: further evidence from combined fMRI and EEG

The aim of the present study was to explore auditory cortical oscillation properties in developmental dyslexia. We recorded cortical activity in 17 dyslexic participants and 15 matched controls using simultaneous EEG and fMRI during passive viewing of an audiovisual movie. We compared the distribution of brain oscillations in the delta, theta and gamma ranges over left and right auditory cortices. In controls, our results are consistent with the hypothesis that there is a dominance of gamma oscillations in the left hemisphere and a dominance of delta-theta oscillations in the right hemisphere. In dyslexics, we did not find such an interaction, but similar oscillations in both hemispheres. Thus, our results confirm that the primary cortical disruption in dyslexia lies in a lack of hemispheric specialization for gamma oscillations, which might disrupt the representation of or the access to phonemic units.