What is a Rhythm for the Brain? The Impact of Contextual Temporal Variability on Auditory Perception.

Temporal predictions can be formed and impact perception when sensory timing is fully predictable: for instance, the discrimination of a target sound is enhanced if it is presented on the beat of an isochronous rhythm. However, natural sensory stimuli, like speech or music, are not entirely predictable, but still possess statistical temporal regularities. We investigated whether temporal expectations can be formed in non-fully predictable contexts, and how the temporal variability of sensory contexts affects auditory perception. Specifically, we asked how "rhythmic" an auditory stimulation needs to be in order to observe temporal predictions effects on auditory discrimination performances. In this behavioral auditory oddball experiment, participants listened to auditory sound sequences where the temporal interval between each sound was drawn from gaussian distributions with distinct standard deviations. Participants were asked to discriminate sounds with a deviant pitch in the sequences. Auditory discrimination performances, as measured with deviant sound discrimination accuracy and response times, progressively declined as the temporal variability of the sound sequence increased. Moreover, both global and local temporal statistics impacted auditory perception, suggesting that temporal statistics are promptly integrated to optimize perception. Altogether, these results suggests that temporal predictions can be set up quickly based on the temporal statistics of past sensory events and are robust to a certain amount of temporal variability. Therefore, temporal predictions can be built on sensory stimulations that are not purely periodic nor temporally deterministic.

A New Generation of OPM for High Dynamic and Large Bandwidth MEG: The 4He OPMs-First Applications in Healthy Volunteers.

MagnetoEncephaloGraphy (MEG) provides a measure of electrical activity in the brain at a millisecond time scale. From these signals, one can non-invasively derive the dynamics of brain activity. Conventional MEG systems (SQUID-MEG) use very low temperatures to achieve the necessary sensitivity. This leads to severe experimental and economical limitations. A new generation of MEG sensors is emerging: the optically pumped magnetometers (OPM). In OPM, an atomic gas enclosed in a glass cell is traversed by a laser beam whose modulation depends on the local magnetic field. MAG4Health is developing OPMs using Helium gas (4He-OPM). They operate at room temperature with a large dynamic range and a large frequency bandwidth and output natively a 3D vectorial measure of the magnetic field. In this study, five 4He-OPMs were compared to a classical SQUID-MEG system in a group of 18 volunteers to evaluate their experimental performances. Considering that the 4He-OPMs operate at real room temperature and can be placed directly on the head, our assumption was that 4He-OPMs would provide a reliable recording of physiological magnetic brain activity. Indeed, the results showed that the 4He-OPMs showed very similar results to the classical SQUID-MEG system by taking advantage of a shorter distance to the brain, despite having a lower sensitivity.

Relating neural oscillations to laminar fMRI connectivity in visual cortex.

Laminar functional magnetic resonance imaging (fMRI) holds the potential to study connectivity at the laminar level in humans. Here we analyze simultaneously recorded electroencephalography (EEG) and high-resolution fMRI data to investigate how EEG power modulations, induced by a task with an attentional component, relate to changes in fMRI laminar connectivity between and within brain regions in visual cortex. Our results indicate that our task-induced decrease in beta power relates to an increase in deep-to-deep layer coupling between regions and to an increase in deep/middle-to-superficial layer connectivity within brain regions. The attention-related alpha power decrease predominantly relates to reduced connectivity between deep and superficial layers within brain regions, since, unlike beta power, alpha power was found to be positively correlated to connectivity. We observed no strong relation between laminar connectivity and gamma band oscillations. These results indicate that especially beta band, and to a lesser extent, alpha band oscillations relate to laminar-specific fMRI connectivity. The differential effects for alpha and beta bands indicate that they relate to different feedback-related neural processes that are differentially expressed in intra-region laminar fMRI-based connectivity.

New insights on the ventral attention network: Active suppression and involuntary recruitment during a bimodal task.

Detection of unexpected, yet relevant events is essential in daily life. fMRI studies have revealed the involvement of the ventral attention network (VAN), including the temporo-parietal junction (TPJ), in such process. In this MEG study with 34 participants (17 women), we used a bimodal (visual/auditory) attention task to determine the neuronal dynamics associated with suppression of the activity of the VAN during top-down attention and its recruitment when information from the unattended sensory modality is involuntarily integrated. We observed an anticipatory power increase of alpha/beta oscillations (12-20 Hz, previously associated with functional inhibition) in the VAN following a cue indicating the modality to attend. Stronger VAN power increases were associated with better task performance, suggesting that the VAN suppression prevents shifting attention to distractors. Moreover, the TPJ was synchronized with the frontal eye field in that frequency band, indicating that the dorsal attention network (DAN) might participate in such suppression. Furthermore, we found a 12-20 Hz power decrease and enhanced synchronization, in both the VAN and DAN, when information between sensory modalities was congruent, suggesting an involvement of these networks when attention is involuntarily enhanced due to multisensory integration. Our results show that effective multimodal attentional allocation includes the modulation of the VAN and DAN through upper-alpha/beta oscillations. Altogether these results indicate that the suppressing role of alpha/beta oscillations might operate beyond sensory regions.

Estimates of cortical column orientation improve MEG source inversion.

Determining the anatomical source of brain activity non-invasively measured from EEG or MEG sensors is challenging. In order to simplify the source localization problem, many techniques introduce the assumption that current sources lie on the cortical surface. Another common assumption is that this current flow is orthogonal to the cortical surface, thereby approximating the orientation of cortical columns. However, it is not clear which cortical surface to use to define the current source locations, and normal vectors computed from a single cortical surface may not be the best approximation to the orientation of cortical columns. We compared three different surface location priors and five different approaches for estimating dipole vector orientation, both in simulations and visual and motor evoked MEG responses. We show that models with source locations on the white matter surface and using methods based on establishing correspondences between white matter and pial cortical surfaces dramatically outperform models with source locations on the pial or combined pial/white surfaces and which use methods based on the geometry of a single cortical surface in fitting evoked visual and motor responses. These methods can be easily implemented and adopted in most M/EEG analysis pipelines, with the potential to significantly improve source localization of evoked responses.

Top-Down Control of Alpha Phase Adjustment in Anticipation of Temporally Predictable Visual Stimuli.

Alpha oscillations (8-14 Hz) are proposed to represent an active mechanism of functional inhibition of neuronal processing. Specifically, alpha oscillations are associated with pulses of inhibition repeating every ∼100 msec. Whether alpha phase, similar to alpha power, is under top-down control remains unclear. Moreover, the sources of such putative top-down phase control are unknown. We designed a cross-modal (visual/auditory) attention study in which we used magnetoencephalography to record the brain activity from 34 healthy participants. In each trial, a somatosensory cue indicated whether to attend to either the visual or auditory domain. The timing of the stimulus onset was predictable across trials. We found that, when visual information was attended, anticipatory alpha power was reduced in visual areas, whereas the phase adjusted just before the stimulus onset. Performance in each modality was predicted by the phase of the alpha oscillations previous to stimulus onset. Alpha oscillations in the left pFC appeared to lead the adjustment of alpha phase in visual areas. Finally, alpha phase modulated stimulus-induced gamma activity. Our results confirm that alpha phase can be top-down adjusted in anticipation of predictable stimuli and improve performance. Phase adjustment of the alpha rhythm might serve as a neurophysiological resource for optimizing visual processing when temporal predictions are possible and there is considerable competition between target and distracting stimuli.

Communication between Brain Areas Based on Nested Oscillations.

Unraveling how brain regions communicate is crucial for understanding how the brain processes external and internal information. Neuronal oscillations within and across brain regions have been proposed to play a crucial role in this process. Two main hypotheses have been suggested for routing of information based on oscillations, namely communication through coherence and gating by inhibition. Here, we propose a framework unifying these two hypotheses that is based on recent empirical findings. We discuss a theory in which communication between two regions is established by phase synchronization of oscillations at lower frequencies (<25 Hz), which serve as temporal reference frame for information carried by high-frequency activity (>40 Hz). Our framework, consistent with numerous recent empirical findings, posits that cross-frequency interactions are essential for understanding how large-scale cognitive and perceptual networks operate.

Hippocampal pattern completion is linked to gamma power increases and alpha power decreases during recollection.

How do we retrieve vivid memories upon encountering a simple cue? Computational models suggest that this feat is accomplished by pattern completion processes involving the hippocampus. However, empirical evidence for hippocampal pattern completion and its underlying mechanisms has remained elusive. Here, we recorded direct intracranial EEG as human participants performed an associative memory task. For each study (encoding) and test (retrieval) event, we derived time-frequency resolved representational patterns in the hippocampus and compared the extent of pattern reinstatement for different mnemonic outcomes. Results show that successful associative recognition (AR) yields enhanced event-specific reinstatement of encoding patterns compared to non-associative item recognition (IR). Moreover, we found that gamma power (50-90 Hz) increases - in conjunction with alpha power (8-12 Hz) decreases not only distinguish AR from IR, but also correlate with the level of hippocampal reinstatement. These results link single-shot hippocampal pattern completion to episodic recollection and reveal how oscillatory dynamics in the gamma and alpha bands orchestrate these mnemonic processes.

Directed Communication between Nucleus Accumbens and Neocortex in Humans Is Differentially Supported by Synchronization in the Theta and Alpha Band.

Here, we report evidence for oscillatory bi-directional interactions between the nucleus accumbens and the neocortex in humans. Six patients performed a demanding covert visual attention task while we simultaneously recorded brain activity from deep-brain electrodes implanted in the nucleus accumbens and the surface electroencephalogram (EEG). Both theta and alpha oscillations were strongly coherent with the frontal and parietal EEG during the task. Theta-band coherence increased during processing of the visual stimuli. Granger causality analysis revealed that the nucleus accumbens was communicating with the neocortex primarily in the theta-band, while the cortex was communicating the nucleus accumbens in the alpha-band. These data are consistent with a model, in which theta- and alpha-band oscillations serve dissociable roles: Prior to stimulus processing, the cortex might suppress ongoing processing in the nucleus accumbens by modulating alpha-band activity. Subsequently, upon stimulus presentation, theta oscillations might facilitate the active exchange of stimulus information from the nucleus accumbens to the cortex.

Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep.

During systems-level consolidation, mnemonic representations initially reliant on the hippocampus are thought to migrate to neocortical sites for more permanent storage, with an eminent role of sleep for facilitating this information transfer. Mechanistically, consolidation processes have been hypothesized to rely on systematic interactions between the three cardinal neuronal oscillations characterizing non-rapid eye movement (NREM) sleep. Under global control of de- and hyperpolarizing slow oscillations (SOs), sleep spindles may cluster hippocampal ripples for a precisely timed transfer of local information to the neocortex. We used direct intracranial electroencephalogram recordings from human epilepsy patients during natural sleep to test the assumption that SOs, spindles and ripples are functionally coupled in the hippocampus. Employing cross-frequency phase-amplitude coupling analyses, we found that spindles were modulated by the up-state of SOs. Notably, spindles were found to in turn cluster ripples in their troughs, providing fine-tuned temporal frames for the hypothesized transfer of hippocampal memory traces.

Gamma activity coupled to alpha phase as a mechanism for top-down controlled gating.

Coupling between neural oscillations in different frequency bands has been proposed to coordinate neural processing. In particular, gamma power coupled to alpha phase is proposed to reflect gating of information in the visual system but the existence of such a mechanism remains untested. Here, we recorded ongoing brain activity using magnetoencephalography in subjects who performed a modified Sternberg working memory task in which distractors were presented in the retention interval. During the anticipatory pre-distractor period, we show that the phase of alpha oscillations was coupled with the power of high (80-120Hz) gamma band activity, i.e. gamma power consistently was lower at the trough than at the peak of the alpha cycle (9-12Hz). We further show that high alpha power was associated with weaker gamma power at the trough of the alpha cycle. This result is in line with alpha activity in sensory region implementing a mechanism of pulsed inhibition silencing neuronal firing every ~100 ms.

Oscillatory mechanisms of feedforward and feedback visual processing.

Two recent monkey studies demonstrate that feedforward processing in the visual system is reflected by activity in the 40-90Hz gamma band, whereas feedback is reflected by activity in the 5-18Hz alpha and beta band. These findings can be applied to interpret human electrophysiological activity in complex visual tasks.

Reasoning from transitive premises: an EEG study.

Neuroimaging studies have contributed to a major advance in understanding the neural and cognitive mechanisms underpinning deductive reasoning. However, the dynamics of cognitive events associated with inference making have been largely neglected. Using electroencephalography, the present study aims at describing the rapid sequence of processes involved in performing transitive inference (A B; B C therefore "A C"; with AB meaning "A is to the left of B"). The results indicate that when the second premise can be integrated into the first one (e.g. A B; B C) its processing elicits a P3b component. In contrast, when the second premise cannot be integrated into the first premise (e.g. A B; D C), a P600-like components is elicited. These ERP components are discussed with respect to cognitive expectations.

Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing.

Sensory systems must rely on powerful mechanisms for organizing complex information. We propose a framework in which inhibitory alpha oscillations limit and prioritize neuronal processing. At oscillatory peaks, inhibition prevents neuronal firing. As the inhibition ramps down within a cycle, a set of neuronal representations will activate sequentially according to their respective excitability. Both top-down and bottom-up drives determine excitability; in particular, spatial attention is a major top-down influence. On a shorter time scale, fast recurrent inhibition segments representations in slots 10-30 ms apart, generating gamma-band activity at the population level. The proposed mechanism serves to convert spatially distributed representations in early visual regions to a temporal phase code: that is, 'to-do lists' that can be processed sequentially by downstream regions.

Distinct patterns of brain activity characterise lexical activation and competition in spoken word production.

According to a prominent theory of language production, concepts activate multiple associated words in memory, which enter into competition for selection. However, only a few electrophysiological studies have identified brain responses reflecting competition. Here, we report a magnetoencephalography study in which the activation of competing words was manipulated by presenting pictures (e.g., dog) with distractor words. The distractor and picture name were semantically related (cat), unrelated (pin), or identical (dog). Related distractors are stronger competitors to the picture name because they receive additional activation from the picture relative to other distractors. Picture naming times were longer with related than unrelated and identical distractors. Phase-locked and non-phase-locked activity were distinct but temporally related. Phase-locked activity in left temporal cortex, peaking at 400 ms, was larger on unrelated than related and identical trials, suggesting differential activation of alternative words by the picture-word stimuli. Non-phase-locked activity between roughly 350-650 ms (4-10 Hz) in left superior frontal gyrus was larger on related than unrelated and identical trials, suggesting differential resolution of the competition among the alternatives, as reflected in the naming times. These findings characterise distinct patterns of activity associated with lexical activation and competition, supporting the theory that words are selected by competition.

Medial prefrontal theta phase coupling during spatial memory retrieval.

Memory retrieval is believed to involve a disparate network of areas, including medial prefrontal and medial temporal cortices, but the mechanisms underlying their coordination remain elusive. One suggestion is that oscillatory coherence mediates inter-regional communication, implicating theta phase and theta-gamma phase-amplitude coupling in mnemonic function across species. To examine this hypothesis, we used non-invasive whole-head magnetoencephalography (MEG) as participants retrieved the location of objects encountered within a virtual environment. We demonstrate that, when participants are cued with the image of an object whose location they must subsequently navigate to, there is a significant increase in 4-8 Hz theta power in medial prefrontal cortex (mPFC), and the phase of this oscillation is coupled both with ongoing theta phase in the medial temporal lobe (MTL) and perceptually induced 65-85 Hz gamma amplitude in medial parietal cortex. These results suggest that theta phase coupling between mPFC and MTL and theta-gamma phase-amplitude coupling between mPFC and neocortical regions may play a role in human spatial memory retrieval.

Disabling conditional inferences: an EEG study.

Although the Modus Ponens inference is one of the most basic logical rules, decades of conditional reasoning research show that it is often rejected when people consider stored background knowledge about potential disabling conditions. In the present study we used EEG to identify neural markers of this process. We presented participants with many and few disabler conditionals for which retrieval of disabling conditions was likely or unlikely. As in classic behavioral studies we observed that participants accepted the standard MP conclusion less for conditionals with many disablers. The key finding was that the presentation of the standard MP conclusion also resulted in a more pronounced N2 and less pronounced P3b for the many disabler conditionals. This specific N2/P3b pattern has been linked to the violation and satisfaction of expectations, respectively. Thereby, the present ERP findings support the idea that disabler retrieval lowers reasoners' expectations that the standard MP conclusion can be drawn.

Alpha activity reflects individual abilities to adapt to the environment.

Recent findings suggest that oscillatory alpha activity (7-13Hz) is associated with functional inhibition of sensory regions by filtering incoming information. Accordingly the alpha power in visual regions varies in anticipation of upcoming, predictable stimuli which has consequences for visual processing and subsequent behavior. In covert spatial attention studies it has been demonstrated that performance correlates with the adaptation of alpha power in response to explicit spatial cueing. However it remains unknown whether such an adaptation also occurs in response to implicit statistical properties of a task. In a covert attention switching paradigm, we here show evidence that individuals differ on how they adapt to implicit statistical properties of the task. Subjects whose behavioral performance reflects the implicit change in switch trial likelihood show strong adjustment of anticipatory alpha power lateralization. Most importantly, the stronger the behavioral adjustment to the switch trial likelihood was, the stronger the adjustment of anticipatory posterior alpha lateralization. We conclude that anticipatory spatial attention is reflected in the distribution of posterior alpha band power which is predictive of individual detection performance in response to the implicit statistical properties of the task.

The role of gamma and alpha oscillations for blocking out distraction.

Although alpha activity (10 Hz) is by far the strongest signal produced by the human brain, it has for decades been considered to reflect rest or idling. However, recent studies have clearly demonstrated that alpha activity plays a pivotal role for cognitive processing. Gamma oscillations (> 30 Hz) and their role for cognition have also been the subject of intensive research. While gamma activity is thought to reflect functional processing, alpha oscillations are now thought to reflect functional inhibition in order to suppress the processing of distracting information. In our recent magnetoencephalography study we found that both power and phase of posterior alpha oscillations are top-down modulated in order to prevent the incorporation of predictable distracters in working memory. We further discuss these results here. We additionally show that the processing of the distracters is clearly distinguishable from the processing of the items to be remembered. The former induced a weaker gamma power and evoked a higher alpha activity. The higher the evoked alpha activity, the better the efficiency of distracter suppression which also depends on the pre-distracter alpha power and phase adjustment. Altogether, these results emphasize the protecting role of alpha activity and its remarkable flexibility. This ability to inhibit distracter information is crucial in our complex environment, as illustrated by the difficulties encountered by patients suffering from attentional disorders.