Neural tracking of visual periodic motion.

Periodicity is a fundamental property of biological systems, including human movement systems. Periodic movements support displacements of the body in the environment as well as interactions and communication between individuals. Here, we use electroencephalography (EEG) to investigate the neural tracking of visual periodic motion, and more specifically, the relevance of spatiotemporal information contained at and between their turning points. We compared EEG responses to visual sinusoidal oscillations versus nonlinear Rayleigh oscillations, which are both typical of human movements. These oscillations contain the same spatiotemporal information at their turning points but differ between turning points, with Rayleigh oscillations having an earlier peak velocity, shown to increase an individual's capacity to produce accurately synchronized movements. EEG analyses highlighted the relevance of spatiotemporal information between the turning points by showing that the brain precisely tracks subtle differences in velocity profiles, as indicated by earlier EEG responses for Rayleigh oscillations. The results suggest that the brain is particularly responsive to velocity peaks in visual periodic motion, supporting their role in conveying behaviorally relevant timing information at a neurophysiological level. The results also suggest key functions of neural oscillations in the Alpha and Beta frequency bands, particularly in the right hemisphere. Together, these findings provide insights into the neural mechanisms underpinning the processing of visual periodic motion and the critical role of velocity peaks in enabling proficient visuomotor synchronization.

Spatial and temporal (non)binding of audiovisual rhythms in sensorimotor synchronisation.

Human movement synchronisation with moving objects strongly relies on visual input. However, auditory information also plays an important role, since real environments are intrinsically multimodal. We used electroencephalography (EEG) frequency tagging to investigate the selective neural processing and integration of visual and auditory information during motor tracking and tested the effects of spatial and temporal congruency between audiovisual modalities. EEG was recorded while participants tracked with their index finger a red flickering (rate fV = 15 Hz) dot oscillating horizontally on a screen. The simultaneous auditory stimulus was modulated in pitch (rate fA = 32 Hz) and lateralised between left and right audio channels to induce perception of a periodic displacement of the sound source. Audiovisual congruency was manipulated in terms of space in Experiment 1 (no motion, same direction or opposite direction), and timing in Experiment 2 (no delay, medium delay or large delay). For both experiments, significant EEG responses were elicited at fV and fA tagging frequencies. It was also hypothesised that intermodulation products corresponding to the nonlinear integration of visual and auditory stimuli at frequencies fV ± fA would be elicited, due to audiovisual integration, especially in Congruent conditions. However, these components were not observed. Moreover, synchronisation and EEG results were not influenced by congruency manipulations, which invites further exploration of the conditions which may modulate audiovisual processing and the motor tracking of moving objects.

Infants show enhanced neural responses to musical meter frequencies beyond low-level features.

Music listening often entails spontaneous perception and body movement to a periodic pulse-like meter. There is increasing evidence that this cross-cultural ability relates to neural processes that selectively enhance metric periodicities, even when these periodicities are not prominent in the acoustic stimulus. However, whether these neural processes emerge early in development remains largely unknown. Here, we recorded the electroencephalogram (EEG) of 20 healthy 5- to 6-month-old infants, while they were exposed to two rhythms known to induce the perception of meter consistently across Western adults. One rhythm contained prominent acoustic periodicities corresponding to the meter, whereas the other rhythm did not. Infants showed significantly enhanced representations of meter periodicities in their EEG responses to both rhythms. This effect is unlikely to reflect the tracking of salient acoustic features in the stimulus, as it was observed irrespective of the prominence of meter periodicities in the audio signals. Moreover, as previously observed in adults, the neural enhancement of meter was greater when the rhythm was delivered by low-pitched sounds. Together, these findings indicate that the endogenous enhancement of metric periodicities beyond low-level acoustic features is a neural property that is already present soon after birth. These high-level neural processes could set the stage for internal representations of musical meter that are critical for human movement coordination during rhythmic musical behavior. RESEARCH HIGHLIGHTS: 5- to 6-month-old infants were presented with auditory rhythms that induce the perception of a periodic pulse-like meter in adults. Infants showed selective enhancement of EEG activity at meter-related frequencies irrespective of the prominence of these frequencies in the stimulus. Responses at meter-related frequencies were boosted when the rhythm was conveyed by bass sounds. High-level neural processes that transform rhythmic auditory stimuli into internal meter templates emerge early after birth.

Partially Preserved Processing of Musical Rhythms in REM but Not in NREM Sleep.

The extent of high-level perceptual processing during sleep remains controversial. In wakefulness, perception of periodicities supports the emergence of high-order representations such as the pulse-like meter perceived while listening to music. Electroencephalography (EEG) frequency-tagged responses elicited at envelope frequencies of musical rhythms have been shown to provide a neural representation of rhythm processing. Specifically, responses at frequencies corresponding to the perceived meter are enhanced over responses at meter-unrelated frequencies. This selective enhancement must rely on higher-level perceptual processes, as it occurs even in irregular (i.e., syncopated) rhythms where meter frequencies are not prominent input features, thus ruling out acoustic confounds. We recorded EEG while presenting a regular (unsyncopated) and an irregular (syncopated) rhythm across sleep stages and wakefulness. Our results show that frequency-tagged responses at meter-related frequencies of the rhythms were selectively enhanced during wakefulness but attenuated across sleep states. Most importantly, this selective attenuation occurred even in response to the irregular rhythm, where meter-related frequencies were not prominent in the stimulus, thus suggesting that neural processes selectively enhancing meter-related frequencies during wakefulness are weakened during rapid eye movement (REM) and further suppressed in non-rapid eye movement (NREM) sleep. These results indicate preserved processing of low-level acoustic properties but limited higher-order processing of auditory rhythms during sleep.

Dynamic modulation of cortico-muscular coupling during real and imagined sensorimotor synchronisation.

People have a natural and intrinsic ability to coordinate body movements with rhythms surrounding them, known as sensorimotor synchronisation. This can be observed in daily environments, when dancing or singing along with music, or spontaneously walking, talking or applauding in synchrony with one another. However, the neurophysiological mechanisms underlying accurately synchronised movement with selected rhythms in the environment remain unclear. Here we studied real and imagined sensorimotor synchronisation with interleaved auditory and visual rhythms using cortico-muscular coherence (CMC) to better understand the processes underlying the preparation and execution of synchronised movement. Electroencephalography (EEG), electromyography (EMG) from the finger flexors, and continuous force signals were recorded in 20 participants during tapping and imagined tapping with discrete stimulus sequences consisting of alternating auditory beeps and visual flashes. The results show that the synchronisation between cortical and muscular activity in the beta (14-38 Hz) frequency band becomes time-locked to the taps executed in synchrony with the visual and auditory stimuli. Dynamic modulation in CMC also occurred when participants imagined tapping with the visual stimuli, but with lower amplitude and a different temporal profile compared to real tapping. These results suggest that CMC does not only reflect changes related to the production of the synchronised movement, but also to its preparation, which appears heightened under higher attentional demands imposed when synchronising with the visual stimuli. These findings highlight a critical role of beta band neural oscillations in the cortical-muscular coupling underlying sensorimotor synchronisation.

Free-Field Cortical Steady-State Evoked Potentials in Cochlear Implant Users.

Auditory steady-state evoked potentials (SS-EPs) are phase-locked neural responses to periodic stimuli, believed to reflect specific neural generators. As an objective measure, steady-state responses have been used in different clinical settings, including measuring hearing thresholds of normal and hearing-impaired subjects. Recent studies are in favor of recording these responses as a part of the cochlear implant (CI) device-fitting procedure. Considering these potential benefits, the goals of the present study were to assess the feasibility of recording free-field SS-EPs in CI users and to compare their characteristics between CI users and controls. By taking advantage of a recently developed dual-frequency tagging method, we attempted to record subcortical and cortical SS-EPs from adult CI users and controls and measured reliable subcortical and cortical SS-EPs in the control group. Independent component analysis (ICA) was used to remove CI stimulation artifacts, yet subcortical responses of several CIs were heavily contaminated by these artifacts. Consequently, only cortical SS-EPs were compared between groups, which were found to be larger in the controls. The lower cortical SS-EPs' amplitude in CI users might indicate a reduction in neural synchrony evoked by the modulation rate of the auditory input across different neural assemblies in the auditory pathway. The brain topographies of cortical auditory SS-EPs, the time course of cortical responses, and the reconstructed cortical maps were highly similar between groups, confirming their neural origin and possibility to obtain such responses also in CI recipients. As for subcortical SS-EPs, our results highlight a need for sophisticated denoising algorithms to pinpoint and remove artifactual components from the biological response.

Neural tracking of the musical beat is enhanced by low-frequency sounds.

Music makes us move, and using bass instruments to build the rhythmic foundations of music is especially effective at inducing people to dance to periodic pulse-like beats. Here, we show that this culturally widespread practice may exploit a neurophysiological mechanism whereby low-frequency sounds shape the neural representations of rhythmic input by boosting selective locking to the beat. Cortical activity was captured using electroencephalography (EEG) while participants listened to a regular rhythm or to a relatively complex syncopated rhythm conveyed either by low tones (130 Hz) or high tones (1236.8 Hz). We found that cortical activity at the frequency of the perceived beat is selectively enhanced compared with other frequencies in the EEG spectrum when rhythms are conveyed by bass sounds. This effect is unlikely to arise from early cochlear processes, as revealed by auditory physiological modeling, and was particularly pronounced for the complex rhythm requiring endogenous generation of the beat. The effect is likewise not attributable to differences in perceived loudness between low and high tones, as a control experiment manipulating sound intensity alone did not yield similar results. Finally, the privileged role of bass sounds is contingent on allocation of attentional resources to the temporal properties of the stimulus, as revealed by a further control experiment examining the role of a behavioral task. Together, our results provide a neurobiological basis for the convention of using bass instruments to carry the rhythmic foundations of music and to drive people to move to the beat.

Accent-induced Modulation of Neural and Movement Patterns during Spontaneous Synchronization to Auditory Rhythms.

Human rhythmic movements spontaneously synchronize with auditory rhythms at various frequency ratios. The emergence of more complex relationships-for instance, frequency ratios of 1:2 and 1:3-is enhanced by adding a congruent accentuation pattern (binary for 1:2 and ternary for 1:3), resulting in a 1:1 movement-accentuation relationship. However, this benefit of accentuation on movement synchronization appears to be stronger for the ternary pattern than for the binary pattern. Here, we investigated whether this difference in accent-induced movement synchronization may be related to a difference in the neural tracking of these accentuation profiles. Accented and control unaccented auditory sequences were presented to participants who concurrently produced finger taps at their preferred frequency, and spontaneous movement synchronization was measured. EEG was recorded during passive listening to each auditory sequence. The results revealed that enhanced movement synchronization with ternary accentuation was accompanied by enhanced neural tracking of this pattern. Larger EEG responses at the accentuation frequency were found for the ternary pattern compared with the binary pattern. Moreover, the amplitude of accent-induced EEG responses was positively correlated with the magnitude of accent-induced movement synchronization across participants. Altogether, these findings show that the dynamics of spontaneous auditory-motor synchronization is strongly driven by the multi-time-scale sensory processing of auditory rhythms, highlighting the importance of considering neural responses to rhythmic sequences for understanding and enhancing synchronization performance.

Neural tracking and integration of 'self' and 'other' in improvised interpersonal coordination.

Humans coordinate their movements with one another in a range of everyday activities and skill domains. Optimal joint performance requires the continuous anticipation of and adaptation to each other's movements, especially when actions are spontaneous rather than pre-planned. Here we employ dual-EEG and frequency-tagging techniques to investigate how the neural tracking of self- and other-generated movements supports interpersonal coordination during improvised motion. LEDs flickering at 5.7 and 7.7 Hz were attached to participants' index fingers in 28 dyads as they produced novel patterns of synchronous horizontal forearm movements. EEG responses at these frequencies revealed enhanced neural tracking of self-generated movement when leading and of other-generated movements when following. A marker of self-other integration at 13.4 Hz (inter-modulation frequency of 5.7 and 7.7 Hz) peaked when no leader was designated, and mutual adaptation and movement synchrony were maximal. Furthermore, the amplitude of EEG responses reflected differences in the capacity of dyads to synchronize their movements, offering a neurophysiologically grounded perspective for understanding perceptual-motor mechanisms underlying joint action.

Visuomotor Correlates of Conflict Expectation in the Context of Motor Decisions.

Many behaviors require choosing between conflicting options competing against each other in visuomotor areas. Such choices can benefit from top-down control processes engaging frontal areas in advance of conflict when it is anticipated. Yet, very little is known about how this proactive control system shapes the visuomotor competition. Here, we used electroencephalography in human subjects (male and female) to identify the visual and motor correlates of conflict expectation in a version of the Eriksen Flanker task that required left or right responses according to the direction of a central target arrow surrounded by congruent or incongruent (conflicting) flankers. Visual conflict was either highly expected (it occurred in 80% of trials; mostly incongruent blocks) or very unlikely (20% of trials; mostly congruent blocks). We evaluated selective attention in the visual cortex by recording target- and flanker-related steady-state visual-evoked potentials (SSVEPs) and probed action selection by measuring response-locked potentials (RLPs) in the motor cortex. Conflict expectation enhanced accuracy in incongruent trials, but this improvement occurred at the cost of speed in congruent trials. Intriguingly, this behavioral adjustment occurred while visuomotor activity was less finely tuned: target-related SSVEPs were smaller while flanker-related SSVEPs were higher in mostly incongruent blocks than in mostly congruent blocks, and incongruent trials were associated with larger RLPs in the ipsilateral (nonselected) motor cortex. Hence, our data suggest that conflict expectation recruits control processes that augment the tolerance for inappropriate visuomotor activations (rather than processes that downregulate their amplitude), allowing for overflow activity to occur without having it turn into the selection of an incorrect response.SIGNIFICANCE STATEMENT Motor choices made in front of discordant visual information are more accurate when conflict can be anticipated, probably due to the engagement of top-down control from frontal areas. How this control system modulates activity within visual and motor areas is unknown. Here, we show that, when control processes are recruited in anticipation of conflict, as evidenced by higher midfrontal theta activity, visuomotor activity is less finely tuned: visual processing of the goal-relevant location was reduced and the motor cortex displayed more inappropriate activations, compared with when conflict was unlikely. We argue that conflict expectation is associated with an expansion of the distance-to-selection threshold, improving accuracy while the need for online control of visuomotor activity is reduced.

Neural bases of rhythmic entrainment in humans: critical transformation between cortical and lower-level representations of auditory rhythm.

The spontaneous ability to entrain to meter periodicities is central to music perception and production across cultures. There is increasing evidence that this ability involves selective neural responses to meter-related frequencies. This phenomenon has been observed in the human auditory cortex, yet it could be the product of evolutionarily older lower-level properties of brainstem auditory neurons, as suggested by recent recordings from rodent midbrain. We addressed this question by taking advantage of a new method to simultaneously record human EEG activity originating from cortical and lower-level sources, in the form of slow (< 20 Hz) and fast (> 150 Hz) responses to auditory rhythms. Cortical responses showed increased amplitudes at meter-related frequencies compared to meter-unrelated frequencies, regardless of the prominence of the meter-related frequencies in the modulation spectrum of the rhythmic inputs. In contrast, frequency-following responses showed increased amplitudes at meter-related frequencies only in rhythms with prominent meter-related frequencies in the input but not for a more complex rhythm requiring more endogenous generation of the meter. This interaction with rhythm complexity suggests that the selective enhancement of meter-related frequencies does not fully rely on subcortical auditory properties, but is critically shaped at the cortical level, possibly through functional connections between the auditory cortex and other, movement-related, brain structures. This process of temporal selection would thus enable endogenous and motor entrainment to emerge with substantial flexibility and invariance with respect to the rhythmic input in humans in contrast with non-human animals.

EEG Frequency-Tagging and Input-Output Comparison in Rhythm Perception.

The combination of frequency-tagging with electroencephalography (EEG) has recently proved fruitful for understanding the perception of beat and meter in musical rhythm, a common behavior shared by humans of all cultures. EEG frequency-tagging allows the objective measurement of input-output transforms to investigate beat perception, its modulation by exogenous and endogenous factors, development, and neural basis. Recent doubt has been raised about the validity of comparing frequency-domain representations of auditory rhythmic stimuli and corresponding EEG responses, assuming that it implies a one-to-one mapping between the envelope of the rhythmic input and the neural output, and that it neglects the sensitivity of frequency-domain representations to acoustic features making up the rhythms. Here we argue that these elements actually reinforce the strengths of the approach. The obvious fact that acoustic features influence the frequency spectrum of the sound envelope precisely justifies taking into consideration the sounds used to generate a beat percept for interpreting neural responses to auditory rhythms. Most importantly, the many-to-one relationship between rhythmic input and perceived beat actually validates an approach that objectively measures the input-output transforms underlying the perceptual categorization of rhythmic inputs. Hence, provided that a number of potential pitfalls and fallacies are avoided, EEG frequency-tagging to study input-output relationships appears valuable for understanding rhythm perception.

Frequency tagging to track the neural processing of contrast in fast, continuous sound sequences.

The human auditory system presents a remarkable ability to detect rapid changes in fast, continuous acoustic sequences, as best illustrated in speech and music. However, the neural processing of rapid auditory contrast remains largely unclear, probably due to the lack of methods to objectively dissociate the response components specifically related to the contrast from the other components in response to the sequence of fast continuous sounds. To overcome this issue, we tested a novel use of the frequency-tagging approach allowing contrast-specific neural responses to be tracked based on their expected frequencies. The EEG was recorded while participants listened to 40-s sequences of sounds presented at 8Hz. A tone or interaural time contrast was embedded every fifth sound (AAAAB), such that a response observed in the EEG at exactly 8 Hz/5 (1.6 Hz) or harmonics should be the signature of contrast processing by neural populations. Contrast-related responses were successfully identified, even in the case of very fine contrasts. Moreover, analysis of the time course of the responses revealed a stable amplitude over repetitions of the AAAAB patterns in the sequence, except for the response to perceptually salient contrasts that showed a buildup and decay across repetitions of the sounds. Overall, this new combination of frequency-tagging with an oddball design provides a valuable complement to the classic, transient, evoked potentials approach, especially in the context of rapid auditory information. Specifically, we provide objective evidence on the neural processing of contrast embedded in fast, continuous sound sequences.NEW & NOTEWORTHY Recent theories suggest that the basis of neurodevelopmental auditory disorders such as dyslexia might be an impaired processing of fast auditory changes, highlighting how the encoding of rapid acoustic information is critical for auditory communication. Here, we present a novel electrophysiological approach to capture in humans neural markers of contrasts in fast continuous tone sequences. Contrast-specific responses were successfully identified, even for very fine contrasts, providing direct insight on the encoding of rapid auditory information.

Enhanced brainstem and cortical encoding of sound during synchronized movement.

Movement to a steady beat has been widely studied as a model of alignment of motor outputs on sensory inputs. However, how the encoding of sensory inputs is shaped during synchronized movements along the sensory pathway remains unknown. To investigate this, we simultaneously recorded brainstem and cortical electro-encephalographic activity while participants listened to periodic amplitude-modulated tones. Participants listened either without moving or while tapping in sync on every second beat. Cortical responses were identified at the envelope modulation rate (beat frequency), whereas brainstem responses were identified at the partials frequencies of the chord and at their modulation by the beat frequency (sidebands). During sensorimotor synchronization, cortical responses at beat frequency were larger than during passive listening. Importantly, brainstem responses were also enhanced, with a selective amplification of the sidebands, in particular at the lower-pitched tone of the chord, and no significant correlation with electromyographic measures at tapping frequency. These findings provide first evidence for an online gain in the cortical and subcortical encoding of sounds during synchronized movement, selective to behavior-relevant sound features. Moreover, the frequency-tagging method to isolate concurrent brainstem and cortical activities even during actual movements appears promising to reveal coordinated processes along the human auditory pathway.

Capturing with EEG the neural entrainment and coupling underlying sensorimotor synchronization to the beat.

Synchronizing movements with rhythmic inputs requires tight coupling of sensory and motor neural processes. Here, using a novel approach based on the recording of steady-state-evoked potentials (SS-EPs), we examine how distant brain areas supporting these processes coordinate their dynamics. The electroencephalogram was recorded while subjects listened to a 2.4-Hz auditory beat and tapped their hand on every second beat. When subjects tapped to the beat, the EEG was characterized by a 2.4-Hz SS-EP compatible with beat-related entrainment and a 1.2-Hz SS-EP compatible with movement-related entrainment, based on the results of source analysis. Most importantly, when compared with passive listening of the beat, we found evidence suggesting an interaction between sensory- and motor-related activities when subjects tapped to the beat, in the form of (1) additional SS-EP appearing at 3.6 Hz, compatible with a nonlinear product of sensorimotor integration; (2) phase coupling of beat- and movement-related activities; and (3) selective enhancement of beat-related activities over the hemisphere contralateral to the tapping, suggesting a top-down effect of movement-related activities on auditory beat processing. Taken together, our results are compatible with the view that rhythmic sensorimotor synchronization is supported by a dynamic coupling of sensory and motor related activities.

Body movement selectively shapes the neural representation of musical rhythms.

It is increasingly recognized that motor routines dynamically shape the processing of sensory inflow (e.g., when hand movements are used to feel a texture or identify an object). In the present research, we captured the shaping of auditory perception by movement in humans by taking advantage of a specific context: music. Participants listened to a repeated rhythmical sequence before and after moving their bodies to this rhythm in a specific meter. We found that the brain responses to the rhythm (as recorded with electroencephalography) after body movement were significantly enhanced at frequencies related to the meter to which the participants had moved. These results provide evidence that body movement can selectively shape the subsequent internal representation of auditory rhythms.

Selective neuronal entrainment to the beat and meter embedded in a musical rhythm.

Fundamental to the experience of music, beat and meter perception refers to the perception of periodicities while listening to music occurring within the frequency range of musical tempo. Here, we explored the spontaneous building of beat and meter hypothesized to emerge from the selective entrainment of neuronal populations at beat and meter frequencies. The electroencephalogram (EEG) was recorded while human participants listened to rhythms consisting of short sounds alternating with silences to induce a spontaneous perception of beat and meter. We found that the rhythmic stimuli elicited multiple steady state-evoked potentials (SS-EPs) observed in the EEG spectrum at frequencies corresponding to the rhythmic pattern envelope. Most importantly, the amplitude of the SS-EPs obtained at beat and meter frequencies were selectively enhanced even though the acoustic energy was not necessarily predominant at these frequencies. Furthermore, accelerating the tempo of the rhythmic stimuli so as to move away from the range of frequencies at which beats are usually perceived impaired the selective enhancement of SS-EPs at these frequencies. The observation that beat- and meter-related SS-EPs are selectively enhanced at frequencies compatible with beat and meter perception indicates that these responses do not merely reflect the physical structure of the sound envelope but, instead, reflect the spontaneous emergence of an internal representation of beat, possibly through a mechanism of selective neuronal entrainment within a resonance frequency range. Taken together, these results suggest that musical rhythms constitute a unique context to gain insight on general mechanisms of entrainment, from the neuronal level to individual level.

Tagging the neuronal entrainment to beat and meter.

Feeling the beat and meter is fundamental to the experience of music. However, how these periodicities are represented in the brain remains largely unknown. Here, we test whether this function emerges from the entrainment of neurons resonating to the beat and meter. We recorded the electroencephalogram while participants listened to a musical beat and imagined a binary or a ternary meter on this beat (i.e., a march or a waltz). We found that the beat elicits a sustained periodic EEG response tuned to the beat frequency. Most importantly, we found that meter imagery elicits an additional frequency tuned to the corresponding metric interpretation of this beat. These results provide compelling evidence that neural entrainment to beat and meter can be captured directly in the electroencephalogram. More generally, our results suggest that music constitutes a unique context to explore entrainment phenomena in dynamic cognitive processing at the level of neural networks.