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. © 2019 Elsevier Inc

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

Dynamic modulation of beta band cortico-muscular coupling induced by audio-visual rhythms

Human movements often spontaneously fall into synchrony with auditory and visual environmental rhythms. Related behavioral studies have shown that motor responses are automatically and unintentionally coupled with external rhythmic stimuli. However, the neurophysiological processes underlying such motor entrainment remain largely unknown. Here we investigated with electroencephalography (EEG) and electromyography (EMG) the modulation of neural and muscular activity induced by periodic audio and/or visual sequences. The sequences were presented at either 1 Hz or 2 Hz while participants maintained constant finger pressure on a force sensor. The results revealed that although there was no change of amplitude in participants’ EMG in response to the sequences, the synchronization between EMG and EEG recorded over motor areas in the beta (12–40 Hz) frequency band was dynamically modulated, with maximal coherence occurring about 100 ms before each stimulus. These modulations in beta EEG–EMG motor coherence were found for the 2 Hz audio-visual sequences, confirming at a neurophysiological level the enhancement of motor entrainment with multimodal rhythms that fall within preferred perceptual and movement frequency ranges. Our findings identify beta band cortico-muscular coupling as a potential underlying mechanism of motor entrainment, further elucidating the nature of the link between sensory and motor systems in humans

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

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

Measuring neural entrainment to beat and meter in infants : effects of music background

Caregivers often engage in musical interactions with their infants. For example, parents across cultures sing lullabies and playsongs to their infants from birth. Behavioral studies indicate that infants not only extract beat information, but also group these beats into metrical hierarchies by as early as 6 months of age. However, it is not known how this is accomplished in the infant brain. An EEG frequency-tagging approach has been used successfully with adults to measure neural entrainment to auditory rhythms. The current study is the first to use this technique with infants in order to investigate how infants' brains encode rhythms. Furthermore, we examine how infant and parent music background is associated with individual differences in rhythm encoding. In Experiment 1, EEG was recorded while 7-month-old infants listened to an ambiguous rhythmic pattern that could be perceived to be in two different meters. In Experiment 2, EEG was recorded while 15-month-old infants listened to a rhythmic pattern with an unambiguous meter. In both age groups, information about music background (parent music training, infant music classes, hours of music listening) was collected. Both age groups showed clear EEG responses frequency-locked to the rhythms, at frequencies corresponding to both beat and meter. For the younger infants (Experiment 1), the amplitudes at duple meter frequencies were selectively enhanced for infants enrolled in music classes compared to those who had not engaged in such classes. For the older infants (Experiment 2), amplitudes at beat and meter frequencies were larger for infants with musically-trained compared to musically-untrained parents. These results suggest that the frequency-tagging method is sensitive to individual differences in beat and meter processing in infancy and could be used to track developmental changes

TREKiSM Issue 39

November-December 198

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 ( 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

Intracerebral evidence of rhythm transform in the human auditory cortex

Musical entrainment is shared by all human cultures and the perception of a periodic beat is a cornerstone of this entrainment behavior. Here, we investigated whether beat perception might have its roots in the earliest stages of auditory cortical processing. Local field potentials were recorded from 8 patients implanted with depth-electrodes in Heschl’s gyrus and the planum temporale (55 recording sites in total), usually considered as human primary and secondary auditory cortices. Using a frequency-tagging approach, we show that both low-frequency (30 Hz) neural activities in these structures faithfully track auditory rhythms through frequency-locking to the rhythm envelope. A selective gain in amplitude of the response frequency-locked to the beat frequency was observed for the low-frequency activities but not for the high-frequency activities, and was sharper in the planum temporale, especially for the more challenging syncopated rhythm. Hence, this gain process is not systematic in all activities produced in these areas and depends on the complexity of the rhythmic input. Moreover, this gain was disrupted when the rhythm was presented at fast speed, revealing low-pass response properties which could account for the propensity to perceive a beat only within the musical tempo range. Together, these observations show that, even though part of these neural transforms of rhythms could already take place in subcortical auditory processes, the earliest auditory cortical processes shape the neural representation of rhythmic inputs in favor of the emergence of a periodic 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