A Cortical Mechanism Linking Saliency Detection and Motor Reactivity in Rhesus Monkeys.

Sudden and surprising sensory events trigger neural processes that swiftly adjust behavior. To study the phylogenesis and the mechanism of this phenomenon, we trained two male rhesus monkeys to keep a cursor inside a visual target by exerting force on an isometric joystick. We examined the effect of surprising auditory stimuli on exerted force, scalp electroencephalographic (EEG) activity, and local field potentials (LFPs) recorded from the dorsolateral prefrontal cortex. Auditory stimuli elicited (1) a biphasic modulation of isometric force, a transient decrease followed by a corrective tonic increase, and (2) EEG and LFP deflections dominated by two large negative-positive waves (N70 and P130). The EEG potential was symmetrical and maximal at the scalp vertex, highly reminiscent of the human "vertex potential." Electrocortical potentials and force were tightly coupled: the P130 amplitude predicted the magnitude of the corrective force increase, particularly in the LFPs recorded from deep rather than superficial cortical layers. These results disclose a phylogenetically preserved corticomotor mechanism supporting adaptive behavior in response to salient sensory events.Significance Statement Survival in the natural world depends on an animal's capacity to adapt ongoing behavior to abrupt unexpected events. To study the neural mechanisms underlying this capacity, we trained monkeys to apply constant force on a joystick while we recorded their brain activity from the scalp and the prefrontal cortex contralateral to the hand holding the joystick. Unexpected auditory stimuli elicited a biphasic force modulation: a transient reduction followed by a corrective adjustment. The same stimuli also elicited EEG and LFP responses, dominated by a biphasic wave that predicted the magnitude of the behavioral adjustment. These results disclose a phylogenetically preserved corticomotor mechanism supporting adaptive behavior in response to unexpected events.

Cortico-cerebellar audio-motor regions coordinate self and other in musical joint action.

Joint music performance requires flexible sensorimotor coordination between self and other. Cognitive and sensory parameters of joint action-such as shared knowledge or temporal (a)synchrony-influence this coordination by shifting the balance between self-other segregation and integration. To investigate the neural bases of these parameters and their interaction during joint action, we asked pianists to play on an MR-compatible piano, in duet with a partner outside of the scanner room. Motor knowledge of the partner's musical part and the temporal compatibility of the partner's action feedback were manipulated. First, we found stronger activity and functional connectivity within cortico-cerebellar audio-motor networks when pianists had practiced their partner's part before. This indicates that they simulated and anticipated the auditory feedback of the partner by virtue of an internal model. Second, we observed stronger cerebellar activity and reduced behavioral adaptation when pianists encountered subtle asynchronies between these model-based anticipations and the perceived sensory outcome of (familiar) partner actions, indicating a shift towards self-other segregation. These combined findings demonstrate that cortico-cerebellar audio-motor networks link motor knowledge and other-produced sounds depending on cognitive and sensory factors of the joint performance, and play a crucial role in balancing self-other integration and segregation.

Spontaneous dyadic behavior predicts the emergence of interpersonal neural synchrony.

Synchronization of neural activity across brains - Interpersonal Neural Synchrony (INS) - is emerging as a powerful marker of social interaction that predicts success of multi-person coordination, communication, and cooperation. As the origins of INS are poorly understood, we tested whether and how INS might emerge from spontaneous dyadic behavior. We recorded neural activity (EEG) and human behavior (full-body kinematics, eye movements, and facial expressions) while dyads of participants were instructed to look at each other without speaking or making co-verbal gestures. We made four fundamental observations. First, despite the absence of a structured social task, INS emerged spontaneously only when participants were able to see each other. Second, we show that such spontaneous INS, comprising specific spectral and topographic profiles, did not merely reflect intra-personal modulations of neural activity, but it rather reflected real-time and dyad-specific coupling of neural activities. Third, using state-of-art video-image processing and deep learning, we extracted the temporal unfolding of three notable social behavioral cues - body movement, eye contact, and smiling - and demonstrated that these behaviors also spontaneously synchronized within dyads. Fourth, we probed the correlates of INS in such synchronized social behaviors. Using cross-correlation and Granger causality analyses, we show that synchronized social behaviors anticipate and in fact Granger cause INS. These results provide proof-of-concept evidence for studying interpersonal neural and behavioral synchrony under natural and unconstrained conditions. Most importantly, the results suggest that INS could be conceptualized as an emergent property of two coupled neural systems: an entrainment phenomenon, promoted by real-time dyadic behavior.

Ultralow-frequency neural entrainment to pain.

Nervous systems exploit regularities in the sensory environment to predict sensory input, adjust behavior, and thereby maximize fitness. Entrainment of neural oscillations allows retaining temporal regularities of sensory information, a prerequisite for prediction. Entrainment has been extensively described at the frequencies of periodic inputs most commonly present in visual and auditory landscapes (e.g., >0.5 Hz). An open question is whether neural entrainment also occurs for regularities at much longer timescales. Here, we exploited the fact that the temporal dynamics of thermal stimuli in natural environment can unfold very slowly. We show that ultralow-frequency neural oscillations preserved a long-lasting trace of sensory information through neural entrainment to periodic thermo-nociceptive input as low as 0.1 Hz. Importantly, revealing the functional significance of this phenomenon, both power and phase of the entrainment predicted individual pain sensitivity. In contrast, periodic auditory input at the same ultralow frequency did not entrain ultralow-frequency oscillations. These results demonstrate that a functionally significant neural entrainment can occur at temporal scales far longer than those commonly explored. The non-supramodal nature of our results suggests that ultralow-frequency entrainment might be tuned to the temporal scale of the statistical regularities characteristic of different sensory modalities.

Sex-related communicative functions of voice spectral energy in human chorusing.

Music is a human communicative art whose evolutionary origins may lie in capacities that support cooperation and/or competition. A mixed account favouring simultaneous cooperation and competition draws on analogous interactive displays produced by collectively signalling non-human animals (e.g. crickets and frogs). In these displays, rhythmically coordinated calls serve as a beacon whereby groups of males 'cooperatively' attract potential female mates, while the likelihood of each male competitively attracting an actual mate depends on the precedence of his signal. Human behaviour consistent with the mixed account was previously observed in a renowned boys choir, where the basses-the oldest boys with the deepest voices-boosted their acoustic prominence by increasing energy in a high-frequency band of the vocal spectrum when girls were in an otherwise male audience. The current study tested female and male sensitivity and preferences for this subtle vocal modulation in online listening tasks. Results indicate that while female and male listeners are similarly sensitive to enhanced high-spectral energy elicited by the presence of girls in the audience, only female listeners exhibit a reliable preference for it. Findings suggest that human chorusing is a flexible form of social communicative behaviour that allows simultaneous group cohesion and sexually motivated competition.

Endogenous sources of interbrain synchrony in duetting pianists.

When people interact with each other, their brains synchronize. However, it remains unclear whether interbrain synchrony (IBS) is functionally relevant for social interaction or stems from exposure of individual brains to identical sensorimotor information. To disentangle these views, the current dual-EEG study investigated amplitude-based IBS in pianists jointly performing duets containing a silent pause followed by a tempo change. First, we manipulated the similarity of the anticipated tempo change and measured IBS during the pause, hence, capturing the alignment of purely endogenous, temporal plans without sound or movement. Notably, right posterior gamma IBS was higher when partners planned similar tempi, it predicted whether partners' tempi matched after the pause, and it was modulated only in real, not in surrogate pairs. Second, we manipulated the familiarity with the partner's actions and measured IBS during joint performance with sound. Although sensorimotor information was similar across conditions, gamma IBS was higher when partners were unfamiliar with each other's part and had to attend more closely to the sound of the performance. These combined findings demonstrate that IBS is not merely an epiphenomenon of shared sensorimotor information but can also hinge on endogenous, cognitive processes crucial for behavioral synchrony and successful social interaction.

Lateral prefrontal cortex is a hub for music production from structural rules to movements.

Complex sequential behaviors, such as speaking or playing music, entail flexible rule-based chaining of single acts. However, it remains unclear how the brain translates abstract structural rules into movements. We combined music production with multimodal neuroimaging to dissociate high-level structural and low-level motor planning. Pianists played novel musical chord sequences on a muted MR-compatible piano by imitating a model hand on screen. Chord sequences were manipulated in terms of musical harmony and context length to assess structural planning, and in terms of fingers used for playing to assess motor planning. A model of probabilistic sequence processing confirmed temporally extended dependencies between chords, as opposed to local dependencies between movements. Violations of structural plans activated the left inferior frontal and middle temporal gyrus, and the fractional anisotropy of the ventral pathway connecting these two regions positively predicted behavioral measures of structural planning. A bilateral frontoparietal network was instead activated by violations of motor plans. Both structural and motor networks converged in lateral prefrontal cortex, with anterior regions contributing to musical structure building, and posterior areas to movement planning. These results establish a promising approach to study sequence production at different levels of action representation.

Measuring the nonselective effects of motor inhibition using isometric force recordings.

Inhibition is a key cognitive control mechanism humans use to enable goal-directed behavior. When rapidly exerted, inhibitory control has broad, nonselective motor effects, typically demonstrated using corticospinal excitability measurements (CSE) elicited by transcranial magnetic stimulation (TMS). For example, during rapid action-stopping, CSE is suppressed at both stopped and task-unrelated muscles. While such TMS-based CSE measurements have provided crucial insights into the fronto-basal ganglia circuitry underlying inhibitory control, they have several downsides. TMS is contraindicated in many populations (e.g., epilepsy or deep-brain stimulation patients), has limited temporal resolution, produces distracting auditory and haptic stimulation, is difficult to combine with other imaging methods, and necessitates expensive, immobile equipment. Here, we attempted to measure the nonselective motor effects of inhibitory control using a method unaffected by these shortcomings. Thirty male and female human participants exerted isometric force on a high-precision handheld force transducer while performing a foot-response stop-signal task. Indeed, when foot movements were successfully stopped, force output at the task-irrelevant hand was suppressed as well. Moreover, this nonselective reduction of isometric force was highly correlated with stop-signal performance and showed frequency dynamics similar to established inhibitory signatures typically found in neural and muscle recordings. Together, these findings demonstrate that isometric force recordings can reliably capture the nonselective effects of motor inhibition, opening the door to many applications that are hard or impossible to realize with TMS.

Saliency Detection as a Reactive Process: Unexpected Sensory Events Evoke Corticomuscular Coupling.

Survival in a fast-changing environment requires animals not only to detect unexpected sensory events, but also to react. In humans, these salient sensory events generate large electrocortical responses, which have been traditionally interpreted within the sensory domain. Here we describe a basic physiological mechanism coupling saliency-related cortical responses with motor output. In four experiments conducted on 70 healthy participants, we show that salient substartle sensory stimuli modulate isometric force exertion by human participants, and that this modulation is tightly coupled with electrocortical activity elicited by the same stimuli. We obtained four main results. First, the force modulation follows a complex triphasic pattern consisting of alternating decreases and increases of force, time-locked to stimulus onset. Second, this modulation occurs regardless of the sensory modality of the eliciting stimulus. Third, the magnitude of the force modulation is predicted by the amplitude of the electrocortical activity elicited by the same stimuli. Fourth, both neural and motor effects are not reflexive but depend on contextual factors. Together, these results indicate that sudden environmental stimuli have an immediate effect on motor processing, through a tight corticomuscular coupling. These observations suggest that saliency detection is not merely perceptive but reactive, preparing the animal for subsequent appropriate actions.SIGNIFICANCE STATEMENT Salient events occurring in the environment, regardless of their modalities, elicit large electrical brain responses, dominated by a widespread "vertex" negative-positive potential. This response is the largest synchronization of neural activity that can be recorded from a healthy human being. Current interpretations assume that this vertex potential reflects sensory processes. Contrary to this general assumption, we show that the vertex potential is strongly coupled with a modulation of muscular activity that follows the same pattern. Both the vertex potential and its motor effects are not reflexive but strongly depend on contextual factors. These results reconceptualize the significance of these evoked electrocortical responses, suggesting that saliency detection is not merely perceptive but reactive, preparing the animal for subsequent appropriate actions.

The effect of salient stimuli on neural oscillations, isometric force, and their coupling.

Survival in a suddenly-changing environment requires animals not only to detect salient stimuli, but also to promptly respond to them by initiating or revising ongoing motor processes. We recently discovered that the large vertex brain potentials elicited by sudden supramodal stimuli are strongly coupled with a multiphasic modulation of isometric force, a phenomenon that we named cortico-muscular resonance (CMR). Here, we extend our investigation of the CMR to the time-frequency domain. We show that (i) both somatosensory and auditory stimuli evoke a number of phase-locked and non-phase-locked modulations of EEG spectral power. Remarkably, (ii) some of these phase-locked and non-phase-locked modulations are also present in the Force spectral power. Finally, (iii) EEG and Force time-frequency responses are correlated in two distinct regions of the power spectrum. An early, low-frequency region (∼4 Hz) reflects the previously-described coupling between the phase-locked EEG vertex potential and force modulations. A late, higher-frequency region (beta-band, ∼20 Hz) reflects a second coupling between the non-phase-locked increase of power observed in both EEG and Force. In both time-frequency regions, coupling was maximal over the sensorimotor cortex contralateral to the hand exerting the force, suggesting an effect of the stimuli on the tonic corticospinal drive. Thus, stimulus-induced CMR occurs across at least two different types of cortical activities, whose functional significance in relation to the motor system should be investigated further. We propose that these different types of corticomuscular coupling are important to alter motor behaviour in response to salient environmental events.

Interpersonal synchronization of inferior frontal cortices tracks social interactive learning of a song.

Much of human learning emerges as a result of interaction with others. Yet, this interpersonal process has been poorly characterized from a neurophysiological perspective. This study investigated (i) whether Interpersonal Brain Synchronization (IBS) can reliably mark social interactive learning, and specifically (ii) during what kind of interactive behavior. We recorded brain activity from learner-instructor dyads using functional Near-Infrared Spectroscopy (fNIRS) during the acquisition of a music song. We made four fundamental observations. First, during the interactive learning task, brain activity recorded from the bilateral Inferior Frontal Cortex (IFC) synchronized across the learner and the instructor. Second, such IBS was observed in particular when the learner was observing the instructor's vocal behavior and when the learning experience entailed a turn-taking and more active mode of interaction. Third, this specific enhancement of IBS predicted learner's behavioral performance. Fourth, Granger causality analyses further disclosed that the signal recorded from the instructor's brain better predicted that recorded from the learner's brain than vice versa. Together, these results indicate that social interactive learning can be neurophysiologically characterized in terms of IBS. Furthermore, they suggest that the learner's involvement in the learning experience, alongside the instructor's modeling, are key factors driving the alignment of neural processes across learner and instructor. Such alignment impacts upon the real-time acquisition of new information and eventually upon the learning (behavioral) performance. Hence, besides providing a biological characterization of social interactive learning, our results hold relevance for clinical and pedagogical practices.

Dynamical entrainment of corticospinal excitability during rhythmic movement observation: a Transcranial Magnetic Stimulation study.

Spontaneous modulations of corticospinal excitability during action observation have been interpreted as evidence for the activation of internal motor representations equivalent to the observed action. Alternatively or complementary to this perspective, growing evidence shows that motor activity during observation of rhythmic movements can be modulated by direct visuomotor couplings and dynamical entrainment. In-phase and anti-phase entrainment spontaneously occur, characterized by cyclic movements proceeding simultaneously in the same (in-phase) or opposite (anti-phase) direction. Here we investigate corticospinal excitability during the observation of vertical oscillations of an index finger using Transcranial Magnetic Stimulation (TMS). Motor-evoked potentials (MEPs) were recorded from participants' flexor and extensor muscles of the right index finger, placed in either a maximal steady flexion or extension position, with stimulations delivered at maximal flexion, maximal extension or mid-trajectory of the observed finger oscillations. Consistent with the occurrence of dynamical motor entrainment, increased and decreased MEP responses - suggesting the facilitation of stable in-phase and anti-phase relations but not an unstable 90° phase relation - were found in participants' flexors. Anti-phase motor facilitation contrasts with the activation of internal motor representation as it involves activity in the motor system opposite from activity required for the execution of the observed movement. These findings demonstrate the relevance of dynamical entrainment theories and methods for understanding spontaneous motor activity in the brain during action observation and the mechanisms underpinning coordinated movements during social interaction.

Causal Role of Motor Simulation in Turn-Taking Behavior.

Overlap between sensory and motor representations has been documented for a range of human actions, from grasping (Rizzolatti et al., 1996b) to playing a musical instrument (Novembre and Keller, 2014). Such overlap suggests that individuals use motor simulation to predict the outcome of observed actions (Wolpert, 1997). Here we investigate motor simulation as a basis of human communication. Using a musical turn-taking task, we show that pianists call on motor representations of their partner's part to predict when to come in for their own turn. Pianists played alternating solos with a videoed partner, and double-pulse transcranial magnetic stimulation was applied around the turn-switch to temporarily disrupt processing in two cortical regions implicated previously in different forms of motor simulation: (1) the dorsal premotor cortex (dPMC), associated with automatic motor resonance during passive observation of hand actions, especially when the actions are familiar (Lahav et al., 2007); and (2) the supplementary motor area (SMA), involved in active motor imagery, especially when the actions are familiar (Baumann et al., 2007). Stimulation of the right dPMC decreased the temporal accuracy of pianists' (right-hand) entries relative to sham when the partner's (left-hand) part had been rehearsed previously. This effect did not occur for dPMC stimulation without rehearsal or for SMA stimulation. These findings support the role of the dPMC in predicting the time course of observed actions via resonance-based motor simulation during turn-taking. Because turn-taking spans multiple modes of human interaction, we suggest that simulation is a foundational mechanism underlying the temporal dynamics of joint action. SIGNIFICANCE STATEMENT: Even during passive observation, seeing or hearing somebody execute an action from within our repertoire activates motor cortices of our brain. But what is the functional relevance of such "motor simulation"? By combining a musical duet task with a real-time repetitive transcranial magnetic stimulation protocol, we provide evidence indicating that the dorsal premotor cortex plays a causal role in accurate turn-taking coordination between a pianist and their observed interaction partner. Given that turn-taking behavior is a fundamental feature of human communication, we suggest that simulation is a foundational mechanism underlying the temporal dynamics of communicative joint action.

Syntax in Action Has Priority over Movement Selection in Piano Playing: An ERP Study.

Complex human behavior is hierarchically organized. Whether or not syntax plays a role in this organization is currently under debate. The present ERP study uses piano performance to isolate syntactic operations in action planning and to demonstrate their priority over nonsyntactic levels of movement selection. Expert pianists were asked to execute chord progressions on a mute keyboard by copying the posture of a performing model hand shown in sequences of photos. We manipulated the final chord of each sequence in terms of Syntax (congruent/incongruent keys) and Manner (conventional/unconventional fingering), as well as the strength of its predictability by varying the length of the Context (five-chord/two-chord progressions). The production of syntactically incongruent compared to congruent chords showed a response delay that was larger in the long compared to the short context. This behavioral effect was accompanied by a centroparietal negativity in the long but not in the short context, suggesting that a syntax-based motor plan was prepared ahead. Conversely, the execution of the unconventional manner was not delayed as a function of Context and elicited an opposite electrophysiological pattern (a posterior positivity). The current data support the hypothesis that motor plans operate at the level of musical syntax and are incrementally translated to lower levels of movement selection.

The geometry of interpersonal synchrony in human dance.

Collective synchronized behavior has powerful social-communicative functions observed across several animal taxa.1,2,3,4,5,6,7 Operationally, synchronized behavior can be explained by individuals responding to shared external cues (e.g., light, sound, or food) as well as by inter-individual adaptation.3,8,9,10,11 We contrasted these accounts in the context of a universal human practice-collective dance-by recording full-body kinematics from dyads of laypersons freely dancing to music in a "silent disco" setting. We orthogonally manipulated musical input (whether participants were dancing to the same, synchronous music) and visual contact (whether participants could see their dancing partner). Using a data-driven method, we decomposed full-body kinematics of 70 participants into 15 principal movement patterns, reminiscent of common dance moves, explaining over 95% of kinematic variance. We find that both music and partners drive synchrony, but through distinct dance moves. This leads to distinct kinds of synchrony that occur in parallel by virtue of a geometric organization: anteroposterior movements such as head bobs synchronize through music, while hand gestures and full-body lateral movements synchronize through visual contact. One specific dance move-vertical bounce-emerged as a supramodal pacesetter of coordination, synchronizing through both music and visual contact, and at the pace of the musical beat. These findings reveal that synchrony in human dance is independently supported by shared musical input and inter-individual adaptation. The independence between these drivers of synchrony hinges on a geometric organization, enabling dancers to synchronize to music and partners simultaneously by allocating distinct synchronies to distinct spatial axes and body parts.

A Framework for Joint Music Making: Behavioral Findings, Neural Processes, and Computational Models.

Across different epochs and societies, humans occasionally gather to jointly make music. This universal form of collective behavior is as fascinating as it is fragmentedly understood. As the interest in joint music making (JMM) rapidly grows, we review the state-of-the-art of this emerging science, blending behavioral, neural, and computational contributions. We present a conceptual framework synthesizing research on JMM within four components. The framework is centered upon interpersonal coordination, a crucial requirement for JMM. The other components imply the influence of individuals' (past) experience, (current) social factors, and (future) goals on real-time coordination. Our aim is to promote the development of JMM research by organizing existing work, inspiring new questions, and fostering accessibility for researchers belonging to other research communities.

Neural encoding of musical expectations in a non-human primate.

The appreciation of music is a universal trait of humankind.1,2,3 Evidence supporting this notion includes the ubiquity of music across cultures4,5,6,7 and the natural predisposition toward music that humans display early in development.8,9,10 Are we musical animals because of species-specific predispositions? This question cannot be answered by relying on cross-cultural or developmental studies alone, as these cannot rule out enculturation.11 Instead, it calls for cross-species experiments testing whether homologous neural mechanisms underlying music perception are present in non-human primates. We present music to two rhesus monkeys, reared without musical exposure, while recording electroencephalography (EEG) and pupillometry. Monkeys exhibit higher engagement and neural encoding of expectations based on the previously seeded musical context when passively listening to real music as opposed to shuffled controls. We then compare human and monkey neural responses to the same stimuli and find a species-dependent contribution of two fundamental musical features-pitch and timing12-in generating expectations: while timing- and pitch-based expectations13 are similarly weighted in humans, monkeys rely on timing rather than pitch. Together, these results shed light on the phylogeny of music perception. They highlight monkeys' capacity for processing temporal structures beyond plain acoustic processing, and they identify a species-dependent contribution of time- and pitch-related features to the neural encoding of musical expectations.

Musical groove modulates motor cortex excitability: a TMS investigation.

Groove is often described as a musical quality that can induce movement in a listener. This study examines the effects of listening to groove music on corticospinal excitability. Musicians and non-musicians listened to high-groove music, low-groove music, and spectrally matched noise, while receiving single-pulse transcranial magnetic stimulation (TMS) over the primary motor cortex either on-beat or off-beat. We examined changes in the amplitude of the motor-evoked potentials (MEPs), recorded from hand and arm muscles, as an index of activity within the motor system. Musicians and non-musicians rated groove similarly. MEP results showed that high-groove music modulated corticospinal excitability, whereas no difference occurred between low-groove music and noise. More specifically, musicians' MEPs were larger with high-groove than low-groove music, and this effect was especially pronounced for on-beat compared to off-beat pulses. These results indicate that high-groove music increasingly engages the motor system, and the temporal modulation of corticospinal excitability with the beat could stem from tight auditory-motor links in musicians. Conversely, non-musicians' MEPs were smaller for high-groove than low-groove music, and there was no effect of on- versus off-beat pulses, potentially stemming from suppression of overt movement. In sum, high-groove music engages the motor system, and previous training modulates how listening to music with a strong groove activates the motor system.

Distinguishing self and other in joint action. Evidence from a musical paradigm.

The capacity to distinguish between one's own and others' behavior is a cognitive prerequisite for successful joint action. We employed a musical joint action task to investigate how the brain achieves this distinction. Pianists performed the right-hand part of piano pieces, previously learned bimanually, while the complementary left-hand part either was not executed or was (believed to be) played by a co-performer. This experimental setting served to induce a co-representation of the left-hand part reflecting either the self or the co-performer. Single-pulse transcranial magnetic stimulation was applied to the right primary motor cortex and motor-evoked potentials (MEPs) were recorded from the resting left forearm. Results show that corticospinal excitability was modulated by whether the representation of the left hand was associated with the self or the other, with the MEP amplitude being low and high, respectively. This result remained unchanged in a separate session where participants could neither see nor hear the other but still infer his presence by means of contextual information. Furthermore, the amplitude of MEPs associated with co-performer presence increased with pianists' self-reported empathy. Thus, the sociality of the context modulates action attribution at the level of the motor control system.