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.

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.

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.

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.

Early social communication through music: State of the art and future perspectives.

A growing body of research shows that the universal capacity for music perception and production emerges early in development. Possibly building on this predisposition, caregivers around the world often communicate with infants using songs or speech entailing song-like characteristics. This suggests that music might be one of the earliest developing and most accessible forms of interpersonal communication, providing a platform for studying early communicative behavior. However, little research has examined music in truly communicative contexts. The current work aims to facilitate the development of experimental approaches that rely on dynamic and naturalistic social interactions. We first review two longstanding lines of research that examine musical interactions by focusing either on the caregiver or the infant. These include defining the acoustic and non-acoustic features that characterize infant-directed (ID) music, as well as behavioral and neurophysiological research examining infants' processing of musical timing and pitch. Next, we review recent studies looking at early musical interactions holistically. This research focuses on how caregivers and infants interact using music to achieve co-regulation, mutual engagement, and increase affiliation and prosocial behavior. We conclude by discussing methodological, technological, and analytical advances that might empower a comprehensive study of musical communication in early childhood.

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.

Interpersonal synchronization of spontaneously generated body movements.

Interpersonal movement synchrony (IMS) is central to social behavior in several species. In humans, IMS is typically studied using structured tasks requiring participants to produce specific body movements. Instead, spontaneously generated (i.e., not instructed) movements have received less attention. To test whether spontaneous movements synchronize interpersonally, we recorded full-body kinematics from dyads of participants who were only asked to sit face-to-face and to look at each other. We manipulated interpersonal (i) visual contact and (ii) spatial proximity. We found that spontaneous movements synchronized across participants only when they could see each other and regardless of interpersonal spatial proximity. This synchronization emerged very rapidly and did not selectively entail homologous body parts (as in mimicry); rather, the synchrony generalized to nearly all possible combinations of body parts. Hence, spontaneous behavior alone can lead to IMS. More generally, our results highlight that IMS can be studied under natural and unconstrained conditions.

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.

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.

The Interpersonal Neuroscience of Social Learning.

The study of the brain mechanisms underpinning social behavior is currently undergoing a paradigm shift, moving its focus from single individuals to the real-time interaction among groups of individuals. Although this development opens unprecedented opportunities to study how interpersonal brain activity shapes behaviors through learning, there have been few direct connections to the rich field of learning science. Our article examines how the rapidly developing field of interpersonal neuroscience is (and could be) contributing to our understanding of social learning. To this end, we first review recent research extracting indices of brain-to-brain coupling (BtBC) in the context of social behaviors and, in particular, social learning. We then discuss how studying communicative behaviors during learning can aid the interpretation of BtBC and how studying BtBC can inform our understanding of such behaviors. We then discuss how BtBC and communicative behaviors collectively can predict learning outcomes, and we suggest several causative and mechanistic models. Finally, we highlight key methodological and interpretational challenges as well as exciting opportunities for integrating research in interpersonal neuroscience with social learning, and we propose a multiperson framework for understanding how interpersonal transmission of information between individual brains shapes social learning.

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.

Towards a unified neural mechanism for reactive adaptive behaviour.

Surviving in natural environments requires animals to sense sudden events and swiftly adapt behaviour accordingly. The study of such Reactive Adaptive Behaviour (RAB) has been central to a number of research streams, all orbiting around movement science but progressing in parallel, with little cross-field fertilization. We first provide a concise review of these research streams, independently describing four types of RAB: (1) cortico-muscular resonance, (2) stimulus locked response, (3) online motor correction and (4) action stopping. We then highlight remarkable similarities across these four RABs, suggesting that they might be subserved by the same neural mechanism, and propose directions for future research on this topic.

Simultaneous self-other integration and segregation support real-time interpersonal coordination in a musical joint action task.

The ability to distinguish between an individual's own actions and those of another person is a requirement for successful joint action, particularly in domains such as group music making where precise interpersonal coordination ensures perceptual overlap in the effects of co-performers' actions. We tested the hypothesis that such coordination benefits from simultaneous integration and segregation of information about 'self' and 'other' in an experiment using a musical joint action paradigm. Sixteen pairs of individuals with little or no musical training performed a dyadic synchronization task on a pair of electronic music boxes. The relationship between pitches produced by paired participants (same vs. different) and the relationship between movement frequencies required to trigger synchronous tones (congruent vs. incongruent) were varied in a repeated measures design. The results indicate that interpersonal coordination was most accurate when sounds were different in pitch but movement frequency was congruent. Under other conditions, participants often drifted apart, resulting in poor coordination, especially with same sounds and incongruent movements across co-performers. These findings suggest that interpersonal coordination was facilitated when simultaneous self-other integration and segregation occurred across sensory modalities in an asymmetrical manner where pitch relations favoured segregation via auditory streaming while movement congruence favoured integration via visuo-motor coupling. Such self-other representational balance may enable co-performers to maintain autonomous control while attending, anticipating, and adapting to each other's timing when joint action requires precise temporal coordination.

Not all errors are alike: modulation of error-related neural responses in musical joint action.

During joint action, the sense of agency enables interaction partners to implement corrective and adaptive behaviour in response to performance errors. When agency becomes ambiguous (e.g. when action similarity encourages perceptual self-other overlap), confusion as to who produced what may disrupt this process. The current experiment investigated how ambiguity of agency affects behavioural and neural responses to errors in a joint action domain where self-other overlap is common: musical duos. Pairs of pianists performed piano pieces in synchrony, playing either the same pitches (ambiguous agency) or different pitches (unambiguous agency) while electroencephalography (EEG) was recorded for each individual. Behavioural and event-related potential results showed no effects of the agency manipulation but revealed differences in how distinct error types are processed. Self-produced 'wrong note' errors (substitutions) were left uncorrected, showed post-error slowing and elicited an error-related negativity (ERN) peaking before erroneous keystrokes (pre-ERN). In contrast, self-produced 'extra note' errors (additions) exhibited pre-error slowing, error and post-error speeding, were rapidly corrected and elicited the ERN. Other-produced errors evoked a feedback-related negativity but no behavioural effects. Overall findings shed light upon how the nervous system supports fluent interpersonal coordination in real-time joint action by employing distinct mechanisms to manage different types of errors.

Dual brain stimulation enhances interpersonal learning through spontaneous movement synchrony.

Social interactive learning denotes the ability to acquire new information from a conspecific-a prerequisite for cultural evolution and survival. As inspired by recent neurophysiological research, here we tested whether social interactive learning can be augmented by exogenously synchronizing oscillatory brain activity across an instructor and a learner engaged in a naturalistic song-learning task. We used a dual brain stimulation protocol entailing the trans-cranial delivery of synchronized electric currents in two individuals simultaneously. When we stimulated inferior frontal brain regions, with 6 Hz alternating currents being in-phase between the instructor and the learner, the dyad exhibited spontaneous and synchronized body movement. Remarkably, this stimulation also led to enhanced learning performance. These effects were both phase- and frequency-specific: 6 Hz anti-phase stimulation or 10 Hz in-phase stimulation, did not yield comparable results. Furthermore, a mediation analysis disclosed that interpersonal movement synchrony acted as a partial mediator of the effect of dual brain stimulation on learning performance, i.e. possibly facilitating the effect of dual brain stimulation on learning. Our results provide a causal demonstration that inter-brain synchronization is a sufficient condition to improve real-time information transfer between pairs of individuals.

Hyperscanning Alone Cannot Prove Causality. Multibrain Stimulation Can.

Brains that work together, couple together through interbrain synchrony. Does interbrain synchrony causally facilitate social interaction? This question cannot be answered by simply recording from multiple brains (hyperscanning). It instead requires causal protocols entailing their simultaneous stimulation (multibrain stimulation). We highlight promising findings and future horizons of this nascent field.

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.

Empathic perspective taking promotes interpersonal coordination through music.

Coordinated behavior promotes collaboration among humans. To shed light upon this relationship, we investigated whether and how interpersonal coordination is promoted by empathic perspective taking (EPT). In a joint music-making task, pairs of participants rotated electronic music-boxes, producing two streams of musical sounds that were meant to be played synchronously. Participants - who were not musically trained - were assigned to high and low EPT groups based on pre-experimental assessments using a standardized personality questionnaire. Results indicated that high EPT pairs were generally more accurate in synchronizing their actions. When instructed to lead the interaction, high and low EPT leaders were equally cooperative with followers, making their performance tempo more regular, presumably in order to increase their predictability and help followers to synchronize. Crucially, however, high EPT followers were better able to use this information to predict leaders' behavior and thus improve interpersonal synchronization. Thus, empathic perspective taking promotes interpersonal coordination by enhancing accuracy in predicting others' behavior while leaving the aptitude for cooperation unaltered. We argue that such predictive capacity relies on a sensorimotor mechanism responsible for simulating others' actions in an anticipatory manner, leading to behavioral advantages that may impact social cognition on a broad scale.