From a general perspective, harmony in music is the balance of the proportions between the different parts of a whole, which causes a feeling of pleasure.
“When we listen to music, each sound we hear helps us to imagine what is coming next. It what we expect is fulfilled, we feel satisfied.
But if not, we may be pleasantly surprised or upset”, comments Carlota Pagès Portabella, a researcher with the Language and Comparative Cognition research group (LCC) at the Center for Brain and Cognition (CBC).
A study by Joan M. Toro, director of the LCC and ICREA research professor at the Department of Information and Communication Technologies (DTIC) at UPF and Carlota Pagès Portabella, published in the journal Psychophysiology, studies human musical perception comparing how the brain reacts when the musical sequences perceived do not finish as might be expected.
The study is part of a H2020 international European project which the CBC is conducting the with Fundació Bial to understand the bases of musical cognition.
Topographic map of how the brain reacts in musicians and non-musicians. The image is credited to Juan M. Toro (UPF).
The results of the study have shown that although the perception of music is universal, training in music alters its perception.
To reach this conclusion, the researchers used encephalographic registers to record what happened in the brains of 28 people, with and without musical training, when they listened to melodies with various unexpected endings.
A specific response to any irregularity
First, the researchers showed that regardless of the subjects’ musical training, in the event of any irregularity in musical sequences the brain produces a specific response known as early right anterior negativity (ERAN).
Furthermore, the authors observed that people with no musical training do not distinguish between a simply unexpected and a musically unacceptable ending.
Nevertheless, when the musically trained participants heard an utterly unacceptable ending with regard to harmony, their brain underwent a stronger response than when they were presented with simply unexpected endings.
These results show that while the perception of music is a relatively universal experience, musical training alters how humans perceive music.
The brains of musicians distinguish between different types of musical irregularities that untrained listeners do not differentiate.
The human brain is both wired with innate music abilities and shaped by music experience, starting in utero and continuing across the lifespan [1].
A growing body of literature from music therapy, music cognition, musicology, neurosciences, and affective and behavioral sciences target fetal and neonatal life, shedding light on the emergence and early development of sound and music perception.
However, the great variability present in the literature in terms, for example, of type of music exposure, means of music administration, or age at exposure, has not yet allowed a clear understanding of how music experience impacts and shapes the human infant brain in the context of early neuroplasticity.
Human neural processing of music involves an extremely complex and widespread bilateral network of cortical and subcortical areas, integrating several auditory, cognitive, sensory motor, and emotional functions [2, 3].
Although part of the mechanism underlying music processing might be explained by simple sound processing, music perception is more than the sum of its basic acoustic features. In addition to auditory signal transduction, it triggers a sequence of cognitive, motor, and emotional processes that involve a number of brain areas, unilaterally (e.g., pitch and melody processing are more lateralized to the right hemisphere), as well as bilaterally, involving a number of “musical subfunctions” (for review see [4]).
The wide effects of music on brain function, encompassing auditory perception, language processing, attention and memory, emotion and mood, and motor skills, have suggested the use of music as a therapeutic tool in neuropsychiatric patients, including young infants at neurodevelopmental risk.
Indeed, several systematic reviews and meta-analyses have examined the therapeutic role of music in preterm infants at neurodevelopmental risk, with inconclusive results, mainly due to the variation in study quality and methodology [5–10].
In most cases, the effects of the intervention were assessed in relation to cardiorespiratory parameters, growth and feeding outcomes, length of stay, effects on behavioral state, or pain. Much less is known on the effect of music intervention on direct measures of brain function and structure or on short- and long-term neurodevelopmental outcomes.
In this viewpoint review, we will firstly summarize current knowledge on the emergence and development of music processing during fetal and early postnatal life.
Then, we will review the effects of music exposure in fetuses, preterm, and term newborns, with a specific emphasis on the effects of music on brain structure and function. Finally, in the light of these findings, we will discuss the possible role of music in early intervention programs, within the framework of early socioemotional development and environmental enrichment.
Effects of Music Exposure in Fetuses, Preterms, and Term Infants
Several studies have explored, in fetuses and newborns, the effects of the experimental manipulation of music stimuli to test the specific influence of music as compared to other or no stimuli, either between groups of otherwise matched subjects or within the same subjects at different times (intervention studies).
The majority of them have focused on infants at neurodevelopmental risk, in particular preterm infants, as shown by the relevant number of systematic reviews and meta-analyses that addressed the question on the effects of music intervention in neonatal intensive care unit (NICU) populations [5–10]. In most cases, the effects of the intervention as to infant parameters were assessed in relation to physiological indexes such as heart rate or respiratory rate, to growth/feeding outcomes and length of stay, to impact on behavioral state, or to pain attenuation.
In spite of the numerous studies available, systematic reviews of the literature failed to provide conclusive results on the benefit of music intervention in infants at neurodevelopmental risk, possibly due to the high study heterogeneity. Indeed, the reviewed studies have shown important differences in methodological aspects such as type and complexity of music exposure (e.g., vocal, instrumental, solo, or ensemble/orchestral), means of music administration (e.g., live or recorded music played in the environment; live or recorded music directed to/provided for each infant), and age or age range of the exposition.
Much less attention has been given to the effects of music intervention on more direct measures of brain function and structure, which is the focus of this part of the present review.
Effects of Music Exposure as Assessed by Neurophysiological Techniques
Few studies investigated through neurophysiological techniques the effects of fetal exposure to music. In one study, fetal exposure to a simple recorded lullaby presented 5 times per week starting from the 29th week of pregnancy until birth was compared to controls.
The exposure group had significantly stronger amplitude event-related potential (ERP) responses at birth and 4 months that also correlated with the amount of prenatal exposure [40]. This indicates that prenatal music exposure has an effect on the neural responsiveness to sounds several months later, supporting a sustained effect of fetal memory through early infancy.
In preterm-born infants, amplitude-integrated EEG (aEEG, a restricted channel, compressed display EEG) has been utilized to investigate the effect of recording music on sleep-wake cycles, reporting positive effects of music exposure on quiet sleep in hospitalized premature infants [41, 42]. More recently, aEEG was used to study the effect of Brahms’ Lullaby on the sleep-wake cycle of low-risk preterm infants between 33 and 37 weeks of gestation, reporting fewer interruptions of quiet sleep and increased postconceptional age sleep patterns as the result of music exposure [43]. The results, however, were called to be read with caution due to the potential conceptual flaws in the interpretation of the findings presented by the authors [44].
Additionally, ERP responses have been used as a biomarker of infant speech-sound differentiation during the neonatal period; at the same time, cortical responses to speech sounds were shown to be a feasible measure of the effect of infant vocal music exposure in the NICU. Specifically, infants were exposed to their mother’s a cappella lullabies recording versus standard female a cappella lullabies recording, contingent to infant suck response for 20 minutes twice per day for 2 weeks. Infants in both groups had an increase in speech sound differentiation response on ERP. However, those that listened to their mother’s voice had greater increase in spoken (standard) speech sound differentiation [45].
Clinical compatibility of care and research is an important factor to consider in data collection with vulnerable populations such as preterm infants; therefore, recommendations are consistent in encouraging the utilization of multichannel methods for a comprehensive view of the maturation process of preterm born infants, especially since the feasibility of acquiring electrophysiology data at bedside has been well established [46–48].
Effects of Music Exposure as Assessed by Neuroimaging Techniques
To the best of our knowledge, no studies have investigated the effects of music exposition through neuroimaging techniques during fetal life.
In preterm infants, cranial ultrasonography was utilized for the evaluation of the effect of music on development. A study using cranial ultrasonography evaluated the effect of a musical intervention during neonatal stay of extremely premature infants until they reached term [49]. Infants exposed to maternal sounds (speech, filtered reading, and singing voice, as well as heart beat), for about a month of cumulative daily 3 hours of stimuli, had a significantly larger auditory cortex bilaterally, but not in frontal horn neither in corpus callosum, as compared to control newborns receiving standard care in the NICU. However, the magnitude of the right and left auditory cortex thickness was significantly correlated with gestational age but not with the duration of sound exposure.
Only one study explored music processing in preterm infants at term-equivalent age using fMRI [50]. The authors showed that very preterm infants at term-equivalent age already distinguish between a known music and the same melody played on a different tempo. In this study, authors used psychophysiological analysis to show that, unlike preterm infants without previous music listening or full-term newborns, preterm infants who listened to music from 33 weeks of gestation until term equivalent age show an increased functional connectivity between the primary auditory cortex and the thalamus and the middle cingulate cortex and the striatum, when listening again to the known music. These brain regions have been linked to tempo, familiarity, pleasantness, and arousing music processing, suggesting that these abilities might be modulated by music exposure during the week preceding term equivalent age.
Music and Musicality in the Frame of Early Social and Emotional Development
Findings summarized in the previous sections of this review support the view that, starting from the very early phases of development, listening to music is far from a simple auditory experience, as it triggers a series of cognitive and emotional components with distinct and interconnected neural substrates [51]. Human brain imaging studies have shown that neural activity associated with music listening extends well beyond the auditory cortex involving a widespread bilateral network of frontal, temporal, parietal, and subcortical areas related to attention, motor functions, memory [52–54], and limbic and paralimbic regions related to emotional processing [55–57]. Music can therefore be a useful tool for infant multisensory stimulation [58–60].
Experiments on adult rodents proved that enriched environment, including auditory enrichment, stimulates cortical plasticity [61, 62]. In humans, imaging studies on adults suffering from traumatic brain injury, stroke, and degenerative diseases have shown that they benefit from the exposure to music with an enhanced memory functioning, attention focusing, motor regulation, and emotional adjustment [63–65]. Särkämö and colleagues [66] further showed that music listening after middle cerebral artery stroke induced a larger increase of grey matter volume in frontolimbic network, including orbitofrontal cortex.
Development of neural networks in the perinatal period is highly dependent on the intrinsic and extrinsic multisensory activity driving maturation of neuronal circuits. In particular, music during prenatal and early postnatal period in rats has been shown to modulate brain development in improving learning capacities [67–69]. As prematurity affects socioemotional development and its neural correlates, musical intervention, as framework for brain plasticity, has shown major impact on the reward system [70]. Music induces activity in limbic (e.g., amygdala and hippocampus) and paralimbic structures (e.g., orbitofrontal cortex, parahippocampal gyrus, and temporal poles), regions implicated in emotion generation and regulation and might therefore influence the maturation of socioemotional development [71]. Previous studies showed that full-term infants in the first days of life already show neural emotional responses to musical stimuli [39]. Recently, preterm infants were shown to benefit from enrichment of their environment in the form of audio recordings of maternal sounds with an increased cortical thickness in primary auditory cortex [49]. But, to what extent music during the early postnatal period in preterm infants can influence socioemotional development and the underlying corticolimbic network formation?
Early social interactions in a specifically structured context, such as music and singing, can be a tool for early social and emotional intervention in a broad sense. Beyond the enrichment of auditory skills, through the organization of primary and secondary auditory brain regions, early experiences in music and singing might be also a way to sensitize newborns to the dynamics of social interactions. Actually, when parents interact with their newborns, they provide a dynamic structure in which microevents produced by parents (e.g., silence and prosodic accents) are contingent to the specific reactions of their newborns. For example, it has been shown that when preterm newborns produced a motor action such as open eyes or mouth corners elevation (interpreted as a smile by the mothers), the mothers modulated their voice in a dynamic way, thereby establishing a dyad contingency [72]. In this early face-to-face interaction, when infants open the eyes or smile, the maternal voice is perceived by adult naïve listeners as more emotional and more smiling than it is in the absence of any infants’ facial display. When mothers sing or speak directed to their preterm infants, their vocal act is not only related to preterm infant behavior but also bears modulated emotional content [73]. It is likely, given the fact that music and singing induced brain activations in a widespread neural network including the reward and habits system, i.e., the basal ganglia, the orbitofrontal regions, and deeper structures including the amygdala and the hippocampus [74], that early interactions have an impact on the development and the organization of these neural networks involved in social interactions and emotion regulation. Moreover, it has also been shown that human voice induces a specific set of brain activations localized in the middle superior temporal sulci and gyri in adults, i.e., the so-called voice sensitive areas [75]. These regions have also been shown being sensitive to the emotion conveyed by the voice [76, 77].
Therefore, early exposure to human voice (often emotional in the context of early interactions between preterm babies and parents) in a structured context such as in singing might be served in neural organization during early stages of development and might have a long-term impact on the relevance and importance of human voice in social interactions. These voice-sensitive regions (i.e., superior temporal sulcus and superior temporal gyrus) are in close interactions with frontal areas and especially important for the acoustical invariance extractions. Therefore, premature infant exposure to voice during live interactions in early period may be a way to establish the precursors of the acoustical invariance extractions for the categorization of specific emotions inferred from human voice [78]. These abilities are fundamental in social interactions and especially important in the social exchanges between parents and fragile infants.
Source:
UPF Barcelona
Media Contacts:
Carlota Pagès Portabella – UPF Barcelona
Image Source:
The image is credited to Juan M. Toro (UPF).
Original Research: Closed access
“Dissonant endings of chord progressions elicit a larger ERAN than ambiguous endings in musicians”. Carlota Pagès‐Portabella and Juan M. Toro.
Psychophysiology doi:10.1111/psyp.13476.
