Beat processing in newborn infants cannot be explained by statistical learning based on transition probabilities.

Newborn infants have been shown to extract temporal regularities from sound sequences, both in the form of learning regular sequential properties, and extracting periodicity in the input, commonly referred to as a regular pulse or the 'beat'. However, these two types of regularities are often indistinguishable in isochronous sequences, as both statistical learning and beat perception can be elicited by the regular alternation of accented and unaccented sounds. Here, we manipulated the isochrony of sound sequences in order to disentangle statistical learning from beat perception in sleeping newborn infants in an EEG experiment, as previously done in adults and macaque monkeys. We used a binary accented sequence that induces a beat when presented with isochronous timing, but not when presented with randomly jittered timing. We compared mismatch responses to infrequent deviants falling on either accented or unaccented (i.e., odd and even) positions. Results showed a clear difference between metrical positions in the isochronous sequence, but not in the equivalent jittered sequence. This suggests that beat processing is present in newborns. Despite previous evidence for statistical learning in newborns the effects of this ability were not detected in the jittered condition. These results show that statistical learning by itself does not fully explain beat processing in newborn infants.

Early maturation of sound duration processing in the infant's brain.

The ability to process sound duration is crucial already at a very early age for laying the foundation for the main functions of auditory perception, such as object perception and music and language acquisition. With the availability of age-appropriate structural anatomical templates, we can reconstruct EEG source activity with much-improved reliability. The current study capitalized on this possibility by reconstructing the sources of event-related potential (ERP) waveforms sensitive to sound duration in 4- and 9-month-old infants. Infants were presented with short (200 ms) and long (300 ms) sounds equiprobable delivered in random order. Two temporally separate ERP waveforms were found to be modulated by sound duration. Generators of these waveforms were mainly located in the primary and secondary auditory areas and other language-related regions. The results show marked developmental changes between 4 and 9 months, partly reflected by scalp-recorded ERPs, but appearing in the underlying generators in a far more nuanced way. The results also confirm the feasibility of the application of anatomical templates in developmental populations.

Relevance to the higher order structure may govern auditory statistical learning in neonates.

Hearing is one of the earliest senses to develop and is quite mature by birth. Contemporary theories assume that regularities in sound are exploited by the brain to create internal models of the environment. Through statistical learning, internal models extrapolate from patterns to predictions about subsequent experience. In adults, altered brain responses to sound enable us to infer the existence and properties of these models. In this study, brain potentials were used to determine whether newborns exhibit context-dependent modulations of a brain response that can be used to infer the existence and properties of internal models. Results are indicative of significant context-dependence in the responsivity to sound in newborns. When common and rare sounds continue in stable probabilities over a very long period, neonates respond to all sounds equivalently (no differentiation). However, when the same common and rare sounds at the same probabilities alternate over time, the neonate responses show clear differentiations. The context-dependence is consistent with the possibility that the neonate brain produces more precise internal models that discriminate between contexts when there is an emergent structure to be discovered but appears to adopt broader models when discrimination delivers little or no additional information about the environment.

Newborn infants differently process adult directed and infant directed speech.

Infant directed speech (IDS) may serve important functions in language acquisition and in adult-infant communication. The processing of IDS evolves during the first years of life. In order to serve as an effective tool of language acquisition, already very young infants should be able to distinguish IDS from adult directed speech (ADS). We tested whether the ability to discriminate these two speech registers is functional in neonates, by recording EEG from 98 newborn infants in response to Hungarian words naturally spoken in the IDS and the ADS register. Words presented in the ADS register elicited a centro-parietal slow positivity in the 200-600 ms time window whereas words in IDS register elicited a small frontal negativity in the 700-900 ms time window. We conclude that newborn infants differentiate natural speech sounds based on speech register.

Large-scale network organization of EEG functional connectivity in newborn infants.

The organization of functional brain networks changes across human lifespan. The present study analyzed functional brain networks in healthy full-term infants (N = 139) within 1-6 days from birth by measuring neural synchrony in EEG recordings during quiet sleep. Large-scale phase synchronization was measured in six frequency bands with the Phase Lag Index. Macroscopic network organization characteristics were quantified by constructing unweighted minimum spanning tree graphs. The cortical networks in early infancy were found to be significantly more hierarchical and had a more cost-efficient organization compared with MST of random control networks, more so in the theta and alpha than in other frequency bands. Frontal and parietal sites acted as the main hubs of these networks, the topological characteristics of which were associated with gestation age (GA). This suggests that individual differences in network topology are related to cortical maturation during the prenatal period, when functional networks shift from strictly centralized toward segregated configurations. Hum Brain Mapp 38:4019-4033, 2017. © 2017 Wiley Periodicals, Inc.

EEG signatures accompanying auditory figure-ground segregation.

In everyday acoustic scenes, figure-ground segregation typically requires one to group together sound elements over both time and frequency. Electroencephalogram was recorded while listeners detected repeating tonal complexes composed of a random set of pure tones within stimuli consisting of randomly varying tonal elements. The repeating pattern was perceived as a figure over the randomly changing background. It was found that detection performance improved both as the number of pure tones making up each repeated complex (figure coherence) increased, and as the number of repeated complexes (duration) increased - i.e., detection was easier when either the spectral or temporal structure of the figure was enhanced. Figure detection was accompanied by the elicitation of the object related negativity (ORN) and the P400 event-related potentials (ERPs), which have been previously shown to be evoked by the presence of two concurrent sounds. Both ERP components had generators within and outside of auditory cortex. The amplitudes of the ORN and the P400 increased with both figure coherence and figure duration. However, only the P400 amplitude correlated with detection performance. These results suggest that 1) the ORN and P400 reflect processes involved in detecting the emergence of a new auditory object in the presence of other concurrent auditory objects; 2) the ORN corresponds to the likelihood of the presence of two or more concurrent sound objects, whereas the P400 reflects the perceptual recognition of the presence of multiple auditory objects and/or preparation for reporting the detection of a target object.

Relative Pitch Perception and the Detection of Deviant Tone Patterns.

Most people are able to recognise familiar tunes even when played in a different key. It is assumed that this depends on a general capacity for relative pitch perception; the ability to recognise the pattern of inter-note intervals that characterises the tune. However, when healthy adults are required to detect rare deviant melodic patterns in a sequence of randomly transposed standard patterns they perform close to chance. Musically experienced participants perform better than naïve participants, but even they find the task difficult, despite the fact that musical education includes training in interval recognition.To understand the source of this difficulty we designed an experiment to explore the relative influence of the size of within-pattern intervals and between-pattern transpositions on detecting deviant melodic patterns. We found that task difficulty increases when patterns contain large intervals (5-7 semitones) rather than small intervals (1-3 semitones). While task difficulty increases substantially when transpositions are introduced, the effect of transposition size (large vs small) is weaker. Increasing the range of permissible intervals to be used also makes the task more difficult. Furthermore, providing an initial exact repetition followed by subsequent transpositions does not improve performance. Although musical training correlates with task performance, we find no evidence that violations to musical intervals important in Western music (i.e. the perfect fifth or fourth) are more easily detected. In summary, relative pitch perception does not appear to be conducive to simple explanations based exclusively on invariant physical ratios.

Mismatch response (MMR) in neonates: Beyond refractoriness.

In the adult auditory system, deviant detection and updating the representation of the environment is reflected by the event-related potential (ERP) component termed the mismatch negativity (MMN). MMN is elicited when a rare-pitch deviant stimulus is presented amongst frequent standard pitch stimuli. The same stimuli also elicit a similar discriminative ERP component in sleeping newborn infants (termed the mismatch response: MMR). Both the MMN and the MMR can be confounded by responses generated by differential refractoriness of frequency-selective neural populations. Employing a stimulus paradigm designed to minimize this confounding effect, newborns were presented with sequences of pure tones under two conditions: In the oddball block, rare deviant tones (500Hz; 10%) were delivered amongst frequent standards (700Hz; 90%). In the control block, a comparison tone (500Hz) was presented with the same probability as the deviant (10%) along with the four contextual tones (700Hz, 980Hz, 1372Hz, 1920.8Hz; 22.5% each). The significant difference found between the response elicited by the deviant and the comparison tone showed that the response elicited by the deviant in the oddball sequences cannot be fully explained by frequency-specific refractoriness of the neural generators. This shows that neonates process sounds in a context-dependent manner as well as strengthens the correspondence between the adult MMN and the infant MMR.

Processing of Horizontal Sound Localization Cues in Newborn Infants.

OBJECTIVES: By measuring event-related brain potentials (ERPs), the authors tested the sensitivity of the newborn auditory cortex to sound lateralization and to the most common cues of horizontal sound localization. DESIGN: Sixty-eight healthy full-term newborn infants were presented with auditory oddball sequences composed of frequent and rare noise segments in four experimental conditions. The authors tested in them the detection of deviations in the primary cues of sound lateralization (interaural time and level difference) and in actual sound source location (free-field and monaural sound presentation). ERP correlates of deviance detection were measured in two time windows. RESULTS: Deviations in both primary sound localization cues and the ear of stimulation elicited a significant ERP difference in the early (90 to 140 msec) time window. Deviance in actual sound source location (the free-field condition) elicited a significant response in the late (290 to 340 msec) time window. CONCLUSIONS: The early differential response may indicate the detection of a change in the respective auditory features. The authors suggest that the late differential response, which was only elicited by actual sound source location deviation, reflects the detection of location deviance integrating the various cues of sound source location. Although the results suggest that all of the tested binaural cues are processed by the neonatal auditory cortex, utilizing the cues for locating sound sources of these cues may require maturation and learning.

Predictive processing of pitch trends in newborn infants.

The notion of predictive sound processing suggests that the auditory system prepares for upcoming sounds once it has detected regular features within a sequence. Here we investigated whether predictive processes are operating at birth in the human auditory system. Event-related potentials (ERP) were recorded from healthy newborns to occasional ascending pitch steps occurring in the 2nd or the 5th position within trains of tones with otherwise monotonously descending pitch. If the trains were processed in a predictive manner only deviant pitch steps occurring in the later train position would elicit the discriminative mismatch response (MMR). Deviants delivered in the 5th but not in the 2nd position of the tone trains elicited a significant MMR response. These results suggest that newborns represent pitch trends within sound sequences and they process them in a predictive manner. This article is part of a Special Issue entitled SI: Prediction and Attention.

Newborn infants detect cues of concurrent sound segregation.

Separating concurrent sounds is fundamental for a veridical perception of one's auditory surroundings. Sound components that are harmonically related and start at the same time are usually grouped into a common perceptual object, whereas components that are not in harmonic relation or have different onset times are more likely to be perceived in terms of separate objects. Here we tested whether neonates are able to pick up the cues supporting this sound organization principle. We presented newborn infants with a series of complex tones with their harmonics in tune (creating the percept of a unitary sound object) and with manipulated variants, which gave the impression of two concurrently active sound sources. The manipulated variant had either one mistuned partial (single-cue condition) or the onset of this mistuned partial was also delayed (double-cue condition). Tuned and manipulated sounds were presented in random order with equal probabilities. Recording the neonates' electroencephalographic responses allowed us to evaluate their processing of the sounds. Results show that, in both conditions, mistuned sounds elicited a negative displacement of the event-related potential (ERP) relative to tuned sounds from 360 to 400 ms after sound onset. The mistuning-related ERP component resembles the object-related negativity (ORN) component in adults, which is associated with concurrent sound segregation. Delayed onset additionally led to a negative displacement from 160 to 200 ms, which was probably more related to the physical parameters of the sounds than to their perceptual segregation. The elicitation of an ORN-like response in newborn infants suggests that neonates possess the basic capabilities of segregating concurrent sounds by detecting inharmonic relations between the co-occurring sounds.

Detecting the temporal structure of sound sequences in newborn infants.

Most high-level auditory functions require one to detect the onset and offset of sound sequences as well as registering the rate at which sounds are presented within the sound trains. By recording event-related brain potentials to onsets and offsets of tone trains as well as to changes in the presentation rate, we tested whether these fundamental auditory capabilities are functional at birth. Each of these events elicited significant event-related potential components in sleeping healthy neonates. The data thus demonstrate that the newborn brain is sensitive to these acoustic features suggesting that infants are geared towards the temporal aspects of segregating sound sources, speech and music perception already at birth.

Perceiving temporal regularity in music: the role of auditory event-related potentials (ERPs) in probing beat perception.

The aim of this chapter is to give an overview of how the perception of a regular beat in music can be studied in humans adults, human newborns, and nonhuman primates using event-related brain potentials (ERPs). Next to a review of the recent literature on the perception of temporal regularity in music, we will discuss in how far ERPs, and especially the component called mismatch negativity (MMN), can be instrumental in probing beat perception. We conclude with a discussion on the pitfalls and prospects of using ERPs to probe the perception of a regular beat, in which we present possible constraints on stimulus design and discuss future perspectives.

Context effects on processing widely deviant sounds in newborn infants.

Detecting and orienting toward sounds carrying new information is a crucial feature of the human brain that supports adaptation to the environment. Rare, acoustically widely deviant sounds presented amongst frequent tones elicit large event-related brain potentials (ERPs) in neonates. Here we tested whether these discriminative ERP responses reflect only the activation of fresh afferent neuronal populations (i.e., neuronal circuits not affected by the tones) or they also index the processing of contextual mismatch between the rare and the frequent sounds. In two separate experiments, we presented sleeping newborns with 150 different environmental sounds and the same number of white noise bursts. Both sounds served either as deviants in an oddball paradigm with the frequent standard stimulus a tone (Novel/Noise deviant), or as the standard stimulus with the tone as deviant (Novel/Noise standard), or they were delivered alone with the same timing as the deviants in the oddball condition (Novel/Noise alone). Whereas the ERP responses to noise-deviants elicited similar responses as the same sound presented alone, the responses elicited by environmental sounds in the corresponding conditions morphologically differed from each other. Thus whereas the ERP response to the noise sounds can be explained by the different refractory state of stimulus-specific neuronal populations, the ERP response to environmental sounds indicated context-sensitive processing. These results provide evidence for an innate tendency of context-dependent auditory processing as well as a basis for the different developmental trajectories of processing acoustical deviance and contextual novelty.

Rhesus monkeys (Macaca mulatta) detect rhythmic groups in music, but not the beat.

It was recently shown that rhythmic entrainment, long considered a human-specific mechanism, can be demonstrated in a selected group of bird species, and, somewhat surprisingly, not in more closely related species such as nonhuman primates. This observation supports the vocal learning hypothesis that suggests rhythmic entrainment to be a by-product of the vocal learning mechanisms that are shared by several bird and mammal species, including humans, but that are only weakly developed, or missing entirely, in nonhuman primates. To test this hypothesis we measured auditory event-related potentials (ERPs) in two rhesus monkeys (Macaca mulatta), probing a well-documented component in humans, the mismatch negativity (MMN) to study rhythmic expectation. We demonstrate for the first time in rhesus monkeys that, in response to infrequent deviants in pitch that were presented in a continuous sound stream using an oddball paradigm, a comparable ERP component can be detected with negative deflections in early latencies (Experiment 1). Subsequently we tested whether rhesus monkeys can detect gaps (omissions at random positions in the sound stream; Experiment 2) and, using more complex stimuli, also the beat (omissions at the first position of a musical unit, i.e. the 'downbeat'; Experiment 3). In contrast to what has been shown in human adults and newborns (using identical stimuli and experimental paradigm), the results suggest that rhesus monkeys are not able to detect the beat in music. These findings are in support of the hypothesis that beat induction (the cognitive mechanism that supports the perception of a regular pulse from a varying rhythm) is species-specific and absent in nonhuman primates. In addition, the findings support the auditory timing dissociation hypothesis, with rhesus monkeys being sensitive to rhythmic grouping (detecting the start of a rhythmic group), but not to the induced beat (detecting a regularity from a varying rhythm).

Is beat induction innate or learned? Probing emergent meter perception in adults and newborns using event-related brain potentials.

Meter is considered an important structuring mechanism in the perception and experience of rhythm in music. Combining behavioral and electrophysiological measures, in the present study we investigate whether meter is more likely a learned phenomenon, possibly a result of musical expertise, or whether sensitivity to meter is also active in adult nonmusicians and newborn infants. The results provide evidence that meter induction is active in adult nonmusicians and that beat induction is already functional right after birth.

Auditory size-deviant detection in adults and newborn infants.

Auditory size perception refers to the ability to make accurate judgements of the size of a sound source based solely upon the sound emitted from the source. Electro-physiological and behavioural data were collected to test whether sound-source size parameters are detected from task-irrelevant sequences in adults and newborn infants. The mismatch negativity (MMN) obtained from adults indexed automatic detection of changes in size for voices, musical instruments and animal calls, regardless of whether the acoustic change indicated larger or smaller sources. Neonates detected changes in the size of a musical instrument. The data are consistent with the notion that auditory size-deviant detection in humans is an innate automatic process. This conclusion is compatible with the theory that the ability to assess the size of sound sources evolved because it provided selective advantage of being able to detect larger (more competent) suitors and larger (more dangerous) predators.

Newborn infants detect the beat in music.

To shed light on how humans can learn to understand music, we need to discover what the perceptual capabilities with which infants are born. Beat induction, the detection of a regular pulse in an auditory signal, is considered a fundamental human trait that, arguably, played a decisive role in the origin of music. Theorists are divided on the issue whether this ability is innate or learned. We show that newborn infants develop expectation for the onset of rhythmic cycles (the downbeat), even when it is not marked by stress or other distinguishing spectral features. Omitting the downbeat elicits brain activity associated with violating sensory expectations. Thus, our results strongly support the view that beat perception is innate.

Newborn infants process pitch intervals.

OBJECTIVE: We investigated whether the auditory system of newborn babies extracts the constancy of a pitch interval from exemplars varying in absolute pitch. METHODS: Event-related brain potentials (ERP) were recorded from healthy newborn infants in an oddball paradigm consisting of frequent standard and infrequent deviant tone pairs. Tone pairs varied in absolute frequency. Standard and deviant pairs differed in the amount of pitch difference within the pairs, but not in the direction of pitch change. RESULTS: Deviant tone pairs elicited a discriminative ERP response. CONCLUSIONS: This result suggests that the neonate auditory system represents pitch intervals similarly to adults. SIGNIFICANCE: Adult-like processing of pitch intervals allows newborn infants to learn music, speech prosody, and to process various important auditory cues based on spectral acoustic features.