Language experience influences audiovisual speech integration in unimodal and bimodal bilingual infants.

Infants as young as 2 months can integrate audio and visual aspects of speech articulation. A shift of attention from the eyes towards the mouth of talking faces occurs around 6 months of age in monolingual infants. However, it is unknown whether this pattern of attention during audiovisual speech processing is influenced by speech and language experience in infancy. The present study investigated this question by analysing audiovisual speech processing in three groups of 4- to 8-month-old infants who differed in their language experience: monolinguals, unimodal bilinguals (infants exposed to two or more spoken languages) and bimodal bilinguals (hearing infants with Deaf mothers). Eye-tracking was used to study patterns of face scanning while infants were viewing faces articulating syllables with congruent, incongruent and silent auditory tracks. Monolinguals and unimodal bilinguals increased their attention to the mouth of talking faces between 4 and 8 months, while bimodal bilinguals did not show any age difference in their scanning patterns. Moreover, older (6.6 to 8 months), but not younger, monolinguals (4 to 6.5 months) showed increased visual attention to the mouth of faces articulating audiovisually incongruent rather than congruent faces, indicating surprise or novelty. In contrast, no audiovisual congruency effect was found in unimodal or bimodal bilinguals. Results suggest that speech and language experience influences audiovisual integration in infancy. Specifically, reduced or more variable experience of audiovisual speech from the primary caregiver may lead to less sensitivity to the integration of audio and visual cues of speech articulation.

Differences between human auditory event-related potentials (AERPs) measured at 2 and 4 months after birth.

Infant auditory event-related potentials (AERPs) show a series of marked changes during the first year of life. These AERP changes indicate important advances in early development. The current study examined AERP differences between 2- and 4-month-old infants. An auditory oddball paradigm was delivered to infants with a frequent repetitive tone and three rare auditory events. The three rare events included a shorter than the regular inter-stimulus interval (ISI-deviant), white noise segments, and environmental sounds. The results suggest that the N250 infantile AERP component emerges during this period in response to white noise but not to environmental sounds, possibly indicating a developmental step towards separating acoustic deviance from contextual novelty. The scalp distribution of the AERP response to both the white noise and the environmental sounds shifted towards frontal areas and AERP peak latencies were overall lower in infants at 4 than at 2 months of age. These observations indicate improvements in the speed of sound processing and maturation of the frontal attentional network in infants during this period.

Separating acoustic deviance from novelty during the first year of life: a review of event-related potential evidence.

Orienting to salient events in the environment is a first step in the development of attention in young infants. Electrophysiological studies have indicated that in newborns and young infants, sounds with widely distributed spectral energy, such as noise and various environmental sounds, as well as sounds widely deviating from their context elicit an event-related potential (ERP) similar to the adult P3a response. We discuss how the maturation of event-related potentials parallels the process of the development of passive auditory attention during the first year of life. Behavioral studies have indicated that the neonatal orientation to high-energy stimuli gradually changes to attending to genuine novelty and other significant events by approximately 9 months of age. In accordance with these changes, in newborns, the ERP response to large acoustic deviance is dramatically larger than that to small and moderate deviations. This ERP difference, however, rapidly decreases within first months of life and the differentiation of the ERP response to genuine novelty from that to spectrally rich but repeatedly presented sounds commences during the same period. The relative decrease of the response amplitudes elicited by high-energy stimuli may reflect development of an inhibitory brain network suppressing the processing of uninformative stimuli. Based on data obtained from healthy full-term and pre-term infants as well as from infants at risk for various developmental problems, we suggest that the electrophysiological indices of the processing of acoustic and contextual deviance may be indicative of the functioning of auditory attention, a crucial prerequisite of learning and language development.

Socioeconomic status and functional brain development - associations in early infancy.

Socioeconomic status (SES) impacts on both structural and functional brain development in childhood, but how early its effects can be demonstrated is unknown. In this study we measured resting baseline EEG activity in the gamma frequency range in awake 6-9-month-olds from areas of East London with high socioeconomic deprivation. Between-subject comparisons of infants from low- and high-income families revealed significantly lower frontal gamma power in infants from low-income homes. Similar power differences were found when comparing infants according to maternal occupation, with lower occupational status groups yielding lower power. Infant sleep, maternal education, length of gestation, and birth weight, as well as smoke exposure and bilingualism, did not explain these differences. Our results show that the effects of socioeconomic disparities on brain activity can already be detected in early infancy, potentially pointing to very early risk for language and attention difficulties. This is the first study to reveal region-selective differences in functional brain development associated with early infancy in low-income families.

Brain responses and looking behavior during audiovisual speech integration in infants predict auditory speech comprehension in the second year of life.

The use of visual cues during the processing of audiovisual (AV) speech is known to be less efficient in children and adults with language difficulties and difficulties are known to be more prevalent in children from low-income populations. In the present study, we followed an economically diverse group of thirty-seven infants longitudinally from 6-9 months to 14-16 months of age. We used eye-tracking to examine whether individual differences in visual attention during AV processing of speech in 6-9 month old infants, particularly when processing congruent and incongruent auditory and visual speech cues, might be indicative of their later language development. Twenty-two of these 6-9 month old infants also participated in an event-related potential (ERP) AV task within the same experimental session. Language development was then followed-up at the age of 14-16 months, using two measures of language development, the Preschool Language Scale and the Oxford Communicative Development Inventory. The results show that those infants who were less efficient in auditory speech processing at the age of 6-9 months had lower receptive language scores at 14-16 months. A correlational analysis revealed that the pattern of face scanning and ERP responses to audiovisually incongruent stimuli at 6-9 months were both significantly associated with language development at 14-16 months. These findings add to the understanding of individual differences in neural signatures of AV processing and associated looking behavior in infants.

Brain responses to audiovisual speech mismatch in infants are associated with individual differences in looking behaviour.

Research on audiovisual speech integration has reported high levels of individual variability, especially among young infants. In the present study we tested the hypothesis that this variability results from individual differences in the maturation of audiovisual speech processing during infancy. A developmental shift in selective attention to audiovisual speech has been demonstrated between 6 and 9 months with an increase in the time spent looking to articulating mouths as compared to eyes (Lewkowicz & Hansen-Tift. (2012) Proc. Natl Acad. Sci. USA, 109, 1431-1436; Tomalski et al. (2012) Eur. J. Dev. Psychol., 1-14). In the present study we tested whether these changes in behavioural maturational level are associated with differences in brain responses to audiovisual speech across this age range. We measured high-density event-related potentials (ERPs) in response to videos of audiovisually matching and mismatched syllables /ba/ and /ga/, and subsequently examined visual scanning of the same stimuli with eye-tracking. There were no clear age-specific changes in ERPs, but the amplitude of audiovisual mismatch response (AVMMR) to the combination of visual /ba/ and auditory /ga/ was strongly negatively associated with looking time to the mouth in the same condition. These results have significant implications for our understanding of individual differences in neural signatures of audiovisual speech processing in infants, suggesting that they are not strictly related to chronological age but instead associated with the maturation of looking behaviour, and develop at individual rates in the second half of the first year of life.

Atypical audiovisual speech integration in infants at risk for autism.

The language difficulties often seen in individuals with autism might stem from an inability to integrate audiovisual information, a skill important for language development. We investigated whether 9-month-old siblings of older children with autism, who are at an increased risk of developing autism, are able to integrate audiovisual speech cues. We used an eye-tracker to record where infants looked when shown a screen displaying two faces of the same model, where one face is articulating/ba/and the other/ga/, with one face congruent with the syllable sound being presented simultaneously, the other face incongruent. This method was successful in showing that infants at low risk can integrate audiovisual speech: they looked for the same amount of time at the mouths in both the fusible visual/ga/- audio/ba/and the congruent visual/ba/- audio/ba/displays, indicating that the auditory and visual streams fuse into a McGurk-type of syllabic percept in the incongruent condition. It also showed that low-risk infants could perceive a mismatch between auditory and visual cues: they looked longer at the mouth in the mismatched, non-fusible visual/ba/- audio/ga/display compared with the congruent visual/ga/- audio/ga/display, demonstrating that they perceive an uncommon, and therefore interesting, speech-like percept when looking at the incongruent mouth (repeated ANOVA: displays x fusion/mismatch conditions interaction: F(1,16) = 17.153, p = 0.001). The looking behaviour of high-risk infants did not differ according to the type of display, suggesting difficulties in matching auditory and visual information (repeated ANOVA, displays x conditions interaction: F(1,25) = 0.09, p = 0.767), in contrast to low-risk infants (repeated ANOVA: displays x conditions x low/high-risk groups interaction: F(1,41) = 4.466, p = 0.041). In some cases this reduced ability might lead to the poor communication skills characteristic of autism.

Differential habituation to repeated sounds in infants at high risk for autism.

It has been suggested that poor habituation to stimuli might explain atypical sensory behaviours in autism. We investigated habituation to repeated sounds using an oddball paradigm in 9-month-old infants with an older sibling with autism and hence at high risk for developing autism. Auditory-evoked responses to repeated sounds in control infants (at low risk of developing autism) decreased over time, demonstrating habituation, and their responses to deviant sounds were larger than responses to standard sounds, indicating discrimination. In contrast, neural responses in infants at high risk showed less habituation and a reduced sensitivity to changes in frequency. Reduced sensory habituation may be present at a younger age than the emergence of autistic behaviour in some individuals, and we propose that this could play a role in the over responsiveness to some stimuli and undersensitivity to others observed in autism.

Perinatal cerebral insults alter auditory event-related potentials.

BACKGROUND: auditory event-related potentials (AERPs) can be used as indices of neural information processing. Altered AERPs have been reported in children and young adults with frontal lobe infarction. AIM: to test the hypothesis that perinatal brain injury affects cortical auditory processing. METHODS: we assessed AERPs at term, 6 and 12months of age in preterm infants [n=9, median gestational age (GA) 27.9, range 23.9-30.0wk], term infants with perinatal intracerebral hemorrhage (ICH) [n=5, GA 40.3, range 37.4-42.3wk], and term infants with perinatal asphyxia [n=4, GA 39.4, range 37.9-40.3wk]. Healthy preterm (n=16) and term infants (n=22) served as controls. A harmonic tone of 500-Hz frequency was used as standard and of 750-Hz as deviant stimulus. Mean AERP amplitudes were calculated over 100ms periods from 50 to 350ms. The developmental outcome was followed until 2years of age. RESULTS: the term ICH (p=0.012) and asphyxia (p=0.0016) group had smaller or more negative responses to the deviant, resulting in smaller or more negative MMR amplitudes than those of the controls. The preterm ICH group did not differ significantly from their preterm born controls. MMR varied in all patient groups and was not associated with adverse outcome. CONCLUSION: AERP alterations suggest that perinatal cerebral insults affect cortical auditory processing.

Atypical perceptual narrowing in prematurely born infants is associated with compromised language acquisition at 2 years of age.

BACKGROUND: Early auditory experiences are a prerequisite for speech and language acquisition. In healthy children, phoneme discrimination abilities improve for native and degrade for unfamiliar, socially irrelevant phoneme contrasts between 6 and 12 months of age as the brain tunes itself to, and specializes in the native spoken language. This process is known as perceptual narrowing, and has been found to predict normal native language acquisition. Prematurely born infants are known to be at an elevated risk for later language problems, but it remains unclear whether these problems relate to early perceptual narrowing. To address this question, we investigated early neurophysiological phoneme discrimination abilities and later language skills in prematurely born infants and in healthy, full-term infants. RESULTS: Our follow-up study shows for the first time that perceptual narrowing for non-native phoneme contrasts found in the healthy controls at 12 months was not observed in very prematurely born infants. An electric mismatch response of the brain indicated that whereas full-term infants gradually lost their ability to discriminate non-native phonemes from 6 to 12 months of age, prematurely born infants kept on this ability. Language performance tested at the age of 2 years showed a significant delay in the prematurely born group. Moreover, those infants who did not become specialized in native phonemes at the age of one year, performed worse in the communicative language test (MacArthur Communicative Development Inventories) at the age of two years. Thus, decline in sensitivity to non-native phonemes served as a predictor for further language development. CONCLUSION: Our data suggest that detrimental effects of prematurity on language skills are based on the low degree of specialization to native language early in development. Moreover, delayed or atypical perceptual narrowing was associated with slower language acquisition. The results hence suggest that language problems related to prematurity may partially originate already from this early tuning stage of language acquisition.

Electrophysiological evidence of illusory audiovisual speech percept in human infants.

How effortlessly and quickly infants acquire their native language remains one of the most intriguing questions of human development. Our study extends this question into the audiovisual domain, taking into consideration visual speech cues, which were recently shown to have more importance for young infants than previously anticipated [Weikum WM, Vouloumanos A, Navarra J, Soto-Faraco S, Sebastián-Gallés N, Werker JF (2007) Science 316:1159]. A particularly interesting phenomenon of audiovisual speech perception is the McGurk effect [McGurk H, MacDonald J (1976) Nature 264:746-748], an illusory speech percept resulting from integration of incongruent auditory and visual speech cues. For some phonemes, the human brain does not detect the mismatch between conflicting auditory and visual cues but automatically assimilates them into the closest legal phoneme, sometimes different from both auditory and visual ones. Measuring event-related brain potentials in 5-month-old infants, we demonstrate differential brain responses when conflicting auditory and visual speech cues can be integrated and when they cannot be fused into a single percept. This finding reveals a surprisingly early ability to perceive speech cross-modally and highlights the role of visual speech experience during early postnatal development in learning of the phonemes and phonotactics of the native language.

Processing acoustic change and novelty in newborn infants.

Research on event-related potential (ERP) correlates of auditory deviance-detection in newborns provided inconsistent results; temporal and topographic ERP characteristics differed widely across studies and individual infants. Robust and reliable ERP responses were, however, obtained to sounds (termed 'novel' sounds), which cover a wide range of frequencies and widely differ from the context provided by a repeating sound [Kushnerenko et al., (2002) NeuroReport, 13, 1843-1848]. The question we investigated here is whether this effect can be attributed to novelty per se or to acoustic characteristics of the 'novel' sounds, such as their wide frequency spectrum and high signal energy compared with the repeated tones. We also asked how sensitivity to these stimulus aspects changes with development. Twelve newborns and 11 adults were tested in four different oddball conditions, each including a 'standard' sound presented with the probability of 0.8 and two types of infrequent 'deviant' sounds (0.1 probability, each). Deviants were (i) 'novel' sounds (diverse environmental noises); (ii) white-noise segments, or harmonic tones of (iii) a higher pitch, or (iv) higher intensity. In newborns, white-noise deviants elicited the largest response in all latency ranges, whereas in adults, this phenomenon was not found. Thus, newborns appear to be especially sensitive to sounds having a wide frequency spectrum. On the other hand, the pattern of results found for the late discriminative ERP response indicates that newborns may also be able to detect novelty in acoustic stimulation, although with a longer latency than adults, as shown by the ERP response. Results are discussed in terms of developmental refinement of the initially broadly tuned neonate auditory system.

Auditory event-related potentials and cognitive function of preterm children at five years of age.

OBJECTIVE: In our previous study, auditory event-related potentials (AERPs) in preterm 1-year-old children had a positive deflection at 150-350 ms that correlated positively with their 2-year neurodevelopmental outcome. In a study of the same subjects at age 5, our aim was to assess AERPs and their relationship to neuropsychological test results. METHODS: Preterm small (SGA, n=13), appropriate for gestational age (AGA, n=15), and control (n=13) children were assessed with an Easy paradigm presenting a large frequency change accompanied with occasional novel sounds, and a Challenging paradigm presenting small frequency and duration changes with a rapid rate. The preterm children underwent neurocognitive tests. RESULTS: Easy paradigm. The P1 response to frequency deviant was smaller and MMN larger in the preterm than in the control children. Challenging paradigm. The P1 response to standard, frequency, and duration deviants was smaller in the preterm than in the control children. The N2 response to frequency deviant was larger in the preterm than in the control children. AGA and SGA children had similar AERPs. The P1, N2, and MMN amplitudes correlated with verbal IQ and NEPSY language subtests. CONCLUSIONS: Small P1 response(s) appears to be typical for preterm children. SIGNIFICANCE: Small P1 response in preterm children may suggest altered primary auditory processing.

Newborns discriminate novel from harmonic sounds: a study using magnetoencephalography.

OBJECTIVE: We investigated whether newborns respond differently to novel and deviant sounds during quiet sleep. METHODS: Twelve healthy neonates were presented with a three-stimulus oddball paradigm, consisting of frequent standard (76%), infrequent deviant (12%), and infrequent novel stimuli (12%). The standards and deviants were counterbalanced between the newborns and consisted of 500 and 750 Hz tones with two upper harmonics. The novel stimuli contained animal, human, and mechanical sounds. All stimuli had a duration of 300 ms and the stimulus onset asynchrony was 1s. Evoked magnetic responses during quiet sleep were recorded and averaged offline. RESULTS: Two deflections peaking at 345 and 615 ms after stimulus onset were observed in the evoked responses of most of the newborns. The first deflection was larger to novel and deviant stimuli than to the standard and, furthermore, larger to novel than to deviant stimuli. The second deflection was larger to novel and deviant stimuli than to standards, but did not differ between the novels and deviants. CONCLUSIONS: The two deflections found in the present study reflect different mechanisms of auditory change detection and discriminative processes. SIGNIFICANCE: The early brain indicators of novelty detection may be crucial in assessing the normal and abnormal cortical function in newborns. Further, studying evoked magnetic fields to complex auditory stimulation in healthy newborns is needed for studying the newborns at-risk for cognitive or language problems.

Atypical auditory event-related potentials in preterm infants during the first year of life: a possible sign of cognitive dysfunction?

We assessed auditory event-related potentials in small-for-gestational-age (SGA; 850 +/- 258 g, 28.9 +/- 3.3 gestational wk; n = 15) and appropriate for gestational age (AGA; 1014 +/- 231 g, 26.9 +/- 1.9 gestational wk; n = 20) preterm infants and healthy term infants (n = 22). An oddball paradigm was used with a harmonic tone of 500-Hz frequency as the standard and of 750-Hz frequency as the deviant stimulus. The preterm infants were studied at 40 gestational wk and at 6 and 12 mo of corrected age, and the control subjects were studied at 2-4 d and at 3, 6, 9, 12, and 15 mo of age. The peaks of interest were the main positive peak (P350), the negative peaks at 250 ms (N250) and 650 ms (Nc), and the mismatch negativity at 200 ms (MMN). At term, the P350 in the preterm infants was similar to that of the newborn control subjects. In response to the deviant, the Nc was smaller in the SGA than in the AGA (P < 0.02) and control (P < 0.005) infants. The N250 amplitude was also lower in the SGA infants. At 12 mo, the MMN was observed in the control but not in the preterm infants, whose broad difference positivity correlated with the Bayley developmental index. The decreased Nc and N250 peaks in the SGA infants may suggest an increased risk for cognitive dysfunction. The broad difference positivity at 1 y of age may indicate atypical cortical auditory processing. Whether cognitive dysfunction can be predicted by these findings needs to be assessed in a study with extended follow-up.

Auditory magnetic responses of healthy newborns.

We recorded magnetic brain activity from healthy human newborns when they heard frequency changes in an otherwise repetitive sound stream. We were able to record the magnetic counterpart of the mismatch negativity (MMN) previously described only with electric recordings in infants. The results show that these recordings are possible, although still challenging due to the small head size and head movements. The modelling of the neural sources underlying the recorded responses suggests cortical sources in the temporal lobes.

Newborn infants can organize the auditory world.

The perceptual world of neonates is usually regarded as not yet being fully organized in terms of objects in the same way as it is for adults. Using a recently developed method based on electric brain responses, we found that, similarly to adults, newborn infants segregate concurrent streams of sound, allowing them to organize the auditory input according to the existing sound source. The segregation of concurrent sound streams is a crucial step in the path leading to the identification of objects in the environment. Its presence in newborn infants shows that the basic abilities required for the development of conceptual objects are available already at the time of birth.

Maturation of the auditory change detection response in infants: a longitudinal ERP study.

Mismatch negativity (MMN) is a negative component of auditory event-related potential (ERP), reflecting the brain's automatic change detection process. In the present study we investigated the development of the pitch change detection, as indexed by the MMN, in the same infants from birth until 12 months of age. The MMN was identified in approximately 75% of infants at each age, being relatively stable in latency and amplitude at the group level across the ages studied. However, within the same subjects the MMN substantially varied from age to age. The inspection of individual data revealed a possible source of this variability: in a portion of 3- to 9-month-old infants, a large-amplitude positive component commenced at the latency of the MMN and thus might have masked it. The results of the additional experiment, employing distracting novel sounds in 2-year-old infants and newborns, suggested that the observed positive component could represent an infant analogue of the adult P3a response, indexing an involuntary orienting of attention. Therefore, the variability from age to age might be, at least partially, caused by the differences in degree of infants' orienting, resulting in the reduction of the scalp recorded mismatch negativity in recordings when the orienting P3a positivity was elicited.

Auditory ERPs reveal brain dysfunction in infants with plagiocephaly.

It is suspected that the developmental delay in school-aged children diagnosed as infants suffering from plagiocephaly is caused by the modification of the skull form. To detect possible cognitive impairment in these children, we examined auditory ERPs to tones in infant patients. The infants with plagiocephaly exhibited smaller amplitudes of the P150 and the N250 responses to tones than healthy controls. Differences between the patients and control subjects indicate that already at this early age the presence of the plagiocephalic skull signals compromise of brain functioning. The present data suggest that most of the plagiocephalic infants have an elevated risk of auditory processing disorders. In the current study we demonstrated, for the first time, that the central sound processing, as reflected by ERPs, is affected in children with plagiocephaly.

Maturation of the auditory event-related potentials during the first year of life.

This study examined the maturation of cortical auditory event-related potentials (ERPs) from birth until 12 months of age. In the 15 infants studied, all ERP peaks observable at 12 months of age, the P150, N250, P350, and N450 were identifiable already at birth, As in previous studies, the amplitudes of the ERP peaks increased and latencies shortened with increasing age. In addition, the time courses of the amplitude growth of these peaks differed from each other. It was concluded, that the generators of all the infantile ERP peaks are functional already at birth, and that the maturational changes in the waveform morphology can mostly be accounted for by the changing relative strengths of the different generators.