Neural indicators of articulator-specific sensorimotor influences on infant speech perception.

While there is increasing acceptance that even young infants detect correspondences between heard and seen speech, the common view is that oral-motor movements related to speech production cannot influence speech perception until infants begin to babble or speak. We investigated the extent of multimodal speech influences on auditory speech perception in prebabbling infants who have limited speech-like oral-motor repertoires. We used event-related potentials (ERPs) to examine how sensorimotor influences to the infant's own articulatory movements impact auditory speech perception in 3-mo-old infants. In experiment 1, there were ERP discriminative responses to phonetic category changes across two phonetic contrasts (bilabial-dental /ba/-/ɗa/; dental-retroflex /ɗa/-/ɖa/) in a mismatch paradigm, indicating that infants auditorily discriminated both contrasts. In experiment 2, inhibiting infants' own tongue-tip movements had a disruptive influence on the early ERP discriminative response to the /ɗa/-/ɖa/ contrast only. The same articulatory inhibition had contrasting effects on the perception of the /ba/-/ɗa/ contrast, which requires different articulators (the lips vs. the tongue) during production, and the /ɗa/-/ɖa/ contrast, whereby both phones require tongue-tip movement as a place of articulation. This articulatory distinction between the two contrasts plausibly accounts for the distinct influence of tongue-tip suppression on the neural responses to phonetic category change perception in definitively prebabbling, 3-mo-old, infants. The results showing a specificity in the relation between oral-motor inhibition and phonetic speech discrimination suggest a surprisingly early mapping between auditory and motor speech representation already in prebabbling infants.

The neonate brain's sensitivity to repetition-based structure: Specific to speech?

Newborns are able to extract and learn repetition-based regularities from the speech input, that is, they show greater brain activation in the bilateral temporal and left inferior frontal regions to trisyllabic pseudowords of the form AAB (e.g., "babamu") than to random ABC sequences (e.g., "bamuge"). Whether this ability is specific to speech or also applies to other auditory stimuli remains unexplored. To investigate this, we tested whether newborns are sensitive to regularities in musical tones. Neonates listened to AAB and ABC tones sequences, while their brain activity was recorded using functional Near-Infrared Spectroscopy (fNIRS). The paradigm, the frequency of occurrence and the distribution of the tones were identical to those of the syllables used in previous studies with speech. We observed a greater inverted (negative) hemodynamic response to AAB than to ABC sequences in the bilateral temporal and fronto-parietal areas. This inverted response was caused by a decrease in response amplitude, attributed to habituation, over the course of the experiment in the left fronto-temporal region for the ABC condition and in the right fronto-temporal region for both conditions. These findings show that newborns' ability to discriminate AAB from ABC sequences is not specific to speech. However, the neural response to musical tones and spoken language is markedly different. Tones gave rise to habituation, whereas speech was shown to trigger increasing responses over the time course of the study. Relatedly, the repetition regularity gave rise to an inverted hemodynamic response when carried by tones, while it was canonical for speech. Thus, newborns' ability to detect repetition is not speech-specific, but it engages distinct brain mechanisms for speech and music. RESEARCH HIGHLIGHTS: The ability of newborns' to detect repetition-based regularities is not specific to speech, but also extends to other auditory modalities. The brain mechanisms underlying speech and music processing are markedly different.

Critical period regulation across multiple timescales.

Brain plasticity is dynamically regulated across the life span, peaking during windows of early life. Typically assessed in the physiological range of milliseconds (real time), these trajectories are also influenced on the longer timescales of developmental time (nurture) and evolutionary time (nature), which shape neural architectures that support plasticity. Properly sequenced critical periods of circuit refinement build up complex cognitive functions, such as language, from more primary modalities. Here, we consider recent progress in the biological basis of critical periods as a unifying rubric for understanding plasticity across multiple timescales. Notably, the maturation of parvalbumin-positive (PV) inhibitory neurons is pivotal. These fast-spiking cells generate gamma oscillations associated with critical period plasticity, are sensitive to circadian gene manipulation, emerge at different rates across brain regions, acquire perineuronal nets with age, and may be influenced by epigenetic factors over generations. These features provide further novel insight into the impact of early adversity and neurodevelopmental risk factors for mental disorders.

Reduced perceptual narrowing in synesthesia.

Synesthesia is a neurologic trait in which specific inducers, such as sounds, automatically elicit additional idiosyncratic percepts, such as color (thus "colored hearing"). One explanation for this trait-and the one tested here-is that synesthesia results from unusually weak pruning of cortical synaptic hyperconnectivity during early perceptual development. We tested the prediction from this hypothesis that synesthetes would be superior at making discriminations from nonnative categories that are normally weakened by experience-dependent pruning during a critical period early in development-namely, discrimination among nonnative phonemes (Hindi retroflex /d̪a/ and dental /ɖa/), among chimpanzee faces, and among inverted human faces. Like the superiority of 6-mo-old infants over older infants, the synesthetic groups were significantly better than control groups at making all the nonnative discriminations across five samples and three testing sites. The consistent superiority of the synesthetic groups in making discriminations that are normally eliminated during infancy suggests that residual cortical connectivity in synesthesia supports changes in perception that extend beyond the specific synesthetic percepts, consistent with the incomplete pruning hypothesis.

20-month-olds selectively generalize newly learned word meanings based on cues to linguistic community membership.

A growing body of work suggests that speaker-race influences how infants and toddlers interpret the meanings of words. In two experiments, we explored the role of speaker-race on whether newly learned word-object pairs are generalized to new speakers. Seventy-two 20-month-olds were taught two word-object pairs from a familiar race speaker, and two different word-object pairs from an unfamiliar race speaker (four new pairs total). Using an intermodal preferential looking procedure, their interpretation of these new word-object pairs was tested using an unpictured novel speaker. We found that toddlers did not generalize word meanings taught by an unfamiliar race speaker to a new speaker (Experiment 1), unless given evidence that the unfamiliar race speaker was a member of the child's linguistic community through affiliative behaviour and linguistic competence (Experiment 2). In both experiments, generalization was observed for the word-object pairs taught by the familiar race speaker. These experiments indicate that children attend to speakers' non-linguistic properties, and this, in turn, can influence the perceived relevance of speakers' labels.

Bilingualism alters infants' cortical organization for attentional orienting mechanisms.

A bilingual environment is associated with changes in the brain's structure and function. Some suggest that bilingualism also improves higher-cognitive functions in infants as young as 6-months, yet whether this effect is associated with changes in the infant brain remains unknown. In the present study, we measured brain activity using functional near-infrared spectroscopy in monolingual- and bilingual-raised 6- and 10-month-old infants. Infants completed an orienting attention task, in which a cue was presented prior to an object appearing on the same (Valid) or opposite (Invalid) side of a display. Task performance did not differ between the groups but neural activity did. At 6-months, both groups showed greater activity for Valid (> Invalid) trials in frontal regions (left hemisphere for bilinguals, right hemisphere for monolinguals). At 10-months, bilinguals showed greater activity for Invalid (> Valid) trials in bilateral frontal regions, while monolinguals showed greater brain activity for Valid (> Invalid) trials in left frontal regions. Bilinguals' brain activity trended with their parents' reporting of dual-language mixing when speaking to their child. These findings are the first to indicate how early (dual) language experience can alter the cortical organization underlying broader, non-linguistic cognitive functions during the first year of life.

Infants' Mapping of New Faces to New Voices.

The ability to identify individuals by voice is fundamental for communication. However, little is known about the expectations that infants hold when learning unfamiliar voices. Here, the voice-learning skills of 4- and 8-month-olds (N = 53; 29 girls, 14 boys of various ethnicities) were tested using a preferential-looking task that involved audiovisual stimuli of their mothers and other unfamiliar women. Findings reveal that the expectation that novel voices map on to novel faces emerges between 4 and 8 months of age, and that infants can retain learning of face-voice pairings via nonostensive cues by 8 months of age. This study provides new insights about infants' use of disambiguation and fast mapping in early voice learning.

Putting Mutual Exclusivity in Context: Speaker Race Influences Monolingual and Bilingual Infants' Word-Learning Assumptions.

Previous work indicates mutual exclusivity in word learning in monolingual, but not bilingual toddlers. We asked whether this difference indicates distinct conceptual biases, or instead reflects best-guess heuristic use in the absence of context. We altered word-learning contexts by manipulating whether a familiar- or unfamiliar-race speaker introduced a novel word for an object with a known category label painted in a new color. Both monolingual and bilingual infants showed mutual exclusivity for a familiar-race speaker, and relaxed mutual exclusivity and treated the novel word as a category label for an unfamiliar-race speaker. Thus, monolingual and bilingual infants have access to similar word-learning heuristics, and both use nonlinguistic social context to guide their use of the most appropriate heuristic.

Preverbal Infants Discover Statistical Word Patterns at Similar Rates as Adults: Evidence From Neural Entrainment.

The discovery of words in continuous speech is one of the first challenges faced by infants during language acquisition. This process is partially facilitated by statistical learning, the ability to discover and encode relevant patterns in the environment. Here, we used an electroencephalogram (EEG) index of neural entrainment to track 6-month-olds' (N = 25) segmentation of words from continuous speech. Infants' neural entrainment to embedded words increased logarithmically over the learning period, consistent with a perceptual shift from isolated syllables to wordlike units. Moreover, infants' neural entrainment during learning predicted postlearning behavioral measures of word discrimination (n = 18). Finally, the logarithmic increase in entrainment to words was comparable in infants and adults, suggesting that infants and adults follow similar learning trajectories when tracking probability information among speech sounds. Statistical-learning effects in infants and adults may reflect overlapping neural mechanisms, which emerge early in life and are maintained throughout the life span.

Hub distribution of the brain functional networks of newborns prenatally exposed to maternal depression and SSRI antidepressants.

BACKGROUND: Prenatal maternal depression (PMD) and selective serotonin reuptake inhibitor (SSRI) antidepressants are associated with increased developmental risk in infants. Reports suggest that PMD is associated with hyperconnectivity of the insula and the amygdala, while SSRI exposure is associated with hyperconnectivity of the auditory network in the infant brain. However, associations between functional brain organization and PMD and/or SSRI exposure are not well understood. METHODS: We examined the relation between PMD or SSRI exposure and neonatal brain functional organization. Infants of control (n = 17), depressed SSRI-treated (n = 20) and depressed-only (HAM-D ≥ 8) (n = 16) women, underwent resting-state functional magnetic resonance imaging at postnatal Day 6. At 6 months, temperament was assessed using Infant Behavioral Questionnaire (IBQ). We applied GTA and partial least square regression (PLSR) to the resting-state time series to assess group differences in modularity, and connector and provincial hubs. RESULTS: Modularity was similar across all groups. The depressed-only group showed higher connector hub values in the left anterior cingulate, insula, and caudate as well as higher provincial hub values in the amygdala compared to the control group. The SSRI group showed higher provincial hub values in Heschl's gyrus relative to the depressed-only group. PLSR showed that newborns' hub values predicted 10% of the variability in infant temperament at 6 months, suggesting different developmental patterns between groups. CONCLUSIONS: Prenatal exposures to maternal depression and SSRIs have differential impacts on neonatal functional brain organization. Hub values at 6 days predict variance in temperament between infant groups at 6 months of age.

Who can speak that language? Eleven-month-old infants have language-dependent expectations regarding speaker ethnicity.

Research demonstrates that young infants attend to the indexical characteristics of speakers, including age, gender, and ethnicity, and that the relationship between language and ethnicity is intuitive among older children. However, little research has examined whether infants, within the first year, are sensitive to the co-occurrences of ethnicity and language. In this paper, we demonstrate that by 11 months of age, infants hold language-dependent expectations regarding speaker ethnicity. Specifically, 11-month-old English-learning Caucasian infants looked more to Asian versus Caucasian faces when hearing Cantonese versus English (Studies 1 and 3), but did not look more to Asian versus Caucasian faces when paired with Spanish (Study 2), making it unlikely that they held a general expectation that unfamiliar languages pair with unfamiliar faces. Moreover, infants who had regular exposure to one or more significant non-Caucasian individuals showed this pattern more strongly (Study 3). Given that infants tested were raised in a multilingual metropolitan area-which includes a Caucasian population speaking many languages, but seldom Cantonese, as well as a sizeable Asian population speaking both Cantonese and English-these results are most parsimoniously explained by infants having learned specific language-ethnicity associations based on those individuals they encountered in their environment.

The specificity of the neural response to speech at birth.

In this work we ask whether at birth, the human brain responds uniquely to speech, or if similar activation also occurs to a non-speech surrogate 'language'. We compare neural activation in newborn infants to the language heard in utero (English), to an unfamiliar language (Spanish), and to a whistled surrogate language (Silbo Gomero) that, while used by humans to communicate, is not speech. Anterior temporal areas of the neonate cortex are activated in response to both familiar and unfamiliar spoken language, but these classic language areas are not activated to the whistled surrogate form. These results suggest that at the time human infants emerge from the womb, the neural preparation for language is specialized to speech.

Sensorimotor influences on speech perception in infancy.

The influence of speech production on speech perception is well established in adults. However, because adults have a long history of both perceiving and producing speech, the extent to which the perception-production linkage is due to experience is unknown. We addressed this issue by asking whether articulatory configurations can influence infants' speech perception performance. To eliminate influences from specific linguistic experience, we studied preverbal, 6-mo-old infants and tested the discrimination of a nonnative, and hence never-before-experienced, speech sound distinction. In three experimental studies, we used teething toys to control the position and movement of the tongue tip while the infants listened to the speech sounds. Using ultrasound imaging technology, we verified that the teething toys consistently and effectively constrained the movement and positioning of infants' tongues. With a looking-time procedure, we found that temporarily restraining infants' articulators impeded their discrimination of a nonnative consonant contrast but only when the relevant articulator was selectively restrained to prevent the movements associated with producing those sounds. Our results provide striking evidence that even before infants speak their first words and without specific listening experience, sensorimotor information from the articulators influences speech perception. These results transform theories of speech perception by suggesting that even at the initial stages of development, oral-motor movements influence speech sound discrimination. Moreover, an experimentally induced "impairment" in articulator movement can compromise speech perception performance, raising the question of whether long-term oral-motor impairments may impact perceptual development.

Second label learning in bilingual and monolingual infants.

Mutual exclusivity is the assumption that each object has only one category label. Prior research suggests that bilingual infants, unlike monolingual infants, fail to adhere to this assumption to guide word learning. Yet previous work has not addressed whether bilingual infants systematically interpret a novel word for a familiar object (i.e. an object with a known category label) as a second category label. We addressed this question by exploring bilingual and monolingual infants' use of mutual exclusivity in a task in which they heard a novel label for a familiar object with a salient color (e.g. an aqua-colored dog). They were subsequently tested with two trials that probed whether they interpreted the word as a second category label for the object (e.g. another word meaning dog) or as a label for one of the object's salient properties, namely its color (e.g. a word meaning aqua). Bilingual infants failed to adhere to mutual exclusivity and interpreted the novel word systematically as a second object category label for the familiar object. In contrast, consistent with their use of mutual exclusivity, monolingual infants rejected the novel word as a second category label, and instead showed some evidence of interpreting it as a property (color) term for the familiar object. The findings suggest that both bilingual and monolingual infants are systematic in their interpretation of a novel label for a familiar object, but that they show different interpretations of that label. We thus argue that theoretical accounts of early word learning must consider the crucial role of linguistic experience.

The Role of Auditory and Visual Speech in Word Learning at 18 Months and in Adulthood.

Visual information influences speech perception in both infants and adults. It is still unknown whether lexical representations are multisensory. To address this question, we exposed 18-month-old infants (n = 32) and adults (n = 32) to new word-object pairings: Participants either heard the acoustic form of the words or saw the talking face in silence. They were then tested on recognition in the same or the other modality. Both 18-month-old infants and adults learned the lexical mappings when the words were presented auditorily and recognized the mapping at test when the word was presented in either modality, but only adults learned new words in a visual-only presentation. These results suggest developmental changes in the sensory format of lexical representations.

Does early motor development contribute to speech perception?

At the end of the target article, Keven & Akins (K&A) put forward a challenge to the developmental psychology community to consider the development of complex psychological processes - in particular, intermodal infant perception - across different levels of analysis. We take up that challenge and consider the possibility that early emerging stereotypies might help explain the foundations of the link between speech perception and speech production.

The organization and reorganization of audiovisual speech perception in the first year of life.

The period between six and 12 months is a sensitive period for language learning during which infants undergo auditory perceptual attunement, and recent results indicate that this sensitive period may exist across sensory modalities. We tested infants at three stages of perceptual attunement (six, nine, and 11 months) to determine 1) whether they were sensitive to the congruence between heard and seen speech stimuli in an unfamiliar language, and 2) whether familiarization with congruent audiovisual speech could boost subsequent non-native auditory discrimination. Infants at six- and nine-, but not 11-months, detected audiovisual congruence of non-native syllables. Familiarization to incongruent, but not congruent, audiovisual speech changed auditory discrimination at test for six-month-olds but not nine- or 11-month-olds. These results advance the proposal that speech perception is audiovisual from early in ontogeny, and that the sensitive period for audiovisual speech perception may last somewhat longer than that for auditory perception alone.

The neural correlates of processing scale-invariant environmental sounds at birth.

Sensory systems are thought to have evolved to efficiently represent the full range of sensory stimuli encountered in the natural world. The statistics of natural environmental sounds are characterized by scale-invariance: the property of exhibiting similar patterns at different levels of observation. The statistical structure of scale-invariant sounds remains constant at different spectro-temporal scales. Scale-invariance plays a fundamental role in how efficiently animals and human adults perceive acoustic signals. However, the developmental origins and brain correlates of the neural encoding of scale-invariant environmental sounds remain unexplored. Here, we investigate whether the human brain extracts the statistical property of scale-invariance. Synthetic sounds generated by a mathematical model to respect scale-invariance or violate it were presented to newborns. In alternating blocks, the two sound types were presented together in an alternating fashion, whereas in non-alternating blocks, only one type of sound was presented. Newborns' brain responses were measured using near-infrared spectroscopy. We found that scale-invariant and variable-scale sounds were discriminated by the newborn brain, as suggested by differential activation in the left frontal and temporal areas to alternating vs. non-alternating blocks. These results indicate that newborns already detect and encode scale-invariance as a characteristic feature of acoustic stimuli. This suggests that the mathematical principle of efficient coding of information guides the auditory neural code from the beginning of human development, a finding that may help explain how evolution has prepared the brain for perceiving the natural world.

Critical periods in speech perception: new directions.

A continuing debate in language acquisition research is whether there are critical periods (CPs) in development during which the system is most responsive to environmental input. Recent advances in neurobiology provide a mechanistic explanation of CPs, with the balance between excitatory and inhibitory processes establishing the onset and molecular brakes establishing the offset of windows of plasticity. In this article, we review the literature on human speech perception development within the context of this CP model, highlighting research that reveals the interplay of maturational and experiential influences at key junctures in development and presenting paradigmatic examples testing CP models in human subjects. We conclude with a discussion of how a mechanistic understanding of CP processes changes the nature of the debate: The question no longer is, "Are there CPs?" but rather what processes open them, keep them open, close them, and allow them to be reopened.

Prenatal exposure to antidepressants and depressed maternal mood alter trajectory of infant speech perception.

Language acquisition reflects a complex interplay between biology and early experience. Psychotropic medication exposure has been shown to alter neural plasticity and shift sensitive periods in perceptual development. Notably, serotonin reuptake inhibitors (SRIs) are antidepressant agents increasingly prescribed to manage antenatal mood disorders, and depressed maternal mood per se during pregnancy impacts infant behavior, also raising concerns about long-term consequences following such developmental exposure. We studied whether infants' language development is altered by prenatal exposure to SRIs and whether such effects differ from exposure to maternal mood disturbances. Infants from non-SRI-treated mothers with little or no depression (control), depressed but non-SRI-treated (depressed-only), and depressed and treated with an SRI (SRI-exposed) were studied at 36 wk gestation (while still in utero) on a consonant and vowel discrimination task and at 6 and 10 mo of age on a nonnative speech and visual language discrimination task. Whereas the control infants responded as expected (success at 6 mo and failure at 10 mo) the SRI-exposed infants failed to discriminate the language differences at either age and the depressed-only infants succeeded at 10 mo instead of 6 mo. Fetuses at 36 wk gestation in the control condition performed as expected, with a response on vowel but not consonant discrimination, whereas the SRI-exposed fetuses showed accelerated perceptual development by discriminating both vowels and consonants. Thus, prenatal depressed maternal mood and SRI exposure were found to shift developmental milestones bidirectionally on infant speech perception tasks.