Heart-to-heart: infant heart rate at 3 months is linked to infant-directed speech, mother-infant interaction, and later language outcomes.

Introduction: Previous studies underscore the importance of speech input, particularly infant-directed speech (IDS) during one-on-one (1:1) parent-infant interaction, for child language development. We hypothesize that infants' attention to speech input, specifically IDS, supports language acquisition. In infants, attention and orienting responses are associated with heart rate deceleration. We examined whether individual differences in infants' heart rate measured during 1:1 mother-infant interaction is related to speech input and later language development scores in a longitudinal study. Methods: Using a sample of 31 3-month-olds, we assessed infant heart rate during mother-infant face-to-face interaction in a laboratory setting. Multiple measures of speech input were gathered at 3 months of age during naturally occurring interactions at home using the Language ENvironment Analysis (LENA) system. Language outcome measures were assessed in the same children at 30 months of age using the MacArthur-Bates Communicative Development Inventory (CDI). Results: Two novel findings emerged. First, we found that higher maternal IDS in a 1:1 context at home, as well as more mother-infant conversational turns at home, are associated with a lower heart rate measured during mother-infant social interaction in the laboratory. Second, we found significant associations between infant heart rate during mother-infant interaction in the laboratory at 3 months and prospective language development (CDI scores) at 30 months of age. Discussion: Considering the current results in conjunction with other converging theoretical and neuroscientific data, we argue that high IDS input in the context of 1:1 social interaction increases infants' attention to speech and that infants' attention to speech in early development fosters their prospective language growth.

Infants' brain responses to social interaction predict future language growth.

In face-to-face interactions with infants, human adults exhibit a species-specific communicative signal. Adults present a distinctive "social ensemble": they use infant-directed speech (parentese), respond contingently to infants' actions and vocalizations, and react positively through mutual eye-gaze and smiling. Studies suggest that this social ensemble is essential for initial language learning. Our hypothesis is that the social ensemble attracts attentional systems to speech and that sensorimotor systems prepare infants to respond vocally, both of which advance language learning. Using infant magnetoencephalography (MEG), we measure 5-month-old infants' neural responses during live verbal face-to-face (F2F) interaction with an adult (social condition) and during a control (nonsocial condition) in which the adult turns away from the infant to speak to another person. Using a longitudinal design, we tested whether infants' brain responses to these conditions at 5 months of age predicted their language growth at five future time points. Brain areas involved in attention (right hemisphere inferior frontal, right hemisphere superior temporal, and right hemisphere inferior parietal) show significantly higher theta activity in the social versus nonsocial condition. Critical to theory, we found that infants' neural activity in response to F2F interaction in attentional and sensorimotor regions significantly predicted future language development into the third year of life, more than 2 years after the initial measurements. We develop a view of early language acquisition that underscores the centrality of the social ensemble, and we offer new insight into the neurobiological components that link infants' language learning to their early brain functioning during social interaction.

Mother-infant social and language interactions at 3 months are associated with infants' productive language development in the third year of life.

Previous studies underscore the importance of social interactions for child language development-particularly interactions characterized by maternal sensitivity, infant-directed speech (IDS), and conversational turn-taking (CT) in one-on-one contexts. Although infants engage in such interactions from the third month after birth, the prospective link between speech input and maternal sensitivity in the first half year of life and later language development has been understudied. We hypothesized that social interactions embodying maternal sensitivity, IDS and CTs in the first 3 months of life, are significantly associated with later language development and tested this using a longitudinal design. Using a sample of 40 3-month-old infants, we assessed maternal sensitivity during a structured mother-infant one-on-one (1:1) interaction based on a well-validated scoring system (the Coding Interactive Behavior system). Language input (IDS, CT) was assessed during naturally occurring interactions at home using the Language ENvironment Analysis (LENA) system. Language outcome measures were obtained from 18 to 30 months of age using the MacArthur-Bates Communicative Development Inventory. Three novel findings emerged. First, maternal sensitivity at 3 months was significantly associated with infants' productive language scores at 18, 21, 24, 27, and 30 months of age. Second, LENA-recorded IDS during mother-infant 1:1 interaction in the home environment at 3 months of age was positively correlated with productive language scores at 24, 27, and 30 months of age. Third, mother-infant CTs during 1:1 interaction was significantly associated with infants' productive language scores at 27 and 30 months of age. We propose that infants' social attention to speech during this early period-enhanced by sensitive maternal one-on-one interactions and IDS-are potent factors in advancing language development.

Generation WhatsApp: inter-brain synchrony during face-to-face and texting communication.

Texting has become one of the most prevalent ways to interact socially, particularly among youth; however, the effects of text messaging on social brain functioning are unknown. Guided by the biobehavioral synchrony frame, this pre-registered study utilized hyperscanning EEG to evaluate interbrain synchrony during face-to-face versus texting interactions. Participants included 65 mother-adolescent dyads observed during face-to-face conversation compared to texting from different rooms. Results indicate that both face-to-face and texting communication elicit significant neural synchrony compared to surrogate data, demonstrating for the first time brain-to-brain synchrony during texting. Direct comparison between the two interactions highlighted 8 fronto-temporal interbrain links that were significantly stronger in the face-to-face interaction compared to texting. Our findings suggest that partners co-create a fronto-temporal network of inter-brain connections during live social exchanges. The degree of improvement in the partners' right-frontal-right-frontal connectivity from texting to the live social interaction correlated with greater behavioral synchrony, suggesting that this well-researched neural connection may be specific to face-to-face communication. Our findings suggest that while technology-based communication allows humans to synchronize from afar, face-to-face interactions remain the superior mode of communication for interpersonal connection. We conclude by discussing the potential benefits and drawbacks of the pervasive use of texting, particularly among youth.

Mother-Infant Brain-to-Brain Synchrony Patterns Reflect Caregiving Profiles.

Biobehavioral synchrony, the coordination of physiological and behavioral signals between mother and infant during social contact, tunes the child's brain to the social world. Probing this mechanism from a two-brain perspective, we examine the associations between patterns of mother-infant inter-brain synchrony and the two well-studied maternal behavioral orientations-sensitivity and intrusiveness-which have repeatedly been shown to predict positive and negative socio-emotional outcomes, respectively. Using dual-electroencephalogram (EEG) recordings, we measure inter-brain connectivity between 60 mothers and their 5- to 12-month-old infants during face-to-face interaction. Thirty inter-brain connections show significantly higher correlations during the real mother-infant face-to-face interaction compared to surrogate data. Brain-behavior correlations indicate that higher maternal sensitivity linked with greater mother-infant neural synchrony, whereas higher maternal intrusiveness is associated with lower inter-brain coordination. Post hoc analysis reveals that the mother-right-frontal-infant-left-temporal connection is particularly sensitive to the mother's sensitive style, while the mother-left-frontal-infant-right-temporal connection indexes the intrusive style. Our results support the perspective that inter-brain synchrony is a mechanism by which mature brains externally regulate immature brains to social living and suggest that one pathway by which sensitivity and intrusiveness exert their long-term effect may relate to the provision of coordinated inputs to the social brain during its sensitive period of maturation.

Technologically-assisted communication attenuates inter-brain synchrony.

The transition to technologically-assisted communication has permeated all facets of human social life; yet, its impact on the social brain is still unknown and the effects may be particularly intense during periods of developmental transitions. Applying a two-brain perspective, the current preregistered study utilized hyperscanning EEG to measure brain-to-brain synchrony in 62 mother-child pairs at the transition to adolescence (child age; M = 12.26, range 10-14) during live face-to-face interaction versus technologically-assisted remote communication. The live interaction elicited 9 significant cross-brain links between densely inter-connected frontal and temporal areas in the beta range [14-30 Hz]. Mother's right frontal region connected with the child's right and left frontal, temporal, and central regions, suggesting its regulatory role in organizing the two-brain dynamics. In contrast, the remote interaction elicited only 1 significant cross-brain-cross-hemisphere link, attenuating the robust right-to-right-brain connectivity during live social moments that communicates socio-affective signals. Furthermore, while the level of social behavior was comparable between the two interactions, brain-behavior associations emerged only during the live exchange. Mother-child right temporal-temporal synchrony linked with moments of shared gaze and the degree of child engagement and empathic behavior correlated with right frontal-frontal synchrony. Our findings indicate that human co-presence is underpinned by specific neurobiological processes that should be studied in depth. Much further research is needed to tease apart whether the "Zoom fatigue" experienced during technological communication may stem, in part, from overload on more limited inter-brain connections and to address the potential cost of social technology for brain maturation, particularly among youth.

Brains in Sync: Practical Guideline for Parent-Infant EEG During Natural Interaction.

Parent-infant EEG is a novel hyperscanning paradigm to measure social interaction simultaneously in the brains of parents and infants. The number of studies using parent-infant dual-EEG as a theoretical framework to measure brain-to-brain synchrony during interaction is rapidly growing, while the methodology for measuring synchrony is not yet uniform. While adult dual-EEG methodology is quickly improving, open databases, tutorials, and methodological validations for dual-EEG with infants are largely missing. In this practical guide, we provide a step-by-step manual on how to implement and run parent-infant EEG paradigms in a neurodevelopmental laboratory in naturalistic settings (e.g., free interactions). Next, we highlight insights on the variety of choices that can be made during (pre)processing dual-EEG data, including recommendations on interpersonal neural coupling metrics and interpretations of the results. Moreover, we provide an exemplar dataset of two mother-infant dyads during free interactions ("free play") that may serve as practice material. Instead of providing a critical note, we would like to move the field of parent-infant EEG forward and be transparent about the challenges that come along with the exciting opportunity to study the development of our social brain within the naturalistic context of dual-EEG.

Maternal chemosignals enhance infant-adult brain-to-brain synchrony.

Maternal body odors serve as important safety-promoting and social recognition signals, but their role in human brain maturation is largely unknown. Utilizing ecological paradigms and dual- electroencephalography recording, we examined the effects of maternal chemosignals on brain-to-brain synchrony during infant-mother and infant-stranger interactions with and without the presence of maternal body odors. Neural connectivity of right-to-right brain theta synchrony emerged across conditions, sensitizing key nodes of the infant's social brain during its maturational period. Infant-mother interaction elicited greater brain-to-brain synchrony; however, maternal chemosignals attenuated this difference. Infants exhibited more social attention, positive arousal, and safety/approach behaviors in the maternal chemosignals condition, which augmented infant-stranger neural synchrony. Human mothers use interbrain mechanisms to tune the infant's social brain, and chemosignals may sustain the transfer of infant sociality from the mother-infant bond to life within social groups.

Sniffing the human body volatile hexadecanal blocks aggression in men but triggers aggression in women.

In terrestrial mammals, body volatiles can effectively trigger or block conspecific aggression. Here, we tested whether hexadecanal (HEX), a human body volatile implicated as a mammalian-wide social chemosignal, affects human aggression. Using validated behavioral paradigms, we observed a marked dissociation: Sniffing HEX blocked aggression in men but triggered aggression in women. Next, using functional brain imaging, we uncovered a pattern of brain activity mirroring behavior: In both men and women, HEX increased activity in the left angular gyrus, an area implicated in perception of social cues. HEX then modulated functional connectivity between the angular gyrus and a brain network implicated in social appraisal (temporal pole) and aggressive execution (amygdala and orbitofrontal cortex) in a sex-dependent manner consistent with behavior: increasing connectivity in men but decreasing connectivity in women. These findings implicate sex-specific social chemosignaling at the mechanistic heart of human aggressive behavior.

Women Have Reduced Ability to Discriminate Body Odors During the Withdrawal Period of Oral Contraception.

INTRODUCTION: Women's olfactory perception varies across the menstrual cycle. The influence of oral contraceptives on this variability remains unclear. METHODS: To further estimate this, we assessed discrimination performance for both body odors and ordinary odorants in 36 women, 18 naturally ovulating, and 18 using oral contraceptives. Each participant was tested once a week over the course of a month, and data was then parsed into menstrual phases. RESULTS: In naturally ovulating women, at the transition from follicular to luteal phases, there was a decline of 19% (p = 0.003) in olfactory discrimination of body odors but not ordinary odorants. In turn, in women using oral contraceptives, only at a later time of the month, at a point corresponding to the late luteal phase and shift from post-ovulation to pre-menstruation, was there a decline of 20% (p = 0.002) in olfactory discrimination performance. Moreover, when we reorganized the data from women using oral contraceptives in order to separately assess the contraceptive withdrawal period (the few days off pills), we observed a 23% reduction (p = 0.01) in discrimination accuracy of body odors but not ordinary odorants during this time alone. CONCLUSIONS: Women have reduced ability to discriminate body odors during the withdrawal period of oral contraception. IMPLICATIONS: If women indeed consider men's body odor in their mate selections, then the oral contraception withdrawal period may not be the best time to make such decisions.

Unexplained repeated pregnancy loss is associated with altered perceptual and brain responses to men's body-odor.

Mammalian olfaction and reproduction are tightly linked, a link less explored in humans. Here, we asked whether human unexplained repeated pregnancy loss (uRPL) is associated with altered olfaction, and particularly altered olfactory responses to body-odor. We found that whereas most women with uRPL could identify the body-odor of their spouse, most control women could not. Moreover, women with uRPL rated the perceptual attributes of men's body-odor differently from controls. These pronounced differences were accompanied by an only modest albeit significant advantage in ordinary, non-body-odor-related olfaction in uRPL. Next, using structural and functional brain imaging, we found that in comparison to controls, most women with uRPL had smaller olfactory bulbs, yet increased hypothalamic response in association with men's body-odor. These findings combine to suggest altered olfactory perceptual and brain responses in women experiencing uRPL, particularly in relation to men's body-odor. Whether this link has any causal aspects to it remains to be explored.

Trial-to-Trial Variability in Electrodermal Activity to Odor in Autism.

Abnormal trial-to-trial variability (TTV) has been identified as a key feature of neural processing that is related to increased symptom severity in autism. The majority of studies evaluating TTV have focused on cortical processing. However, identifying whether similar atypicalities are evident in the peripheral nervous system will help isolate perturbed mechanisms in autism. The current study focuses on TTV in responses from the peripheral nervous system, specifically from electrodermal activity (EDA). We analyzed previously collected EDA data from 17 adults with autism and 19 neurotypical controls who viewed faces while being simultaneously exposed to fear (fear-induced sweat) and neutral odors. Average EDA peaks were significantly smaller and TTV was reduced in the autism group compared to controls, particularly during the fear odor condition. Amplitude and TTV were positively correlated in both groups, but the relationship was stronger in the control group. In addition, TTV was reduced in those with higher Autism Quotient scores but only for the individuals with autism. These findings confirm the existing results that atypical TTV is a key feature of autism and that it reflects symptom severity, although the smaller TTV in EDA contrasts with the previous findings of greater TTV in cortical responses. Identifying the relationship between cortical and peripheral TTV in autism is key for furthering our understanding of autism physiology. LAY SUMMARY: We compared the changes in electrodermal activity (EDA) to emotional faces over the course of repeated faces in adults with autism and their matched controls. The faces were accompanied by smelling fear-inducing odors. We found smaller and less variable responses to the faces in autism when smelling fear odors, suggesting that the peripheral nervous system may be more rigid. These findings were exaggerated in those who had more severe autism-related symptoms.

SmellSpace: An Odor-Based Social Network as a Platform for Collecting Olfactory Perceptual Data.

A common goal in olfaction research is modeling the link between odorant structure and odor perception. Such modeling efforts require large data sets on olfactory perception, yet only a few of these are publicly and freely available. Given that individual odor perception may be informative on personal makeup and interpersonal relationships, we hypothesized that people would gladly provide olfactory perceptual estimates in the context of an odor-based social network. We developed a web-based infrastructure for such a network we called SmellSpace and distributed 10 000 scratch-and-sniff registration booklets each containing a subset of 12 out of 35 microencapsulated odorants. Within ~100 days, we obtained data from ~1000 participants who rated the odorants along 13 verbal descriptors. To verify that these estimates are comparable to lab-collected estimates we tested 26 participants in a controlled lab setting using the same odorants and descriptors. We observed remarkably high overall group correlations between lab and SmellSpace data, implying that this method provides for credible group-representations of odorants. We further estimated the usability of the data by applying to it two previously published models that used odorant structure alone to predict either odorant pleasantness or pairwise odorant perceptual similarity. We observed statistically significant predictions in both cases, thus further implying that the current data may be helpful toward future efforts of modeling olfactory perception from structure. We conclude that an odor-based social network is a potentially useful instrument for collecting extensive data on olfactory perception and here post the complete raw data set from the first ~1000 participants.

Altered responses to social chemosignals in autism spectrum disorder.

Autism spectrum disorder (ASD) is characterized by impaired social communication, often attributed to misreading of emotional cues. Why individuals with ASD misread emotions remains unclear. Given that terrestrial mammals rely on their sense of smell to read conspecific emotions, we hypothesized that misreading of emotional cues in ASD partially reflects altered social chemosignaling. We found no difference between typically developed (TD) and cognitively able adults with ASD at explicit detection and perception of social chemosignals. Nevertheless, TD and ASD participants dissociated in their responses to subliminal presentation of these same compounds: the undetected 'smell of fear' (skydiver sweat) increased physiological arousal and reduced explicit and implicit measures of trust in TD but acted opposite in ASD participants. Moreover, two different undetected synthetic putative social chemosignals increased or decreased arousal in TD but acted opposite in ASD participants. These results implicate social chemosignaling as a sensory substrate of social impairment in ASD.

A social chemosignaling function for human handshaking.

Social chemosignaling is a part of human behavior, but how chemosignals transfer from one individual to another is unknown. In turn, humans greet each other with handshakes, but the functional antecedents of this behavior remain unclear. To ask whether handshakes are used to sample conspecific social chemosignals, we covertly filmed 271 subjects within a structured greeting event either with or without a handshake. We found that humans often sniff their own hands, and selectively increase this behavior after handshake. After handshakes within gender, subjects increased sniffing of their own right shaking hand by more than 100%. In contrast, after handshakes across gender, subjects increased sniffing of their own left non-shaking hand by more than 100%. Tainting participants with unnoticed odors significantly altered the effects, thus verifying their olfactory nature. Thus, handshaking may functionally serve active yet subliminal social chemosignaling, which likely plays a large role in ongoing human behavior.

Disinhibition of olfaction: human olfactory performance improves following low levels of alcohol.

We hypothesize that true human olfactory abilities are obscured by cortical inhibition. Alcohol reduces inhibition. We therefore tested the hypothesis that olfactory abilities will improve following alcohol consumption. We measured olfaction in 85 subjects, 45 in a between-subjects design, and 40 in a repeated-measures within-subjects design before and after consumption of alcoholic or non-alcoholic beverages. Subjects were also assessed using neurocognitive measures of inhibition. Following alcohol consumption, blood alcohol levels ranged from 0.005% to 0.11%. Across subjects, before any consumption of alcohol, we found that individuals who were less inhibited had lower (better) olfactory detection thresholds (r=0.68, p<0.005). Moreover, after alcohol consumption, subjects with low alcohol levels could make olfactory discriminations that subjects with 0% alcohol could not make (chance=33%, alcohol=51.3±22.7%, control=34.7±31.6%, t(43)=2.03, p<0.05). Within subjects, we found correlations between levels of alcohol and olfactory detection (r=0.63, p<0.005) and discrimination (r=-0.50, p<0.05), such that performance was improved at low levels of alcohol (significantly better than baseline for detection) and deteriorated at higher levels of alcohol. Finally, levels of alcohol-induced improved olfactory discrimination were correlated with levels of alcohol-induced cognitive disinhibition (r=0.48, p<0.05). Although we cannot rule out alternative non-inhibitory alcohol-induced routes of influence, we conclude that improved olfaction at low levels of alcohol supports the notion of an inhibitory mechanism obscuring true olfactory abilities.