The development of intrinsic timescales: A comparison between the neonate and adult brain.

In human adults and other mammals, different brain regions have distinct intrinsic timescales over which they integrate information, from shorter in unimodal sensory-motor regions to longer in transmodal higher-order regions. These have been related to cognitive performance and clinical symptoms, but it remains unclear how they develop. We asked if there are regional differences in timescales at birth that could shape learning by acting as an inductive bias, or if they develop later as the temporal statistics of the environment are learned. We used resting-state fMRI to characterise timescales in human neonates and adults. They were highly consistent across two independent neonatal groups, but in both sensory-motor and higher order areas, timescales were longer in infants compared to adults, as might be expected from their less developed myelination, and recent evidence of longer neural segments in infants watching naturalistic stimuli. In adults, we replicated the finding that transmodal areas have longer timescales than sensory-motor areas, but in infants the opposite pattern was found, driven by long infant timescales in the somotomotor network. Across regions within single brain networks, both positive (limbic) and negative (visual) correlations were found between neonates and adults. In conclusion, neonatal timescales were found to be highly structured, but distinct from adults, suggesting they act as an inductive bias that favours learning on longer timescales, particularly in unimodal regions and then develop with experience or maturation. This "take it slow" initial approach might help human infants to create more regularised, holistic representations of the input less bound to fleeting details, which would favour the development of abstract and contextual representations.

The confound of head position in within-session connectome fingerprinting in infants.

Individuals differ in their functional connectome, which can be demonstrated using a "fingerprinting" analysis in which the connectome from an individual in one dataset is used to identify the same person from an independent dataset. Recently, the origin of these fingerprints has been studied by examining if they are present in infants. The results have varied considerably, with identification rates from 10 to 90%. When fingerprinting has been performed by splitting a single imaging session into two split-sessions (within session), identification rates were higher than when two full-sessions (between sessions) were compared. This study examined whether a methodological difference could account for this variation. It was hypothesized that the infant's exact head position in the head coil may affect the measured connectome, due to the gradual inhomogeneity of signal-to-noise in phased-array coils and the breadth of possible positions for a small infant head in a head coil. This study examined the impact of this using resting state functional MRI data from the Developing Human Connectome Project second release. Using functional timeseries, fingerprinting identification was high (84-91%) within a session while between sessions it was low (7%).Using N = 416 infants' head positions, a map of the average signal-to-noise across the physical volume of the head coil was calculated and was used (independent group of 44 infants with two scan sessions) to demonstrate a significant relationship between head position in the head coil and functional connectivity. Using only the head positions (signal-to-noise values extrapolated from the group average map) of the independent group of 44 infants, high identification success was achieved across split-sessions (within session) but not full-sessions (between sessions). Using a model examining factors influencing the stability of the functional connectome, head position was seen as the strongest of the explanatory variables. We conclude within-session fingerprinting is affected by head position and future infant functional fingerprint analyses must use a different strategy or account for this impact.

Oxytocin receptor gene polymorphisms (rs53576) and early paternal care sensitize males to distressing female vocalizations.

The oxytocinergic system is highly involved in social bonding and early caregiver-infant interactions. Here, we hypothesize that oxytocin receptor (OXTR) gene genotype and parental bonding history interact in influencing social development. To address this question, we assessed adult males' arousal (heart rate changes) in response to different distress vocalizations (human female, human infant and bonobo). Region rs53576 of the OXTR gene was genotyped from buccal mucosa cell samples, and a self-report Parental Bonding Instrument was used (which provide information about parental care or parental overprotection). A significant gene-environment interaction between OXTR genotype and parenting style was found to influence participants' social responsivity to female cry vocalizations. Specifically, a history of appropriate paternal care in participants accentuated the heightened social sensitivity determined by G/G homozygosity, while higher versus lower paternal overprotection lead to distinct levels of physiological arousal particularly in A carriers individuals. These results add to our understanding of the dynamic interplay between genetic susceptibility and early environmental experience in shaping the development of appropriate social sensitivity in males.

In utero testosterone exposure influences physiological responses to dyadic interactions in neurotypical adults.

OBJECTIVE: We investigated how different levels of prenatal exposure to testosterone influence physiological reactions to dyadic interactions, hypothesising that higher levels of prenatal testosterone are linked to greater physiological responses. METHOD: Autonomic nervous system responses to dyadic interactions focussed on social or physical norms were measured. Physiological assessment of excitability (heart rate, facial temperature) and a behavioural assessment (Likert items judgements) were run on 25 neurotypical participants who had distinct testosterone exposure levels in utero. In utero exposure to testosterone was assessed measuring 2D : 4D (ratio between the lengths of the index and the ring fingers). RESULTS: Higher testosterone exposure participants showed greater physiological arousal: a greater heart rate decrease, independent from scenario type (p<0.05), and opposite facial temperature changes in response to social (increase) (vs.) physical scenarios (decrease) were found (Left-cheek: p<0.05; Right-cheek: p<0.05). CONCLUSION: These findings suggest a long-term influence of prenatal environment on adults' physiological responses during social situations.

Anxious about rejection, avoidant of neglect: Infant marmosets tune their attachment based on individual caregiver's parenting style.

Children's secure attachment with their primary caregivers is crucial for physical, cognitive, and emotional maturation. Yet, the causal links between specific parenting behaviors and infant attachment patterns are not fully understood. Here we report infant attachment in New World monkeys common marmosets, characterized by shared infant care among parents and older siblings and complex vocal communications. By integrating natural variations in parenting styles and subsecond-scale microanalyses of dyadic vocal and physical interactions, we demonstrate that marmoset infants signal their needs through context-dependent call use and selective approaches toward familiar caregivers. The infant attachment behaviors are tuned to each caregiver's parenting style; infants use negative calls when carried by rejecting caregivers and selectively avoid neglectful and rejecting caregivers. Family-deprived infants fail to develop such adaptive uses of attachment behaviors. With these similarities with humans, marmosets offer a promising model for investigating the biological mechanisms of attachment security.

Maternal physiological calming responses to infant suckling at the breast.

The mother-infant relation is key to infant physical, cognitive and social development. Mutual regulation and cooperation are required to maintain the dyadic system, but the biological foundation of these responses remains to be clarified. In this study, we report the maternal calming responses to infant suckling during breastfeeding. Using behavioral measures and a Holter electrocardiogram as a readout of the maternal autonomic nervous system, the maternal activities during resting, sitting with her infant on her lap, and breastfeeding were assessed. We found that during breastfeeding, mothers talked less and maternal heart rate was lower than during sitting with the infant without breastfeeding. Congruently, maternal heart rate variability measurements indicated a higher parasympathetic activity during breastfeeding. Time-locked analyses suggested that this maternal calming response was initiated by the tactile stimulation at the breast by the infant face or mouth latch, which preceded the perceived milk ejection. These findings suggest that somatosensory stimuli of breastfeeding activate parasympathetic activity in mothers. Just as how the infant Transport Response facilitates the carrying of infants, the maternal calming responses during breastfeeding may promote efficient milk intake by inhibiting spontaneous maternal activities.

A method to soothe and promote sleep in crying infants utilizing the transport response.

Approximately 20%-30% of infants cry excessively and exhibit sleep difficulties for no apparent reason, causing parental stress and even triggering impulsive child maltreatment in a small number of cases.1-8 While several sleep training methods or parental education programs may provide long-term improvement of infant cry and sleep problems, there is yet to be a conclusive recommendation for on-site behavioral interventions.9-13 Previously we have reported that brief carrying of infants transiently reduces infant cry via the transport response, a coordinated set of vagal activation and behavioral calming conserved in altricial mammals.14-18 In this study, we disentangled complex infant responses to maternal holding and transport by combining subsecond-scale, event-locked physiological analyses with dynamic mother-infant interactions. Infant cry was attenuated either by maternal carrying or by reciprocal motion provided by a moving cot, but not by maternal holding. Five-minute carrying promoted sleep for crying infants even in the daytime when these infants were usually awake, but not for non-crying infants. Maternal laydown of sleeping infants into a cot exerted bimodal effects, either interrupting or deepening the infants' sleep. During laydown, sleeping infants were alerted most consistently by the initiation of maternal detachment, then calmed after the completion of maternal detachment in a successful laydown. Finally, the sleep outcome after laydown was associated with the sleep duration before the laydown onset. These data propose a "5-min carrying, 5- to 8- min sitting" scheme for attending to infant cry and sleep difficulties, which should be further substantiated in future studies. VIDEO ABSTRACT.

The Recognition of Cross-Cultural Emotional Faces Is Affected by Intensity and Ethnicity in a Japanese Sample.

Human faces convey a range of emotions and psychobiological signals that support social interactions. Multiple factors potentially mediate the facial expressions of emotions across cultures. To further determine the mechanisms underlying human emotion recognition in a complex and ecological environment, we hypothesized that both behavioral and neurophysiological measures would be influenced by stimuli ethnicity (Japanese, Caucasian) in the context of ambiguous emotional expressions (mid-happy, angry). We assessed the neurophysiological and behavioral responses of neurotypical Japanese adults (N = 27, 13 males) involved in a facial expression recognition task. Results uncover an interaction between universal and culturally-driven mechanisms. No differences in behavioral responses are found between male and female participants, male and female faces, and neutral Japanese versus Caucasian faces. However, Caucasian ambiguous emotional expressions which require more energy-consuming processing, as highlighted by neurophysiological results of the Arousal Index, were judged more accurately than Japanese ones. Additionally, a differential Frontal Asymmetry Index in neuronal activation, the signature of an approach versus avoidance response, is found in male participants according to the gender and emotional valence of the stimuli.

A decade of infant neuroimaging research: What have we learned and where are we going?

The past decade has seen the emergence of neuroimaging studies of infant populations. Incorporating imaging has resulted in invaluable insights about neurodevelopment at the start of life. However, little has been enquired of the experimental specifications and study characteristics of typical findings. This review systematically screened empirical studies that used electroencephalography (EEG), magnetoencephalography (MEG), functional near-infrared spectroscopy (fNIRS), and functional magnetic resonance imaging (fMRI) on infants (max. age of 24 months). From more than 21,000 publications, a total of 710 records were included for analyses. With the exception of EEG studies, infant studies with MEG, fNIRS, and fMRI were most often conducted around birth and at 12 months. The vast majority of infant studies came from North America, with very few studies conducted in Africa, certain parts of South America, and Southeast Asia. Finally, longitudinal neuroimaging studies were inclined to adopt EEG, followed by fMRI, fNIRS, and MEG. These results show that there is compelling need for studies with larger sample sizes, studies investigating a broader range of infant developmental periods, and studies from under- and less-developed regions in the world. Addressing these shortcomings in the future will provide a more representative and accurate understanding of neurodevelopment in infancy.

Using maternal rescue of pups in a cup to investigate mother-infant interactions in mice/rodents.

Efficient parental care is indispensable for survival of the mammalian offspring, and therefore both parents and offspring cooperate to achieve the best performance. For example, when parents transport altricial offspring, the offspring immediately respond by reducing its cry and movement in both human infants and rodent pups. This coordinated set of central, motor and cardiac responses is designated as the Transport Response (TR) and is shown to facilitate maternal carrying in rodents. The present study aims to investigate the core behavioural characteristics of mother-infant interaction, and to investigate the mechanisms underlying the mother-pup cooperation using pharmacological and genetic manipulations (i.e. Oprm1-/). Along with the clear developmental changes of the pups' immobility and posture during maternal carrying as previously reported, there were also adaptations in maternal strategies, particularly in positioning of foothold and oral grasp over the pup's body, with the pups' age and pup's behaviour. Tree-based models elucidated that both of these maternal variables as well as percentage of pups' struggle predict the time required for pup retrieval from a cup. When the sensory-motor control in pups was disturbed by pharmacological or genetic manipulations, these core behaviours were inefficiently performed and impede maternal retrieval. Mother-infant mutual fit is a complex construct where several intermingled mechanisms are involved. Thus mothers and infants, when interacting, should be considered together as one whole system in which any change in one side or the other, affects the output of the whole dyad. The outcome of the interaction relays on a specific dynamic pattern of infant and maternal behaviours, which mutually change and adapt to fit each other's needs. Key features to reach a successful outcome of the interaction were the maternal retrieving strategy and infants' Transport Response behaviour.

Strangers, Friends, and Lovers Show Different Physiological Synchrony in Different Emotional States.

The mere copresence of another person synchronizes physiological signals, but no study has systematically investigated the effects of the type of emotional state and the type of relationship in eliciting dyadic physiological synchrony. In this study, we investigated the synchrony of pairs of strangers, companions, and romantic partners while watching a series of video clips designed to elicit different emotions. Maximal cross-correlation of heart rate variability (HRV) was used to quantify dyadic synchrony. The findings suggest that an existing social relationship might reduce the predisposition to conform one's autonomic responses to a friend or romantic partner during social situations that do not require direct interaction.

Effects of Baby Schema and Mere Exposure on Explicit and Implicit Face Processing.

In an increasingly multicultural society, the way people perceive individuals from the same vs different ethnic groups greatly affects their own and societal well-being. Two psychological effects that influence these perceptions are the Mere-Exposure Effect (MRE), wherein familiarity with certain objects or persons suffices for people to develop a preference for them, and the Baby Schema (BS), a set of specific facial features that evokes caregiving behaviors and an affective orientation in adults. In the present study, we aimed to investigate whether these two effects play a role in implicit physiological responses to babies vs. adults faces belonging to participants in-group vs. out-group. In study 1, the pupillary diameter of 62 Caucasian participants (M = 31; F = 31) who observed adult and infant faces of different ethnic groups (Caucasian, Chinese) was measured. In study 2, brain waves of 38 Caucasian participants (M = 19; F = 19), who observed the same set of faces, were recorded using EEG. In both studies, adults explicit preferences (i.e., attitudes) toward faces were assessed using questionnaires. In Study 1, females showed greater attention to infant than adult faces (BS effect) in both pupils, regardless of the ethnic group of the face. By contrast, males attended to infant more than adult faces for out-group faces only (BS effect). In Study 2, greater left posterior-parietal alpha activation toward out-group compared to in-group adult faces was found in males (MRE). Participants with a low BS effect toward in-group baby faces exhibited greater left posterior alpha activation to out-group than in-group baby faces (MRE). These findings reveal how different levels of sensitivity to in-group infants may moderate perceptions of both in-group and out-group baby faces. Questionnaire measures on attitudes showed that males and females preferred in-group to out-group adult faces (MRE). Participants in Study 2 also reported a greater preference for infants than adults faces (BS effect). These findings explicate the roles of gender and the Baby Schema effect in moderating implicit processing of in-group and out-group faces, despite their lack in moderating explicit reports. Contradictory findings at the implicit (physiological) and explicit (self-report) levels suggest that differential processing of faces may occur at a non-conscious level.

Language development and disorders: Possible genes and environment interactions.

Language development requires both basic cognitive mechanisms for learning language and a rich social context from which learning takes off. Disruptions in learning mechanisms, processing abilities, and/or social interactions increase the risks associated with social exclusion or developmental delays. Given the complexity of language processes, a multilevel approach is proposed where both cognitive mechanisms, genetic and environmental factors need to be probed together with their possible interactions. Here we review and discuss such interplay between environment and genetic predispositions in understanding language disorders, with a particular focus on a possible endophenotype, the ability for statistical sequential learning.

Putting salient vocalizations in context: Adults' physiological arousal to emotive cues in domestic and external environments.

Salient vocalizations are automatically processed and distinguished from emotionally irrelevant information. However, little is known of how contextual, gender and attentional variables interact to modulate physiological responses to salient emotive vocalizations. In this study, electrocardiogram (ECG) was utilized to investigate differences in peripheral nervous activity of men and women to infant cry (IC), infant laughter (IL) and adult cry (AC) in two different situational contexts: the domestic environment (DE) and the outside environment (OE). As the mental state of listeners can affect their response to vocalizations, a between-subject design was applied: one group was instructed to imagine being inside the scenes (Task 1: explicit task), and the other group was told to look at the scenes (Task 2: implicit task). Results revealed that females exhibited lower inter-beat interval (IBI) index in the OE condition, as compared to both males in OE and females in DE conditions, suggesting greater physiological arousal amongst females in response to vocalizations in an outside environment. Additionally, Task 1 revealed that males demonstrated higher Low Frequency/High Frequency (LFHF) index towards AC than IL. Task 2 showed the same association between these two sounds in females. The implicit task also elicited lower LFHF index in response to both IL and IC than control sound (CS), only amongst females. Findings highlight the important roles that contextual information and cognitive demand play in regulating physiological responses to salient emotive vocalizations. Integrated perspectives of physiological responses to emotive vocalizations that consider the influence of internal (adult mental states) and external (environment) contextual information will provide a better understanding of mechanisms underlying emotional processing of salient social cues.

Response to Infant Cry in Clinically Depressed and Non-Depressed Mothers.

BACKGROUND: Bowlby and Ainsworth hypothesized that maternal responsiveness is displayed in the context of infant distress. Depressed mothers are less responsive to infant distress vocalizations (cry) than non-depressed mothers. The present study focuses on acoustical components of infant cry that give rise to responsive caregiving in clinically depressed (n = 30) compared with non-depressed mothers (n = 30) in the natural setting of the home. METHODS: Analyses of infant and mother behaviors followed three paths: (1) tests of group differences in acoustic characteristics of infant cry, (2) tests of group differences of mothers' behaviors during their infant's crying, and (3) tree-based modeling to ascertain which variable(s) best predict maternal behaviors during infant cry. RESULTS: (1) Infants of depressed mothers cried as frequently and for equal durations as infants of non-depressed mothers; however, infants of depressed mothers cried with a higher fundamental frequency (f0) and in a more restricted range of f0. (2) Depressed mothers fed, rocked, and touched their crying infants less than non-depressed mothers, and depressed mothers were less responsive to their infants overall. (3) Novel tree-based analyses confirmed that depressed mothers engaged in less caregiving during their infants' cry and indicated that depressed mothers responded only to cries at higher f0s and shorter durations. Older non-depressed mothers were the most interactive with infants. CONCLUSIONS: Clinical depression affects maternal responsiveness during infant cry, leading to patterns of action that appear poorly attuned to infant needs.

Dataset on genetic and physiological adults׳ responses to social distress.

Both expectations towards interactions with conspecifics, and genetic predispositions, affect adults׳ social behaviors. However, the underlying mechanisms remain largely unknown. Here, we report data to investigate the interaction between genetic factors, (oxytocin receptor (OXTR) and serotonin transporter (5-HTTLPR) polymorphisms), and adult interactional patterns in shaping physiological responses to social distress. During the presentation of distress vocalizations (cries of human female, infants and bonobos) we assessed participants׳ (N = 42 males) heart rate (HR) and peripheral nose temperature, which index state of arousal and readiness to action. Self-reported questionnaires were used to evaluate participants' interactional patterns towards peers (Attachment Style Questionnaire, Feeney et al., 1994[1]), and the quality of bond with intimate partners (Experiences in Close Relationships Scale, Fraley et al., 2000 [2]). To assess participants׳ genetic predispositions, the OXTR gene (regions rs53576, and rs2254298) and the 5-HTTLPR gene (region SLC6A4) were genotyped. The data set is made publicly available to enable critical or extended analyzes.

Genetic predispositions and parental bonding interact to shape adults' physiological responses to social distress.

Parental bonding and oxytocin receptor (OXTR) gene genotype each influences social abilities in adulthood. Here, we hypothesized an interaction between the two - environmental experience (parental bonding history) and genetic factors (OXTR gene genotype) - in shaping adults' social sensitivity (physiological response to distress). We assessed heart rate and peripheral temperature (tip of the nose) in 42 male adults during presentation of distress vocalizations (distress cries belonging to female human infants and adults as well as bonobo). The two physiological responses index, respectively, state of arousal and readiness to action. Participants' parental bonding in childhood was assessed through the self-report Parental Bonding Instrument. To assess participants' genetic predispositions, buccal mucosa cell samples were collected, and region rs2254298 of the oxytocin receptor gene was analyzed: previous OXTR gene findings point to associations between the G allele and better sociality (protective factor) and the A allele and poorer sociality (risk factor). We found a gene * environment interaction for susceptibility to social distress: Participants with a genetic risk factor (A carriers) with a history of high paternal overprotection showed higher heart rate increase than those without this risk factor (G/G genotype) to social distress.Also, a significant effect of the interaction between paternal care and genotype on nose temperature changes was found. This susceptibility appears to represent an indirect pathway through which genes and experiences interact to shape mature social sensitivity in males.

Serotonin Transporter Gene Polymorphisms and Early Parent-Infant Interactions Are Related to Adult Male Heart Rate Response to Female Crying.

Adults' adaptive interactions with intimate partners enhance well-being. Here we hypothesized that adult males' physiological responses to opposite-sex conspecifics' distress result from an interaction between an environmental factor (early social interaction with caregivers) and a genetic factor (a polymorphism within the promoter region of the serotonin transporter gene, 5-HTTLPR). We assessed heart rate changes in 42 non-married male adults to distress vocalizations (female, infant, and bonobo cries). Males' early interaction with parents was assessed using the Parental Bonding Instrument. Buccal mucosa cell samples were collected to assess their 5-HTTLPR genotype. A significant interaction emerged between early experience and genetic predisposition. Males with a genetic predisposition for higher sensitivity to environmental factors showed atypical physiological responses to adult female cries according to their experienced early maternal parenting. Environmental experiences and genetic characteristics are associated with adult males' physiological responses to socially meaningfully stimuli. Understanding the mechanisms that modulate responses to opposite-sex conspecifics may improve personal well-being and social adaptiveness.

Physiological responses to dyadic interactions are influenced by neurotypical adults' levels of autistic and empathy traits.

Autistic traits are distributed on a continuum that ranges from non-clinical to clinical condition. Atypical responses to social situations represent a core feature of the Autism Spectrum Disorders phenotype. Here, we hypothesize that atypical physiological responses to social stimuli may predict non-clinical autistic and empathy traits levels. We measured physiological responses (heart rate, facial temperature) of 40 adults (20F) while showing them 24 movies representing dyadic interactions. Autistic traits were assessed through Autism Quotient questionnaire (AQ), while empathy traits were measured using the Empathy Quotient questionnaire (EQ). Opposite correlations between AQ and EQ scores and physiological responses were found. Analysis of physiological responses revealed that individuals with better social abilities, low AQ and high EQ, show opposite activation patterns compared to people with high AQ and low EQ. Findings show that physiological responses could be biomarkers for people's autistic traits and social abilities.

Maternal bonding in childhood moderates autonomic responses to distress stimuli in adult males.

Mother-child bonding influences the development of cognitive and social skills. In this study we investigate how maternal attachment, developed in early childhood, modulates physiological responses to social stimuli later in life. Our results suggest that the autonomic nervous system's responses to vocal distress are moderated by the quality of participants' maternal bonding. In particular, participants with optimal maternal bonding showed a greater calming response to distressful stimuli whereas participants with non-optimal maternal bonding showed a heightened distress response.