Infant brain responses to live face-to-face interaction with their mothers: Combining functional near-infrared spectroscopy (fNIRS) with a modified still-face paradigm.

BACKGROUND Non-invasive imaging techniques, such as fNIRS, allow us to shed light on the neural correlates of infant's social-emotional development within the context of parent-infant interaction. On a behavioral level, numerous studies have investigated parent-infant interaction employing the still-face paradigm and found that the primary caregiver(s), often the mother, is an important coregulator of the infant's physiological and behavioral stress response. However, limited information is available on how the infant's brain reacts to the maternal cues during real-life interaction. METHODS Therefore, the main aim of the current study was to design a fNIRS paradigm to study live mother-infant interaction and to explore the neural correlates of infant affect regulation during real-life dyadic interaction. To this end, a modified still-face paradigm was designed, which consists of live face-to-face mother-infant, and stranger-infant, interaction episodes, including stressful, "still-face" and non-stressful, "happy-face" interaction blocks, combined with infant fNIRS imaging. RESULTS Hemodynamic brain responses were collected in n = 10 (6 females, mean age 230.2 ± 17.5 days), typically developing infants using the Hitachi ETG-4000 continuous-wave system (22 channels spanning the frontal cortex; 10 Hz system sampling frequency). Infants with usable data (n = 7) showed negative activations, indicated by a decrease in oxygenated hemoglobin, over the middle frontal gyrus in response to happy-face (reunion) interaction with their mothers compared to a female stranger; suggesting deactivation of brain regions associated with affect regulation. We also explored correlations between infant brain responses to maternal interaction and infant characteristics (temperament) as well as experiential/environmental factors (mothers' self-reported depression symptoms). CONCLUSIONS Although the current results are very preliminary, they overall suggest that live design in infant populations is doable and offers unique opportunities to study the neural mechanisms underlying early caregiver(s)-child interaction in a more naturalistic context. Restrictions, and implications, of the methodology are critically discussed.

[1]  Tobias Grossmann,et al.  The role of medial prefrontal cortex in early social cognition , 2013, Front. Hum. Neurosci..

[2]  Ross E. Vanderwert,et al.  The use of near-infrared spectroscopy in the study of typical and atypical development , 2014, NeuroImage.

[3]  Della J. Derscheid,et al.  Emotional availability (EA): Theoretical background, empirical research using the EA Scales, and clinical applications , 2014 .

[4]  Katherine L. Perdue,et al.  Motion correction for infant functional near-infrared spectroscopy with an application to live interaction data , 2018, Neurophotonics.

[5]  S. Pauen,et al.  [Assessment of temperament with the Infant Behavior Questionnaire Revised (IBQ-R) - the psychometric properties of a German version]. , 2012, Zeitschrift fur Kinder- und Jugendpsychiatrie und Psychotherapie.

[6]  Cécile Issard,et al.  Variability of the hemodynamic response in infants: Influence of experimental design and stimulus complexity , 2018, Developmental Cognitive Neuroscience.

[7]  D. Boas,et al.  HomER: a review of time-series analysis methods for near-infrared spectroscopy of the brain. , 2009, Applied optics.

[8]  Ivan Mervielde,et al.  Temperament, Personality and Developmental Psychopathology: A Review Based on the Conceptual Dimensions Underlying Childhood Traits , 2010, Child psychiatry and human development.

[9]  A. Blasi,et al.  Illuminating the developing brain: The past, present and future of functional near infrared spectroscopy , 2010, Neuroscience & Biobehavioral Reviews.

[10]  C. Nelson,et al.  Early Adverse Experiences and the Developing Brain , 2016, Neuropsychopharmacology.

[11]  Tracy L. Spinrad,et al.  Emotion-related self-regulation and its relation to children's maladjustment. , 2010, Annual review of clinical psychology.

[12]  Christian Gerloff,et al.  Brain-to-brain synchrony in parent-child dyads and the relationship with emotion regulation revealed by fNIRS-based hyperscanning , 2018, NeuroImage.

[13]  G. Csibra,et al.  Are you talking to me? Neural activations in 6-month-old infants in response to being addressed during natural interactions , 2015, Cortex.

[14]  G. Ding,et al.  Leader emergence through interpersonal neural synchronization , 2015, Proceedings of the National Academy of Sciences.

[15]  Tomer Fekete,et al.  Small-world network properties in prefrontal cortex correlate with predictors of psychopathology risk in young children: A NIRS study , 2014, NeuroImage.

[16]  T. Grossmann.  Mapping prefrontal cortex functions in human infancy , 2013 .

[17]  T. Field,et al.  Still-face and separation effects on depressed mother-infant interactions. , 2007, Infant mental health journal.

[18]  Prisca Stenneken,et al.  Exploring the Neural Basis of Real-Life Joint Action: Measuring Brain Activation during Joint Table Setting with Functional Near-Infrared Spectroscopy , 2011, Front. Hum. Neurosci..

[19]  Shozo Kojima,et al.  Cerebral responses to infant-directed speech and the effect of talker familiarity , 2012, NeuroImage.

[20]  S. Goodman,et al.  Maternal Depression and Child Psychopathology: A Meta-Analytic Review , 2011, Clinical child and family psychology review.

[21]  Laura Pirazzoli,et al.  Optical imaging during toddlerhood: brain responses during naturalistic social interactions , 2018, Neurophotonics.

[22]  Kazuo Hiraki,et al.  Infant's brain responses to live and televised action , 2006, NeuroImage.

[23]  Masato Fukuda,et al.  Frontopolar activation during face-to-face conversation: An in situ study using near-infrared spectroscopy , 2010, Neuropsychologia.

[24]  B. Herpertz-Dahlmann,et al.  Like mother, like child? Maternal determinants of children's early social-emotional development. , 2019, Infant mental health journal.

[25]  J. Silk,et al.  The Role of the Family Context in the Development of Emotion Regulation. , 2007, Social development.

[26]  T. Beauchaine,et al.  Trait Impulsivity and the Externalizing Spectrum. , 2017, Annual review of clinical psychology.

[27]  H. Hart,et al.  Neuroimaging of child abuse: a critical review , 2012, Front. Hum. Neurosci..

[28]  R. Kakigi,et al.  I know this face: neural activity during mother's face perception in 7- to 8-month-old infants as investigated by near-infrared spectroscopy. , 2011, Early human development.

[29]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[30]  Nancy L. McElwain,et al.  Maternal sensitivity to infant distress and nondistress as predictors of infant-mother attachment security. , 2006, Journal of family psychology : JFP : journal of the Division of Family Psychology of the American Psychological Association.

[31]  Thomas E. Nichols,et al.  Best practices in data analysis and sharing in neuroimaging using MRI , 2017, Nature Neuroscience.

[32]  M. Ainsworth,et al.  Infant crying and maternal responsiveness. , 1972, Child development.

[33]  A. Beck,et al.  Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. , 1996, Journal of personality assessment.

[34]  M. Hautzinger,et al.  Reliabilität und Validität des revidierten Beck-Depressions-inventars (BDI-II). Befunde aus deutschsprachigen Stichproben , 2007 .

[35]  M. Zentner,et al.  What Is Temperament Now? Assessing Progress in Temperament Research on the Twenty‐Fifth Anniversary of Goldsmith et al. () , 2012 .

[36]  Guy A Dumont,et al.  Wavelet-based motion artifact removal for functional near-infrared spectroscopy , 2012, Physiological measurement.

[37]  S. Calkins,et al.  Longitudinal Associations Between the Quality of Mother-Infant Interactions and Brain Development Across Infancy. , 2016, Child development.

[38]  T. Egner,et al.  Emotional processing in anterior cingulate and medial prefrontal cortex , 2011, Trends in Cognitive Sciences.

[39]  John E. Richards,et al.  A database of age-appropriate average MRI templates , 2016, NeuroImage.

[40]  S. Arridge,et al.  Estimation of optical pathlength through tissue from direct time of flight measurement , 1988 .

[41]  I. Goodyer,et al.  Maternal postnatal depression and the development of depression in offspring up to 16 years of age. , 2011, Journal of the American Academy of Child and Adolescent Psychiatry.

[42]  H. Lagercrantz,et al.  Activation of the right fronto‐temporal cortex during maternal facial recognition in young infants , 2008, Acta paediatrica.

[43]  M. Rothbart,et al.  Studying infant temperament via the Revised Infant Behavior Questionnaire , 2003 .

[44]  M. Hautzinger,et al.  Reliabilität und Validität des revidierten Beck-Depressionsinventars (BDI-II) , 2007, Der Nervenarzt.

[45]  Mark H. Johnson,et al.  Hand or spoon? Exploring the neural basis of affective touch in 5-month-old infants , 2018, Developmental Cognitive Neuroscience.

[46]  T. Ono,et al.  Selective Medial Prefrontal Cortex Responses During Live Mutual Gaze Interactions in Human Infants: An fNIRS Study , 2015, Brain Topography.

[47]  Lauren L Emberson,et al.  Hemodynamic correlates of cognition in human infants. , 2015, Annual review of psychology.

[48]  Rebecca C. Knickmeyer,et al.  A Structural MRI Study of Human Brain Development from Birth to 2 Years , 2008, The Journal of Neuroscience.

[49]  Eric A. Walle,et al.  Interpersonal Responding to Discrete Emotions: A Functionalist Approach to the Development of Affect Specificity , 2012 .

[50]  Judi Mesman,et al.  The many faces of the Still-Face Paradigm: A review and meta-analysis , 2009 .

[51]  Mikko J. Peltola,et al.  Attention to Faces Expressing Negative Emotion at 7 Months Predicts Attachment Security at 14 Months , 2015, Child development.

[52]  D. Delpy,et al.  System for long-term measurement of cerebral blood and tissue oxygenation on newborn infants by near infra-red transillumination , 1988, Medical and Biological Engineering and Computing.

[53]  S. Hinshaw,et al.  Attention-Deficit/Hyperactivity Disorder, Trait Impulsivity, and Externalizing Behavior in a Longitudinal Sample , 2017, Journal of abnormal child psychology.

[54]  R. Feldman.  Parent-infant synchrony and the construction of shared timing; physiological precursors, developmental outcomes, and risk conditions. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[55]  S. M. Carlson,et al.  From external regulation to self-regulation: early parenting precursors of young children's executive functioning. , 2010, Child development.

[56]  Katherine L. Perdue,et al.  The infant brain in the social world: Moving toward interactive social neuroscience with functional near-infrared spectroscopy , 2018, Neuroscience & Biobehavioral Reviews.

[57]  Sabrina Brigadoi,et al.  Recommendations for motion correction of infant fNIRS data applicable to multiple data sets and acquisition systems , 2019, NeuroImage.

[58]  R. Feldman.  The Neurobiology of Human Attachments , 2017, Trends in Cognitive Sciences.

[59]  Ippeita Dan,et al.  Prefrontal activation associated with social attachment: facial-emotion recognition in mothers and infants. , 2009, Cerebral cortex.

[60]  D. Delpy,et al.  Optical pathlength measurements on adult head, calf and forearm and the head of the newborn infant using phase resolved optical spectroscopy. , 1995, Physics in medicine and biology.

[61]  Xian Zhang,et al.  Frontal temporal and parietal systems synchronize within and across brains during live eye-to-eye contact , 2017, NeuroImage.

[62]  Katherine L. Perdue,et al.  Extraction of heart rate from functional near-infrared spectroscopy in infants , 2014, Journal of biomedical optics.

[63]  T. Brazelton,et al.  The infant's response to entrapment between contradictory messages in face-to-face interaction. , 1978, Journal of the American Academy of Child Psychiatry.

[64]  N. Ekas,et al.  Attachment in the making: mother and father sensitivity and infants' responses during the Still-Face Paradigm. , 2014, Journal of experimental child psychology.

[65]  Lauren L Emberson,et al.  Isolating the effects of surface vasculature in infant neuroimaging using short-distance optical channels: a combination of local and global effects , 2016, Neurophotonics.

[66]  R. Sullivan,et al.  Neurobiology of infant attachment: attachment despite adversity and parental programming of emotionality. , 2017, Current opinion in psychology.

[67]  Ruth Feldman,et al.  The adaptive human parental brain: implications for children's social development , 2015, Trends in Neurosciences.

[68]  S. Pauen,et al.  Erfassung des frühkindlichen Temperaments mit dem Infant Behavior Questionnaire Revised , 2012 .

[69]  Joseph P. McCleery,et al.  Effects of maternal depression in the Still-Face Paradigm: A meta-analysis. , 2018, Infant behavior & development.

[70]  Ross E. Vanderwert,et al.  Infants’ neural responses to facial emotion in the prefrontal cortex are correlated with temperament: a functional near-infrared spectroscopy study , 2015, Front. Psychol..

[71]  Kazuo Hiraki,et al.  Sustained decrease in oxygenated hemoglobin during video games in the dorsal prefrontal cortex: A NIRS study of children , 2006, NeuroImage.