Right frontoinsular cortex and subcortical activity to infant cry is associated with maternal mental state talk

Journal of Neuroscience

Volumn 35, Issue 37, 2015, Pages 12725-12732

  Hipwell, Alison E ^a,b   Guo, Chaohui ^a   Phillips, Mary L ^a,b   Swain, James E ^c,d   Moses Kolko, Eydie L ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d YALE UNIVERSITY   (United States)

Author keywords

Affective perceptual empathy; Mental state talk; Right frontoinsular cortex (RFIC); Subcortical limbic region

Indexed keywords

ADULT; ARTICLE; AUDITORY STIMULATION; BEHAVIOR ASSESSMENT; BRAIN ANALYSIS; BRAIN REGION; CHILD; CONTROLLED STUDY; CORRELATION COEFFICIENT; CRYING; FEMALE; FOLLOW UP; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFANT; INFANT CRY; INFORMATION PROCESSING; INTERVIEW; INTRARATER RELIABILITY; MATERNAL CARE; MENTAL HEALTH; MOTHER CHILD RELATION; NEUROIMAGING; PERCEPTION; PRIORITY JOURNAL; PSYCHOSOCIAL CARE; RIGHT FRONTOINSULAR CORTEX; SENSITIVITY ANALYSIS; SOCIOECONOMICS; STIMULUS RESPONSE; SUBCORTICAL LIMBIC REGION; TASK PERFORMANCE; ADOLESCENT; AFRICAN AMERICAN; ASSOCIATION; BIOLOGICAL MODEL; BRAIN CORTEX; BRAIN MAPPING; EMOTION; FRONTAL LOBE; HEMISPHERIC DOMINANCE; LIMBIC SYSTEM; MATERNAL BEHAVIOR; MOTHER; NUCLEAR MAGNETIC RESONANCE IMAGING; OBSERVER VARIATION; PATTERN RECOGNITION; PENNSYLVANIA; PHYSIOLOGY; PSYCHOLOGICAL MODEL; PSYCHOLOGY; THEORY OF MIND; THINKING; VERBAL BEHAVIOR; YOUNG ADULT;

ADOLESCENT; AFRICAN AMERICANS; BRAIN MAPPING; CEREBRAL CORTEX; CRYING; CUES; DOMINANCE, CEREBRAL; EMOTIONS; FEMALE; FRONTAL LOBE; HUMANS; INFANT; LIMBIC SYSTEM; MAGNETIC RESONANCE IMAGING; MATERNAL BEHAVIOR; MODELS, NEUROLOGICAL; MODELS, PSYCHOLOGICAL; MOTHER-CHILD RELATIONS; MOTHERS; OBSERVER VARIATION; PATTERN RECOGNITION, PHYSIOLOGICAL; PENNSYLVANIA; SOCIOECONOMIC FACTORS; THEORY OF MIND; THINKING; VERBAL BEHAVIOR; YOUNG ADULT;

EID: 84941782969     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1286-15.2015     Document Type: Article

References (56)

1. Abu-Akel A (2003) A neurobiological mapping of theory of mind. Brain Res Brain Res Rev 43:29–40. CrossRef Medline
2. Barrett J, Wonch KE, Gonzalez A, Ali N, Steiner M, Hall GB, Fleming AS (2012) Maternal affect and quality of parenting experiences are related to amygdala response to infant faces. Soc Neurosci 7:252–268. CrossRef Medline
3. Berlin LJ, Dodge KA, Reznick JS (2013) Examining pregnant women’s hostile attributions about infants as a predictor of offspring maltreatment. JAMA Pediatr 167:549–553. CrossRef Medline
4. Campbell SB, Matestic P, von Stauffenberg C, Mohan R, Kirchner T (2007) Trajectoriesofmaternaldepressivesymptoms, maternalsensitivity,andchildren’sfunctioning at school entry. Dev Psychol 43:1202–1215. CrossRef Medline
5. Carr L, lacoboni M, Dubeau MC, Mazziotta JC, Lenzi GL (2005) Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas. In: Social neuroscience: key readings, pp 143–152. New York: Psychology Press.
6. Carter RM, Huettel SA (2013) A nexus model of the temporal-parietal junction. Trends Cogn Sci 17:328–336. CrossRef Medline
7. Cooper G, Hoffman K, Powell B, Marvin R (2005) The circle of security intervention: differential diagnosis and differential treatment. In: Enhancing early attachments: theory, research, intervention, and policy, pp 127–151. New York: Guilford.
8. Cox JL, Holden JM, Sagovsky R (1987) Detection of postnatal depression: development of the 10-item Edinburgh Postnatal Depression Scale. Br J Psychiatry 150:782–786. Cross Ref Medline
9. Decety J (2015) The neural pathways, development and functions of empathy. Curr Opin Behav Sci 3:1–6.
10. CrossRef Doan SN, Wang Q (2010) Maternal discussions of mental states and behaviors: relations to emotion situation knowledge in European American and immigrant Chinese children. Child Dev 81:1490–1503. CrossRef Medline
11. Edge D (2007) Ethnicity, psychosocial risk, and perinatal depression—a comparative study among inner-city women in the United Kingdom. J Psychosom Res 63:291–295. CrossRef Medline
12. Fan Y, Duncan NW, de Greck M, Northoff G (2011) Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neurosci Biobeh Rev 35:903–911. CrossRef Medline
13. Geronimus AT (2003) Damned if you do: culture, identity, privilege, and teenage childbearing in the United States. Soc Sci Med 57:881– 893. CrossRef Medline
14. Gibson J, McKenzie-McHarg K, Shakespeare J, Price J, Gray R (2009) A systematic review of studies validating the Edinburgh Postnatal Depression Scale in antepartum and postpartum women. Acta Psychiat Scand 119:350–364. CrossRef Medline
15. Hare TA, Camerer CF, Knoepfle DT, Rangel A (2010) Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J Neurosci 30:583–590. CrossRef Medline
16. Hipwell AE, Loeber R, Stouthamer-Loeber M, Keenan K, White HR, Kroneman L (2002) Characteristics of girls with early onset disruptive and antisocial behaviour. Crim Behav Ment Health 12:99–118. Cross Ref Medline
17. Ho SS, Konrath S, Brown S, Swain JE (2014) Empathy and stress related neural responses in maternal decision making. Front Neurosci 8:152. Cross Ref Medline
18. Iacoboni M, Dapretto M (2006) The mirror neuron system and the consequences of its dysfunction. Nat Rev Neurosci 7:942–951. CrossRef Medline
19. Johnson MK, Raye CL, Mitchell KJ, Touryan SR, Greene EJ, Nolen-Hoeksema S (2006) Dissociating medial frontal and posterior cingulate activity during selfreflection. Soc Cogn Affect Neurosci 1:56–64. CrossRef Medline
20. Kaitz M, Maytal HR, Devor N, Bergman L, Mankuta D (2010) Maternal anxiety, mother-infant interactions, and infants’ response to challenge. Infant Behav Dev 33:136–148. CrossRef Medline
21. Keenan K, Hipwell A, Chung T, Stepp S, Stouthamer-Loeber M, Loeber R, McTigue K (2010) The Pittsburgh Girls Study: overview and initial findings. J Clin Child Adolesc Psychol 39:506–521. CrossRef Medline
22. Kim P, Feldman R, Mayes LC, Eicher V, Thompson N, Leckman JF, Swain JE (2011) Breastfeeding, brain activation to own infant cry, and maternal sensitivity. J Child Psychol Psychiatry 52:907–915. CrossRef Medline
23. Laranjo J, Bernier A, Meins E (2008) Associations between maternal mind- mindedness and infant attachment security: investigating the mediating role of maternal sensitivity. Infant Behav Dev 31:688–695. CrossRef Medline
24. Le Bouc R, Pessiglione M (2013) Imaging social motivation: distinct brain mechanisms drive effort production during collaboration versus competition. J Neurosci 33:15894–15902. CrossRef Medline
25. Lorber MF, Egeland B (2009) Infancy parenting and externalizing psychopathology from childhood through adulthood: developmental trends. Dev Psychol 45:909–912. CrossRef Medline
26. Mammen O, Kolko D, Pilkonis P (2003) Parental cognitions and satisfaction: relationship to aggressive parental behavior in child physical abuse. Child Maltreatment 8:288–301. CrossRef Medline
27. Mars RB, Sallet J, Schüffelgen U, Jbabdi S, Toni I, Rushworth MF (2012) Connectivity-based subdivisions of the human right “temporoparietal junction area”: evidence for different areas participating in different cortical networks. Cereb Cortex 22:1894–1903. CrossRef Medline
28. Meins E, Fernyhough C (1999) Linguistic acquisitional style and mentalising development: the role of maternal mind-mindedness. Cognit Dev 14:363–380. CrossRef
29. Meins E, Fernyhough C, Wainwright R, Clark-Carter D, Das Gupta M, Fradley E, Tuckey M (2003) Pathways to understanding mind: construct validity and predictive validity of maternal mind-mindedness. Child Dev 74:1194–1211. CrossRef Medline
30. Meins E, Fernyhough C, de Rosnay M, Arnott B, Leekam SR, Turner M (2012) Mind-mindedness as a multidimensional construct: appropriate and nonattuned mind-related comments independently predict infantmother attachment in a socially diverse sample. Infancy 17:393–415. CrossRef
31. Menkes J, Sarnat H, Moser F (2000) Neurologic examination of the child and infant. In: Child neurology, Ed 6 (Menkes J, Sarnat H, eds), pp 1–32. Philadelphia: Lippincott Williams and Wilkins.
32. Merrick EN (1995) Adolescent childbearing as career “choice”: perspective from an ecological context. J Counsel Dev 73:288–295. CrossRef
33. Molenberghs P, Cunnington R, Mattingley JB (2012) Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci Biobehav Rev 36:341–349. CrossRef Medline
34. Moses-Kolko EL, Horner MS, Phillips ML, Hipwell AE, Swain JE (2014) In search of neural endophenotypes of postpartum psychopathology and disrupted maternal caregiving. J Neuroendocrinol 26:665–684. CrossRef Medline
35. Musser ED, Kaiser-Laurent H, Ablow JC (2012) The neural correlates of maternal sensitivity: an fMRI study. Dev Cogn Neurosci 2:428–436. CrossRef Medline
36. Numan M, Woodside B (2010) Maternity: Neural mechanisms, motivational processes, and physiological adaptations. Behav Neurosci 124: 715–741. CrossRef Medline
37. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113. CrossRef Medline
38. Parfitt Y, Pike A, Ayers S (2013) The impact of parents’ mental health on parent-baby interaction: a prospective study. Infant Behav Dev 36: 599–608. CrossRef Medline
39. Rizzolatti G, Fabbri-Destro M (2008) The mirror system and its role in social cognition. Curr Opin Neurobiol 18:179–184. CrossRef Medline
40. Sadler LS, Slade A, Close N, Webb DL, Simpson T, Fennie K, Mayes LC(2013) Minding the baby: enhancing reflectiveness to improve early health and relationship outcomes in an interdisciplinary home-visiting program. Infant Ment Health J 34:391–405. CrossRef Medline
41. Sander K, Frome Y, Scheich H (2007) FMRI activations of amygdala, cingulated cortex, and auditory cortex by infant laughing and crying. HumBrain Mapp 28:1007–1022. CrossRef Medline
42. Saxe R, Kanwisher N (2003) People thinking about thinking people. The role of the temporo-parietal junction in “theory of mind.” Neuroimage 19:1835–1842. CrossRef
43. Sharp C, Fonagy P (2008) The parent’s capacity to treat the child as a psychological agent: constructs, measures and implications for developmental psychopathology. Soc Dev 17:737–754. CrossRef
44. Shaw DS, Winslow EB, Owens EB, Vondra JI, Cohn JF, Bell RQ (1998) The development of early externalizing problems among children from lowincome families: a transformational perspective. J Abnorm Child Psychol 26:95–107. CrossRef Medline
45. Soltis J (2004) The signal functions of early infant crying. Behav Brain Sci 27:443–458; discussion 459–490. Medline
46. Strathearn L, Kim S (2013) Mothers’ amygdala response to positive or negative infant affect is modulated by personal relevance. Front Neurosci 7:176. CrossRef Medline
47. Swain JE, Lorberbaum JF (2008) Imaging the human parental brain. In: Neurobiology of the parental brain (Bridges R, ed.), pp 83–100. New York: Academic. CrossRef
48. Swain JE, Mayes LC, Leckman JF (2004) The development of parent-infant attachment through dynamic and interactive signalling loops of care and cry. Behav Brain Sci 27:472–473. CrossRef
49. Swain JE, Lorberbaum JP, Kose S, Strathearn L (2007) Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry 48:262–287. CrossRef Medline
50. Swain JE, Tasgin E, Mayes LC, Feldman R, Constable RT, Leckman JF (2008) Maternal brain response to own baby-cry is affected by cesarean section delivery. J Child Psychol Psychiatry 49:1042–1052. CrossRef Medline
51. Swain JE, Konrath S, Brown SL, Finegood ED, Akce LB, Dayton CJ, Ho S (2012) Parenting and beyond: common neurocircuits underlying parental and altruistic caregiving. Parent Sci Practice 12:115–123. CrossRef
52. Swain JE, Kim P, Spicer J, Ho SS, Dayton CJ, Elmadih A, Abel KM (2014) Approaching the biology of human parental attachment: Brain imaging, oxytocin and coordinated assessments of mothers and fathers. Brain Res 1580:78–101. CrossRef Medline
53. Taumoepeau M, Ruffman T (2008) Stepping stones to others’ minds: Maternal talk relates to child mental state language and emotion understanding at 15, 24, and 33 months. Child Dev 79:284–302. CrossRef Medline
54. Tronick EZ, Olson K, Rosenberg R, Bohne L, Lu J, Lester BM (2004) Normative neurobehavioral performance of healthy infants on the neonatal intensive care un t network neurobehavioral scale. Pediatrics 113:676–678. Medline
55. Van Overwalle F, Baetens K (2009) Understanding others’ actions and goals by mirror and mentalizing systems: a meta-analysis. Neuroimage 48: 564–584. CrossRef Medline
56. Young L, Camprodon JA, Hauser M, Pascual-Leone A, Saxe R (2010) Disruption of the right temporoparietal junction with transcranial magnetic stimulation reduces the role of beliefs in moral judgments. Proc Natl Acad Sci U S A 107:6753–6758. CrossRef Medline