The Adaptive Human Parental Brain: Implications for Children's Social Development
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The adaptive human parental brain: implications for children's social development
Ruth Feldman1,2
1Gonda Multidisciplinary Brain Center, Bar-Ilan University, Tel Aviv, Israel
2Yale University School of Medicine, New Haven, CO, USA
Corresponding author: Feldman, G. ().
Empirical findings regarding the parental brain
Authors & Publication Year / Reference / Subjects / Stimuli / Covariates / ResultsLorberbaum et al. 1999 / [1] / 7 mothers (children 4 years old) / infant cry Vs control sound / Cry> Control: subgenual right anterior cingulate cortex, right middle frontal gyrus, right superior frontal gyrus
Lorberbaum et al. 2002 / [2] / 10 mothers 4-8 weeks post-partum / infant cry Vs control sound / Cry> Control: midbrain, hypothalamus, substantia nigra, VTA, PAG, thalamic nuclei, pulvinar nuclei, striatum, putamen, caudate (GP/BNST), ACC, OFC, prefrontal, TP, insula, dlPFC, and amygdala.
Swain et al. 2008 / [3] / 12 mothers- 6 vaginal delivery (VD)/6 caesarian section (CSD) ( 2-4 weeks post-partum) / own Vs unknown infant cry / parental preoccupation (AITHAR) and depression measure (BDI) / Cry>Control/VD>CSD: anterior cingulate, hypothalamus, basal ganglia, superior and inferior temporal cortex, frontal premotor insular cortex, thalamus, pons and cerebellum. Own>Unknown/VD>CSD: frontal cortex circuits, hypothalamus, basal ganglia, temporal cortex, parietal cortex, caudate head, thalamus and pons. AITHAR-Own cry correlation: bilateral lenticular nuclei. BDI- Own cry correlation: superior frontal gyrus.
Bos et al. 2010 / [4] / 16 non-parent women / infant cry Vs control sound / testosterone administration/placebo / Sound>Rest: bilateral Heschl’s gyrus, medial temporal gyrus, rolandic operculum, right motor cortex, right thalamus, the left amygdala, and the bilateral insula. Cry>Control: superior temporal gyrus, extending bilaterally into the medial temporal gyrus and the superior temporal pole. Drug × Stimulus interaction: heightened activation in response to crying compared to control sound in the left cerebellum, thalamus, the posterior cingulate cortex, and the insula in the testosterone condition when compared to placebo
Kim et al. 2010 / [5] / 26 mothers 2-4 weeks post-partum / infant cry Vs control noise + VBN / perceived maternal care (PMC), Subjective perception of parenting and baby (YIPTA-R) / Cry>Control: activated the superior, medial and inferior frontal regions, superior and middle temporal gyri, insula, and cuneus regions. PMC-Cry activation correlation: dorsolateral prefrontal cortex, middle frontal gyrus, precentral gyrus, superior temporal gyrus, fusiform gyrus and lingual gyrus. VBN increase: superior, middle and inferior prefrontal cortex, precentral and postcentral gyrus, superior and inferior parietal lobe, insula and thalamus. Correlation: mother’s positive perception of her baby at Time 1 predicted gray matter volume change in a cluster of the midbrain including hypothalamus, amygdala, and substantia nigra
Kim et al. 2011 / [6] / 17 mothers- 9 breastfeeding/8 formula-feeding (2-4 weeks post-partum) / own Vs unknown infant cry / sensitivity via CIB (obtained at age 3-4 months) / Breastfeeding>Non-breastfeeding: right lateral globus pallidus/putamen, right putamen, left inferior frontal
gyrus, right superior prefrontal gyrus, bilateral insula, right fusiform gyrus, right precuneus, right cuneus, left superior and middle temporal gyrus. Cry activation-Maternal sensitivity correlation: right superior frontal gyrus and right lateral globus pallidus/amygdala
Landi et al. 2011 / [7] / 54 mothers- 28 control/26 substance abuse (2 months post-partum) / high intense and low-intense infant cry vs control sound + happy and sad Vs neutral infant faces / Happy face-SA<Control: vmPFC, right dlPFC/MFG,dmPFC, middle occipital gyrus, right hippocampus/parahippocampus and cerebellum. SA>Control: left posterior parahippocampal gyrus. Sad faces-SA<Control: right and left dlPFC/MFG, medial orbitofrontal cortex, right inferior frontal gyrus, sensorimotor regions, the middle/superior temporal gyrus, PCC, right occipital gyrus/cuneus, right amygdala and parahippocampal gyrus. Nuetral faces-SA<Control: dmPFC/medial, superior frontal gyri, vmPFC, dlPFC, right IFG, cuneus, PCC , and right amygdala/parahippocampal gyrus/globus pallidu. Low intense cry-SA<Control: right superior/middle temporal gyri,medial frontal gyrus/pre-SMA, insula, thalamus, and bilateral
amygdala/parahippocampal gyrus. High intense cry-SA<Control: left superior/MFG, sensorimotor regions, insula, mid cingulate gyrus/precuneus and bilateral amygdala/parahippocampal gyrus
Laurent, Stevens & Ablow, 2011 / [8] / 22 mothers- 11 depressed/ 11 control (children 18 months old) / own Vs unknown infant cry / cortisol / Own cry activation-Cortisol slopes correlation: right anterior ventrolateral prefrontal cortex/frontal pole as well as right superior parietal lobe and occipital pole. Own cry activation-Cortisol quadratic terms correlation: midbrain-PAG, cerebellum, posterior insula–striatum, thalamus, lateral OFC-vlPFC, anterior insula, ACC, dmPFC, and angular gyri.
Riem et al. 2011 / [9] / 43 non-parent women (twin pairs) / infant cry Vs control sound / OT administration/placebo / Cry>Control: bilateral superior and middle temporal gyrus and right amygdala in control group. OT<Placebo: right amygdala. OT>Placebo: inferior frontal g. and insula.
Laurent & Ablow, 2012 / [10] / 22 mothers- 11 depressed/ 11 control (children 18 months old) / own Vs unknown infant cry / strength of depressive symptoms (CESD) / Cry> Control: bilateral anterior insula, OFC, striatum, thalamus and midbrain (substantia nigra/ventral tegmental area, periaqueductal gray), dorsal mPFC, medial superior frontal gyrus (SFG) extending to dACC, left angular gyrus, posterior cingulate cortex and cerebellum. Non-depressed>Depressed/Own>Unknown: dACC, right insula, right occipital fusiform to lingual gyrus and left posterior supramarginal gyrus. Non-depressed- Own>Unknown: R striatum and thalamus. CESD-Own cry negative correlation: right striatum, thalamus, left OFC extending to ventral striatum, dorsal mPFC, occipital fusiform, and lingual gyri.
Montoya et al. 2012 / [11] / 19 non-parent women / high intense and low-intense infant cry vs control sound + happy and sad Vs neutral infant faces / BIS/BAS scale / Low intense cry>Control: bilateral STG, right middle temporal gyrus, bilateral precentral and postcentral gyri, right IPL, left superior and medial frontal gyri, left putamen, and left claustrum. Low intense cry<Control: left caudate and right MFG/OFC. High intense cry>Control: bilateral STG, right MTG, right precentral and postcentral gyri, right SFG, right MFG, right IFG, bilateral amygdala, and left culmen. High intense cry<Control: right STG and right insula. High intense cry<Low intense cry: bilateral STG, right MTG, left IPL, right superior occipital gyrus, and left precuneus. Happy >Neutral faces: left ventral striatum, left caudate head, left vmPFC/OFC, and right IFG. Happy<Neutral: left cingulate gyrus, bilateral precentral gyrus, right SFG, right STG, left supramarginal gyrus,
and left insula. Sad>Neutral faces: bilateral precuneus, left cingulate gyrus, right MTG, bilateral middle and inferior occipital gyri, right fusiform gyrus, left precentral gyrus, left IPL, left lingual gyrus, right SFG, bilateral MFG, right IFG/OFC, and left ACC Sad<Neutral: left insula, left transverse temporal gyrus, and right STG. Happy<Sad faces: right IFG, bilateral FG, right STG, right supramarginal gyrus, right cuneus, left MTG, left middle occipital gyrus, right precentral gyrus, and right MFG. High+ Low intense-BIS correlation: right STG. High intense-BAScorrelation: inversely correlated with activations in right putamen, right caudate extending into the thalamus, right lateral globus pallidus, left medial globus pallidus, and left angular gyrus. Low intense-BAS correlation: inversely correlated with left precentral gyrus. Sad>Neutral- BAS correlation: positively with right superior occipital gyrus.
Musser, Laurent & Ablow, 2012 / [12] / 22 mothers- 11 depressed/ 11 control (children 18 months old) / own Vs unknown infant cry / mother-child interaction measurements / Own>Unknown- Sensitivity correlation: right frontal pole and the inferior frontal gyrusextending to frontal operculum. Own>Unknown- Intrusively correlation:left anteriorinsula and temporal pole. Own>Unknown- Harmonious correlation:left hippocampus extending to parahippocampal gyrus, right parahippocampal, lingual gyri, and right precuneus.
De Pisapia et al. 2013 / [13] / 9 non-parents- 5 male/4 female and 9 parents- 5 female/4 male (children older than 4 years old) / infant hunger cry Vs control cry, white noise and rest / Female>Male(cry>rest): dmPFC and PCC. Female>Male(cry>noise): dmPFC and PCC
Mascaro et al. 2014 / [14] / 36 fathers (children 1-2 years old) / infant cry Vs control sound / Parental Responsibility Scale, Child Rearing Practices Report (CRPR), and CAG repeat polymorphisms / Cry>Control: bilateral IFG extending into the AI and bilateral globus pallidus. Cry- Responsibility correlation: fathers with low and high levels of AI activity participated less in childcare. Cry- Restrictiveness correlation: restrictiveness was negatively correlated to activation in bilateral IFG stretching into the AI, anterior cingulate cortex (ACC) and medial orbitofrontal cortex. Cry-CAG repeats correlation: bilateral IFG and left insula.
Riem et al. 2012 / [15] / 44 non-parent women (twin pairs) / infant laugh Vs control sounds / OT administration/placebo / Placebo- Laugh>Control: bilateral temporal poles, the bilateral superior temporal gyrus, the bilateral OFC, the bilateral inferior and superior frontal gyrus, the bilateral amygdala, the brainstem, and the right putamen. OT>Placebo (laugh>control): amygdala. Connectivity- OT>Placebo (laugh): oxytocin enhanced connectivity between the right amygdala and the left OFC, the bilateral hippocampus, the left precuneus, the right angular gyrus, hippocampus, the left precuneus, the right angular gyrus, and the right middle temporal gyrus.
Bartels & Zeki, 2004 / [16] / 20 mothers (children 9 month-6 year old) / own Vs familiar child picture/ partner Vs acquaintance adult picture / Own>Familiar: medial insula, cingulate gyrus dorsal, ventral of the genu, lateral orbito-frontal cortex, lateral prefrontal cortex, occipital cortex, lateral fusiform cortex, striatum (putamen globus pallidus, and head of the caudate) nucleus, substantia nigra ,subthalamic regions, postero-ventral thalamus, and PAG of the midbrain. Own child+Own partner (overlapping regions): striatum (putamen, globus pallidus, and caudate nucleus), middle insula and dACC. Own child-Own partner (maternal regions): lateral orbito-frontal cortex and PAG
Leibenluft et al. 2004 / [17] / 7 mothers (children 5-12 year old) / own Vs familiar and unknown children face pictures / Own>Familiar: bilaterally anterior paracingulate, dorsolateral prefrontal cortex, left insula,left posterior fusiform gyrus, left STS, right posterior cingulate, precuneus and right amygdala. Familiar>Unknown: right anterior paracingulate, left insula, left STS, and posterior cingulate/precuneus bilaterally. Familiar<Unknown: ventral occipital regions bilaterally, right fusiform gyrus, and the left amygdala. Unknown children>adults: left fusiform gyrus, right STS, left posterior cingulate/precuneus, and left insula. Own>Familiar VS Familiar<Unknown: bilateral paracingulate cortex, left posterior STS, right posterior cingulate/precuneus, and left anterior insula- for the first equation. intraoccipital sulcus and thalamus- for the second (familiarity) equation.
Nitschke et al. 2004 / [18] / 6 mothers (children 4-6months old) / own infant Vs unknown infant pictures / Own>Unknown: bilateral cuneus precuneus, fusiform g., cerebellum, OFC.
Ranote et al. 2004 / [19] / 10 mothers (4-8 months) / own Vs unknown infant and control videos / Infant>Control: bilateral cerbellum, MO g.,left MT g., ST g., postcentral. Own>Unknown: R anterior TP, R MO g., and L amygdala.
Strathearn et al. 2008 / [20] / 28 mothers (children 11 month old) / own Vs unknown infant faces (sad, happy and neutral) / Own>Unknown: medial prefrontal, anterior cingulate, insula cortex, dorsolateral prefrontal cortex, primary motor area, ventral striatum, head of caudate, putamen, VTA, substantia nigra, inferior, middle, and superior temporal gyri (including the fusiform gyrus and temporal pole), the lateral amygdala, thalamic nuclei, and hypothalamus. Happy- Own>Unknown: bilateral putamen, left substantia nigra region, right thalamus, and left lateral superior amygdala.
Kringelbach et al. 2008 / [21] / 12 non-parents-5 male/7 female / MEG study: happy, neutral and sad faces of infant and adult / Infant>Adult:madial orbitofrontal cortex, in 12-20Hz after 165ms post-stimulus
Noriuchi, Kikuchi & Senoo, 2008 / [22] / 13 mothers (children 1.5 year old) / own Vs unknown-separation & play videos / intensity of feelings during watching the videos(joy, anxiety, love, excitement) / Own>Unknown: orbitofrontal cortices, inferior frontal gyrus ,dorsomedial prefrontal cortex , middle frontal gyrus, middle temporal gyrus , anterior insula,R hypothalamus, L precentral gyrus, posterior cingulate gyrus, putamen, thalamus, and periaqueductal gray . Own<Unknown: bilateral postcentral gyrus,putamen ,R frontal pole, superior temporal gyrus (STG),L inferior parietal lobule (IPL), precuneus, fusiform gyrus, and parahippocampal gyrus. Separation-Own>Unknown: bilateral MFG, superior frontal gyrus (SFG), angular gyrus, posterior cingulate gyrus, R OFC, MTG, precuneus, fusiform gyrus, and putamen and DMPFC. Play Own>Unknown: R MFG, inferior temporal gyrus, MTG, STG, inferior occipital gyrus, and hypothalamus and left putamen. Own Separation>Play: bilateral SFG, DMPFC, MFG, STS, STG, IPL, precuneus , R IFG, MTG, anterior cingulate gyrus, posterior cingulate gyru, L OFC, precentral gyrus, ITG,superior parietal lobule (SPL), angular gyrus, cuneus, thalamus, caudate nucleus, and substantia nigra. Own Separation<Play: right MTG,L precentral gyrus, cuneus, supramarginal gyrus, and hypothalamus. Own>Unknown-Joy correlation: left OFC. Own>Unknown-Anxious correlation: right OFC. Own Separation>Play- Love correlation: left STS. Own Separation>Play- Excitement correlation: right STS.
Glocker et al. 2009 / [23] / 16 non-parent women / infant Vs Adult faces / baby schema / Infant>Adult: fusiform gyrus, thalamus, cingulate gyrus, insula, and orbitofrontal cortex. Baby Schema correlation: right nucleus accumbens , left anterior cingulate cortex ,left precuneus, and left fusiform gyrus.
Lenzi et al. 2009 / [24] / 16 mothers (children 6-12 months old) / own Vs unknown infant face expression ( joy, distress, ambiguous, neutral) / maternal reflective function via AAI / Emotional>Neutral: R vPMC, bilateral insula, amigdala, IPL, STS. Own>Unknown: bilateral vPMC, R IFG, R IPL, R STS, and R anterior insula. Joy- Own>Unknown: R temporal pole, ITG, MTG, STG, hippocampus, insula, fusiform gyrus, R thalamus, amygdala and basal ganglia bilaterally. Ambiguous-Own>Unknown: L anterior middle frontal gyrus , L presupplementary motor area, R anterior cingulum,and L precuneus. All Face>Rest- Reflectivefunction correlation: R anterior insula.
Strathearn et al. 2009 / [25] / 30 mothers (infants 11 month old) / own Vs unknown faces (sad, happy and neutral) / adult attachment classification via AAI and plasma OT / Happy-Own>unknown: substantia nigra, dorsal putamen, thalamic nuclei, striatum, caudate nuclei, insular cortex, superior temporal gyrus, and pre- and postcentral gyri. All- Own>unknown: mesocorticolimbic (ventral tegmental area and ventral striatum) and nigrostriatal pathway (substantia nigra and dorsal striatum). Secure>Insecure (own): lateral prefrontal cortex bilaterally, left mPFC and hypothalamus/pituitary region. Secure>Insecure (own happy): orbitofrontal cortex and mPFC bilaterally. Secure<Insecure (own happy): dlPFC. Secure>Insecure (own sad): right ventral striatum. Secure<Insecure (own sad): dlPFC. Own neutral- OT correlation: right ventral striatum
Moses-Kolko et al. 2010 / [26] / 30 mothers-14 PPD/16 healthy (12 weeks post-partum) / emotional face matching task / Edinburgh Postnatal Depression Scale scores and Parent-to-Infant Attachment Questionnaire scores / Face>Shape: bilateral amigdala. Shape>Face :left dorsomedial prefrontal cortex. Face- Healthy >Depressed: L dmPFC. Correlations for Depressed: Edinburgh Postnatal Depression Scale scores were negatively correlated with face-related left amygdala activity and less hostility toward the infant was associated with greater right amygdala activity. Connectivity-Healthy (face>shape): preceding connectivity from the left dorsomedial prefrontal cortex to the left amygdala reference region.
Atzil, Hendler & Feldman, 2011 / [27] / 28 mothers (children 4-6 months old) / own Vs unknown infant play/mother-infant interaction video / mother-infant synchrony and intrusiveness during interaction via CIB / Infant play-Own>Unknown: R IPL, R ITG, precentral gyrus, claustum, precuneus, caudate head, Nacc, medial FG, SFG, cingulate gyrus, L medial FG, postcentral gyrus, caudate body, infirior occipital gyrus, ventro-lateral thalamus, insula, supramarginal gyrus, and IPL. Synchronous>Intrusive (own>unknown): left NAcc . Synchronous<Intrusive (own>unknown): right amygdala. Synchronous: significantly higher left NAcc activations than right amygdala activations. Plasma oxytocin levels were significantly correlated with the left NAcc and right amygdala. Connectivity-seed region Nacc: Intrusive: higher correlations in occipital, lateral–frontal, temporal and cerebellar cortices. Synchronous: highercortical correlation in mPFC. Connectivity-seed region right amygdala: Intrusive: higher cortical correlation in mPFC, cingulate gyrus, superior temporal gyrus, and cerebellum. Synchronous: higher correlations in temporal, occipital, insular, lateral–frontal, and cerebellar cortices.