What’s in a smile? Maternal brain responses to infant facial cues

In the paper

“However, after contrasting “own” and “unknown” baby faces (ON>UN), no significant activation remained, even at lowered statistical thresholds (Figure 2C). Thus, there was no significant difference in posterior visual pathway response between the own and unknown baby face stimuli.”

In the paper

“As expected, face stimuli activated brain regions along the ventral visual pathway from the primary visual cortex to the temporal lobe, including the fusiform gyrus and the so-called “fusiform face area” (Figure 2A&B) (50).”

What the sources say

• Not checked yetcites [50] Haber SN, Fudge JL, McFarland NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci.2000;20(6):2369–2382 source

In the paper

“No brain region was significantly activated by infant “affect” as a main effect (F>15.66, df=2,54, using a random effects model, FDR corrected q<0.05), nor was an “identity x affect” interaction effect seen, with or without FDR correction.”

In the paper

“A significant difference was also seen between happy and neutral affect in one region, and between neutral and sad affect in another (both P<0.05).”

In the paper

“Smiling, but not neutral or sad, faces specifically activate nigrostriatal brain regions interconnected by dopaminergic neurons (51), with a graded response dependent on infant affect (happy>neutral>sad).”

What the sources say

• Not checked yetcites [51] Crittenden PM, Claussen AH. The Organization of Attachment Relationships: Maturation, Culture, and Context. Cambridge, United Kingdom: Cambridge University Press;2000

In the paper

“Five specific regions of activation were seen in the limbic area (with a cluster threshold of 100 mm3), and one in the midbrain (cluster threshold 30 mm3), including bilateral putamen, left substantia nigra region, right thalamus, and the left lateral superior amygdala (Table 3).”

In the paper

“As an example, in Figure 5 the left dorsal putamen and substantia nigra area, two key interconnecting dopaminergic brain regions, showed a significant fMRI-BOLD response to own-happy faces but much less to neutral faces, and no response difference was seen in the sad face contrast.”

In the paper

“In all six regions, there appeared to be a progressive decrease in the % signal change differences, across happy, neutral and sad affect (Figure 4).”

• Also stated in: § Results · plain

  “A region-of-interest analysis revealed that activation in these regions was related to positive infant affect (happy>neutral>sad) for each own-unknown baby face contrast.”

In the paper

“This was evident from the contrast between sad faces and baseline, which revealed widespread activation in response to both own and unknown sad baby faces, though with a similar pattern for each.”

In the paper

“In addition, most prior studies have had a small sample size (10 or fewer subjects) or used a suboptimal fixed effects analysis (24) which prevents generalization of the results to the population from which the sample was drawn (30).”

What the sources say

• Not checked yetcites [24] Swain JE, Lorberbaum JP, Kose S, Strathearn L. Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry.2007;48(3/4):262–287 source
• Not checked yetcites [30] Huettel SA, Song AW, McCarthy G. Functional Magnetic Resonance Imaging. Sunderland, MA: Sinauer Associates;2004

In the paper

“Using a facial affect coding scheme, based on Cole et al (34), these images were classified by a trained research assistant into one of five affect groups: very happy, happy, neutral, sad or very sad. Excellent inter-observer reliability was demonstrated, based on 466 double coded images (Pearson correlation coefficient 0.925, 2-tailed, P<0.001).”

What the sources say

• Not checked yetcites Cole et al (34)

In the paper

“Since the amygdala plays an important role in processing face affect (27), and its response may be modulated by dopamine (28;29), differences in baby face affect may have been a confounding factor.”

What the sources say

• Not checked yetcites [27] Fitzgerald DA, Angstadt M, Jelsone LM, Nathan PJ, Phan KL. Beyond threat: amygdala reactivity across multiple expressions of facial affect. Neuroimage.2006;30(4):1441–1448 source
• Not checked yetcites [28] Tessitore A, Hariri AR, Fera F, et al. Dopamine modulates the response of the human amygdala: a study in Parkinson's disease. J Neurosci.2002;22(20):9099–9103 source
• Not checked yetcites [29] Floresco SB, Tse MT. Dopaminergic regulation of inhibitory and excitatory transmission in the basolateral amygdala-prefrontal cortical pathway. J Neurosci.2007;27(8):2045–2057 source

In the paper

“In addition, the ability to link these sensory cues with the underlying needs of an infant, and differentially respond to such needs, is thought to be the basis for establishing secure mother-infant attachment (15–17).”

What the sources say

• Not checked yetcites [15] Murray L. The impact of postnatal depression on infant development. J Child Psychol Psychiatry.1992;33(3):543–561 source
• Not checked yetcites [16] Grienenberger JF, Kelly K, Slade A. Maternal reflective functioning, mother-infant affective communication, and infant attachment: exploring the link between mental states and observed caregiving behavior in the intergenerational transmission of attachment. Attach Hum Dev.2005;7(3):299–311 source
• Not checked yetcites [17] Bowlby J. Attachment and Loss.Vol 1. London, United Kingdom: Hogarth Press;1969

In the paper

“The amygdala, for example, is strongly activated in some studies (20;23), but deactivated in another (22).”

What the sources say

• Not checked yetcites [20] Ranote S, Elliott R, Abel KM, Mitchell R, Deakin JF, Appleby L. The neural basis of maternal responsiveness to infants: an fMRI study [published correction appears in Neuroreport. 2004;15(14):2303]. Neuroreport.2004;15(11):1825–1829 source
• Not checked yetcites [23] Leibenluft E, Gobbini MI, Harrison T, Haxby JV. Mothers’ neural activation in response to pictures of their children and other children [published correction appears in Biol Psychiatry. 2004;56(8):612]. Biol Psychiatry.2004;56(4):225–232 source
• Not checked yetcites [22] Bartels A, Zeki S. The neural correlates of maternal and romantic love. Neuroimage.2004;21(3):1155–1166 source

In the paper

“The false discovery rate (FDR) approach (44) was used to correct for multiple comparisons at a threshold of q<0.05, which accepts 5% of the discovered (supra-threshold) voxels as false positives.”

What the sources say

• Not checked yetcites [44] Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage.2002;15(4):870–878 source

In the paper

“In the random effects analysis, statistical maps were created for each individual subject before being subjected to a second level of statistical analysis, allowing generalization to the sample population of first-time mothers.”

In the paper

“Several studies have shown that the striatum, a key projection of midbrain dopamine neurons which includes the putamen and caudate head, is activated in response to face images of a mother’s own child compared to unknown (or familiar but unrelated) children (22;23), as well as to infant cry stimuli (18).”

What the sources say

• Not checked yetcites [22] Bartels A, Zeki S. The neural correlates of maternal and romantic love. Neuroimage.2004;21(3):1155–1166 source
• Not checked yetcites [23] Leibenluft E, Gobbini MI, Harrison T, Haxby JV. Mothers’ neural activation in response to pictures of their children and other children [published correction appears in Biol Psychiatry. 2004;56(8):612]. Biol Psychiatry.2004;56(4):225–232 source
• Not checked yetcites [18] Lorberbaum JP, Newman JD, Horwitz AR, et al. A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry.2002;51(6):431–445 source

In the paper

“Each subject baby was matched to a single control baby, with an equal number of face images from each affect group. Wherever possible, the two babies were also matched on age and race.”

In the paper

“One common theme emerging from these studies has been the possible role of the mesocorticolimbic dopamine system in processing reward-based signals and motivating maternal care, as seen in animal models (see review (24)).”

What the sources say

• Not checked yetcites [24] Swain JE, Lorberbaum JP, Kose S, Strathearn L. Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry.2007;48(3/4):262–287 source

In the paper

“The mothers did not observe the videotaping, to ensure that each baby face image was novel when presented during the subsequent scanning session.”

In the paper

“Similar activation patterns have been seen in response to pictures of romantic partners (22), beautiful faces (25) and sexual stimuli (26), suggesting a link between brain reward circuits and attachment.”

What the sources say

• Not checked yetcites [22] Bartels A, Zeki S. The neural correlates of maternal and romantic love. Neuroimage.2004;21(3):1155–1166 source
• Not checked yetcites [25] Aharon I, Etcoff N, Ariely D, Chabris CF, O'Connor E, Breiter HC. Beautiful faces have variable reward value: fMRI and behavioral evidence. Neuron.2001;32(3):537–551 source
• Not checked yetcites [26] Arnow BA, Desmond JE, Banner LL, et al. Brain activation and sexual arousal in healthy, heterosexual males. Brain.2002;125(pt 5):1014–1023 source

In the paper

“Slices were positioned 30 degrees to the anterior commissure / posterior commissure (ACPC) line in the axial plane, downward from posterior to anterior, which (along with a reduced TE and slice thickness) has been shown to optimize visualization of the orbitofrontal cortex (36).”

What the sources say

• Not checked yetcites [36] McClure SM, Laibson DI, Loewenstein G, Cohen JD. Separate neural systems value immediate and delayed monetary rewards. Science.2004;306(5695):503–507 source

In the paper

“Anatomical regions were confirmed using the automated “Talairach Daemon” (searching for “nearest gray matter”) (45), and manually, using a human brain atlas (46).”

What the sources say

• Not checked yetcites [45] Lancaster JL, Woldorff MG, Parsons LM, et al. Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp.2000;10(3):120–131 source
• Not checked yetcites [46] Mai JK, Assheuer J, Paxinos G. Atlas of the Human Brain. 2nd ed. San Diego, CA: Elsevier;2004

In the paper

“There were no significant differences in the timing of “own” and “unknown” baby face images (natural log of mean presentation times, paired samples t-test, t=−0.73, df=29, P=0.47), or in the OH>UH, ON>UN or OS>US comparisons (df=9; Happy: t=1.52, P=0.16; Neutral: t=0.72, P=0.49; Sad: t=−1.69, P=0.13).”

In the paper

“The protocol was approved by the Institutional Review Board at Baylor College of Medicine, Houston, Texas, and all subjects provided written informed consent.”

In the paper

“One subject had more than 2 mm translation (2.3 mm) during Run 1, and analyses were repeated before and after excluding this subject. A single subject also had unacceptable head motion during Run 2 (3.2 mm translation and 3.5 mm rotation), and was excluded from further analyses.”

In the paper

“Each striatal region is integrally connected to a corresponding region of the midbrain’s VTA and substantia nigra via ascending and descending dopaminergic neurons.”

What the sources say

• Not checked yetcites [51] Crittenden PM, Claussen AH. The Organization of Attachment Relationships: Maturation, Culture, and Context. Cambridge, United Kingdom: Cambridge University Press;2000

In the paper

“Thus, the striatum is believed to be an important relay station between the limbic and motor systems, integrating affective information from limbic regions with cognitive information from the prefrontal cortex, in shaping motor/behavioral responses.”

What the sources say

• Not checked yetcites [51] Crittenden PM, Claussen AH. The Organization of Attachment Relationships: Maturation, Culture, and Context. Cambridge, United Kingdom: Cambridge University Press;2000

In the paper

“In responding to infant social cues, whether positive or negative, mothers need to integrate both affective and cognitive information about their baby, and evaluate competing demands, before choosing the most appropriate behavioral response (52;53).”

What the sources say

• Not checked yetcites [52] Shafritz KM, Collins SH, Blumberg HP. The interaction of emotional and cognitive neural systems in emotionally guided response inhibition. Neuroimage.2006;31(1):468–475 source
• Not checked yetcites [53] Mirenowicz J, Schultz W. Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature.1996;379(6564):449–451 source

In the paper

“In rat dams, extracellular dopamine release in the ventral striatum is associated with an increase in maternal behaviors, with the dopamine signal preceding the onset of the behavior (57).”

What the sources say

• Not checked yetcites [57] Milner JS, Halsey LB, Fultz J. Empathic responsiveness and affective reactivity to infant stimuli in high- and low-risk for physical child abuse mothers. Child Abuse Negl.1995;19(6):767–780 source

In the paper

“In primates, Haber et al (51) demonstrated important anatomical feed-forward loops between the striatum and the VTA / substantia nigra region, suggesting that these striatonigrostriatal circuits funnel information between ventromedial (limbic), central (associative) and dorsolateral (motor) striatal regions (Figure 6).”

What the sources say

• Not checked yetcites [51] Crittenden PM, Claussen AH. The Organization of Attachment Relationships: Maturation, Culture, and Context. Cambridge, United Kingdom: Cambridge University Press;2000

In the paper

“Likewise, there are corresponding connections between the striatum and the forebrain, including those involved in emotion processing (medial prefrontal, anterior cingulate, insula), cognition (dorsolateral prefrontal) and motor/behavioral outputs (primary motor area) (51).”

What the sources say

• Not checked yetcites [51] Crittenden PM, Claussen AH. The Organization of Attachment Relationships: Maturation, Culture, and Context. Cambridge, United Kingdom: Cambridge University Press;2000

In the paper

“Dopaminergic reward-related brain regions are activated specifically in response to happy, but not sad, baby faces.”

In the paper

“Although functional MRI only measures blood-oxygen level dependent changes in brain activity, together these studies suggest that positive sensory cues from infants, such as a smiling facial expression, may stimulate dopamine release in the striatum, and promote responsive maternal care.”

What the sources say

• Not checked yetcites [56] Champagne FA, Chretien P, Stevenson CW, Zhang TY, Gratton A, Meaney MJ. Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J Neurosci.2004;24(17):4113–4123 source
• Not checked yetcites [57] Milner JS, Halsey LB, Fultz J. Empathic responsiveness and affective reactivity to infant stimuli in high- and low-risk for physical child abuse mothers. Child Abuse Negl.1995;19(6):767–780 source

In the paper

“One limitation of this study is that the mothers were scanned at varying times post-partum (between 7 and 17 months), viewing baby faces ranging from 5 to 10 months in age (Table 1).”

In the paper

“For example, the difference in response between own and unknown happy faces in these dopamine-associated regions may be an index of the reward value or salience of the infant’s face to the mother, which may in turn relate to maternal sensitivity or child neglect.”

In the paper

“While individual variation seen within this population (such as breastfeeding duration, mother-infant separation, and psychopathology risk) is another limitation in interpreting study findings, it also presents an opportunity for further research into the significance of these individual differences.”

In the paper

“Although there is no published fMRI data on the question, mothers may respond differently to their infant at differing ages, which may have influenced our results.”

In the paper

“However, other fMRI studies have only demonstrated activation of these areas in mothers of younger babies, during the first few months of life (18, 24), suggesting that these regions may be more important during the early postpartum period.”

What the sources say

• Not checked yetcites [18] Lorberbaum JP, Newman JD, Horwitz AR, et al. A potential role for thalamocingulate circuitry in human maternal behavior. Biol Psychiatry.2002;51(6):431–445 source
• Not checked yetcites [24] Swain JE, Lorberbaum JP, Kose S, Strathearn L. Brain basis of early parent-infant interactions: psychology, physiology, and in vivo functional neuroimaging studies. J Child Psychol Psychiatry.2007;48(3/4):262–287 source

In the paper

“However, it is possible that differences in timing of the two conditions could have biased the results, with earlier images expected to produce a stronger hemodynamic response.”