The impact of depression on mothers’ neural processing of their adolescents’ affective behavior

Depression affects neural processing of emotional stimuli and could, therefore, impact parent–child interactions. However, the neural processes with which mothers with depression process their adolescents’ affective interpersonal signals and how this relates to mothers’ parenting behavior are poorly understood. Mothers with and without depression (N = 64 and N = 51, respectively; M_age = 40 years) from low-income families completed an interaction task with their adolescents (M_age = 12.8 years), which was coded for both individuals’ aggressive, dysphoric, positive and neutral affective behavior. While undergoing fMRI, mothers viewed video clips from this task of affective behavior from their own and an unfamiliar adolescent. Relative to non-depressed mothers, those with depression showed more aggressive and less positive affective behavior during the interaction task and more activation in the bilateral insula, superior temporal gyrus and striatum but less in the lateral prefrontal cortex while viewing aggressive and neutral affect. Findings were comparable for own and unfamiliar adolescents’ affect. Heightened limbic, striatal and sensory responses were associated with more aggressive and dysphoric parenting behavior during the interactions, while reduced lateral prefrontal activation was associated with less positive parenting behavior. These results highlight the importance of depressed mothers’ affective information processing for understanding mothers’ behavior during interactions with their adolescents.     

Maternal dopamine encodes affective signals of human infants

Mothers are highly responsive to their offspring. In non-human mammals, mothers secrete dopamine in the nucleus accumbens (NAcc) in response to their pups. Yet, it is still unknown which aspect of the offspring behavior elicits dopaminergic responses in mothers. Here, we tested whether infants’ affective signals elicit dopaminergic responses in the NAcc of human mothers. First, we conducted a behavioral analysis on videos of infants’ free play and quantified the affective signals infants spontaneously communicated. Then, we presented the same videos to mothers during a magnetic resonance-positron emission tomography scan. We traced the binding of [¹¹C]raclopride to free D_2/3-type receptors to assess maternal dopaminergic responses during the infant videos. When mothers observed videos with many infant signals during the scan, they had less [¹¹C]raclopride binding in the right NAcc. Less [¹¹C]raclopride binding indicates that less D_2/3 receptors were free, possibly due to increased endogenous dopamine responses to infants’ affective signals. We conclude that NAcc D_2/3 receptors are involved in maternal responsiveness to affective signals of human infants. D_2/3 receptors have been associated with maternal responsiveness in nonhuman animals. This evidence supports a similar mechanism in humans and specifies infant-behaviors that activate the maternal dopaminergic system, with implications for social neuroscience, development and psychopathology.     

Infant brain response to affective and discriminative touch: A longitudinal study using fNIRS

ABSTRACT

The affective-motivational component of touch has been shown to consistently activate the social- brain network in children, adolescents and adults, including the posterior superior temporal sulcus (pSTS). However, very little is known about the neural mechanisms of affective touch processing during the first year of life. The objective of the present study was to analyze brain response to affective and discriminative touch in a sample of seven-month-old infants (N = 35) who were followed longitudinally at 12 months of age (N = 25). Infants were given affective and discriminative touch to the bare forearm while their brain response was recorded using functional near-spectroscopy (fNIRS). Seven-month-olds presented brain activation for affective and discriminative stimuli in channels placed over the somatosensory region, but no activation was recorded in channels placed in the temporal region for affective touch. At 12 months of age, infants presented a significant increase in hemodynamic activity in channels placed over the temporal region for affective touch, compared to seven-month-olds. Our study presents evidence of a developmental trajectory for distinct aspects of touch brain processing in the first year of life, with the recruitment of the temporal region for the affective component of touch, maturing in the second semester of life.     

Neural representation of the parent–child attachment from infancy to adulthood

Attachment theory is built on the assumption of consistency; the mother–infant bond is thought to underpin the life-long representations individuals construct of attachment relationships. Still, consistency in the individual’s neural response to attachment-related stimuli representing his or her entire relational history has not been investigated. Mothers and children were followed across two decades and videotaped in infancy (3–6 months), childhood (9–12 years) and young adulthood (18–24 years). In adulthood, participants underwent functional magnetic resonance imaging while exposed to videos of own mother–child interactions (Self) vs unfamiliar interactions (Other). Self-stimuli elicited greater activations across preregistered nodes of the human attachment network, including thalamus-to-brainstem, amygdala, hippocampus, anterior cingulate cortex (ACC), insula and temporal cortex. Critically, self-stimuli were age-invariant in most regions of interest despite large variability in social behavior, and Bayesian analysis showed strong evidence for lack of age-related differences. Psycho–physiological interaction analysis indicated that self-stimuli elicited tighter connectivity between ACC and anterior insula, consolidating an interface associating information from exteroceptive and interceptive sources to sustain attachment representations. Child social engagement behavior was individually stable from infancy to adulthood and linked with greater ACC and insula response to self-stimuli. Findings demonstrate overlap in circuits sustaining parental and child attachment and accord with perspectives on the continuity of attachment across human development.     

Gentle stroking elicits somatosensory ERP that differentiates between hairy and glabrous skin

Here we asked whether, similar to visual and auditory event-related potentials (ERPs), somatosensory ERPs reflect affect. Participants were stroked on hairy or glabrous skin at five stroking velocities (0.5, 1, 3, 10 and 20 cm/s). For stroking of hairy skin, pleasantness ratings related to velocity in an inverted u-shaped manner. ERPs showed a negativity at 400 ms following touch onset over somatosensory cortex contra-lateral to the stimulation site. This negativity, referred to as sN400, was larger for intermediate than for faster and slower velocities and positively predicted pleasantness ratings. For stroking of glabrous skin, pleasantness showed again an inverted u-shaped relation with velocity and, additionally, increased linearly with faster stroking. The sN400 revealed no quadratic effect and instead was larger for faster velocities. Its amplitude failed to significantly predict pleasantness. In sum, as was reported for other senses, a touch’s affective value modulates the somatosensory ERP. Notably, however, this ERP and associated subjective pleasantness dissociate between hairy and glabrous skin underscoring functional differences between the skin with which we typically receive touch and the skin with which we typically reach out to touch.     

ALE meta‐analysis reveals dissociable networks for affective and discriminative aspects of touch

Emotionally‐laden tactile stimulation—such as a caress on the skin or the feel of velvet—may represent a functionally distinct domain of touch, underpinned by specific cortical pathways. In order to determine whether, and to what extent, cortical functional neuroanatomy supports a distinction between affective and discriminative touch, an activation likelihood estimate (ALE) meta‐analysis was performed. This meta‐analysis statistically mapped reported functional magnetic resonance imaging (fMRI) activations from 17 published affective touch studies in which tactile stimulation was associated with positive subjective evaluation (n = 291, 34 experimental contrasts). A separate ALE meta‐analysis mapped regions most likely to be activated by tactile stimulation during detection and discrimination tasks (n = 1,075, 91 experimental contrasts). These meta‐analyses revealed dissociable regions for affective and discriminative touch, with posterior insula (PI) more likely to be activated for affective touch, and primary somatosensory cortices (SI) more likely to be activated for discriminative touch. Secondary somatosensory cortex had a high likelihood of engagement by both affective and discriminative touch. Further, meta‐analytic connectivity (MCAM) analyses investigated network‐level co‐activation likelihoods independent of task or stimulus, across a range of domains and paradigms. Affective‐related PI and discriminative‐related SI regions co‐activated with different networks, implicated in dissociable functions, but sharing somatosensory co‐activations. Taken together, these meta‐analytic findings suggest that affective and discriminative touch are dissociable both on the regional and network levels. However, their degree of shared activation likelihood in somatosensory cortices indicates that this dissociation reflects functional biases within tactile processing networks, rather than functionally and anatomically distinct pathways. Hum Brain Mapp 37:1308‐1320, 2016. © 2016 Wiley Periodicals, Inc.     

Early maternal care and amygdala habituation to emotional stimuli in adulthood

Evidence suggests that maternal care constitutes a protective factor for psychopathology which may be conditional on the level of family adversity. Given that psychopathology is frequently linked with social deficits and the amygdala with social functioning, we investigated the impact of early maternal care on amygdala function under high vs low familial risk for psychopathology. Amygdala activity and habituation during an emotional face-matching paradigm was analyzed in participants of an epidemiological cohort study followed since birth (n = 172, 25 years). Early mother–infant interaction was assessed during a standardized nursing and play setting at the age of 3 months. Information on familial risk during the offspring’s childhood and on the participants’ lifetime psychopathology was obtained with diagnostic interviews. An interaction between maternal stimulation and familial risk was found on amygdala habituation but not on activation, with higher maternal stimulation predicting stronger amygdala habituation in the familial risk group only. Furthermore, amygdala habituation correlated inversely with Attention Deficit Hyperactivity Disorder (ADHD) diagnoses. The findings underline the long-term importance of early maternal care on the offspring’s socioemotional neurodevelopment and of interventions targeting maternal sensitivity early in life, particularly by increasing maternal interactive behavior in those with familial risk.     

Reported maternal childhood maltreatment experiences,amygdala activation and functional connectivity to infant cry

Maternal childhood maltreatment experiences (CMEs) may influence responses to infants and affect child outcomes. We examined associations between CME and mothers’ neural responses and functional connectivity to infant distress. We hypothesized that mothers with greater CME would exhibit higher amygdala reactivity and amygdala–supplementary motor area (SMA) functional connectivity to own infant’s cries. Postpartum mothers (N = 57) assessed for CME completed an functional magnetic resonance imaging task with cry and white-noise stimuli. Amygdala region-of-interest and psychophysiological interaction analyses were performed. Our models tested associations of CME with activation and connectivity during task conditions (own/other and cry/noise). Exploratory analyses with parenting behaviors were performed. Mothers with higher CME exhibited higher amygdala activation to own baby’s cries vs other stimuli (F_1,392 = 6.9, P < 0.01, N = 57) and higher differential connectivity to cry vs noise between amygdala and SMA (F_1,165 = 22.3, P < 0.001). Exploratory analyses revealed positive associations between both amygdala activation and connectivity and maternal non-intrusiveness (Ps < 0.05). Increased amygdala activation to own infant’s cry and higher amygdala–SMA functional connectivity suggest motor responses to baby’s distress. These findings were associated with less intrusive maternal behaviors. Follow-up studies might replicate these findings, add more granular parenting assessments and explore how cue processing leads to a motivated maternal approach in clinical populations.     

Functional white-laser imaging to study brain oxygen uncoupling/recoupling in songbirds

Contrary to the intense debate about brain oxygen dynamics and its uncoupling in mammals, very little is known in birds. In zebra finches, picosecond optical tomography with a white laser and a streak camera can measure in vivo oxyhemoglobin (HbO₂) and deoxyhemoglobin (Hb) concentration changes following physiologic stimulation (familiar calls and songs). Picosecond optical tomography showed sufficient submicromolar sensitivity to resolve the fast changes in the hippocampus and auditory forebrain areas with 250 μm resolution. The time course is composed of (1) an early 2-second-long event with a significant decrease in Hb and HbO₂ levels of −0.7 and −0.9 μmol/L, respectively, (2) a subsequent increase in blood oxygen availability with a plateau of HbO₂ (+0.3 μmol/L), and (3) pronounced vasodilatation events immediately after the end of the stimulus. One of the findings of our study is the direct link between blood oxygen level-dependent signals previously published in birds and our results. Furthermore, the early vasoconstriction event and poststimulus ringing seem to be more pronounced in birds than in mammals. These results in birds, tachymetabolic vertebrates with a long lifespan, can potentially yield new insights, e.g., into brain aging.     

Stages of neuronal morphological development in vitro--an automated assay

The present work addresses the simultaneous monitoring of hemoglobin and glucose consumption in rat somatosensory cortex in vivo. We propose a method which combines two techniques: 2-dimensional optical imaging and an amperometric microbiosensor. The mounted setup optimizes the space in the cranial window so that three micro-electrodes can be inserted: glucose microbiosensor, sentinel and stimulating electrode as well as the holder to manipulate the optical fiber. Additionally, a tool based on graphical user interface programming has been developed to visualize a two-dimension spectral map of oxy-, deoxy- and total hemoglobin, HbO₂, HbR and HbT respectively, in the cortex. Our results showed a good sensitivity, selectivity and spatial resolution for both methods. Relevant hemodynamic responses had a common central focus (at the site of the stimulus) which later segregated to other vascular compartments. A good linear relationship between extracellular glucose concentration and HbO₂ values during brain activation after local electrical stimulation was observed for electrochemical and optical recordings (R² values were over 0.94). Time courses between glucose and HbO₂ signals showed a temporal delay ranging from 1 s to 2 s, suggesting that both variables are not always coupled. The temporal mismatching reported here, provides in vivo evidence that supports a neuronal hypothesis: cerebral blow flow and oxidative metabolism are driven in parallel by neural activity - rather than a concatenation of events (‘in-series’ events) occurring at sites of neuronal activation.     

Neurocognitive processing of infant stimuli in mothers and non-mothers: psychophysiological,cognitive and neuroimaging evidence

Emerging evidence indicates that mothers and non-mothers show different neurocognitive responses to infant stimuli. This study investigated mothers’ psychophysiological, cognitive and neuronal responses to emotional infant stimuli. A total of 35 mothers with 4-month-old infants and 18 control women without young children underwent computerized tests assessing neurocognitive processing of infant stimuli. Their eye gazes and eye fixations, galvanic skin responses (GSRs) and facial expressions towards infant emotional stimuli were recorded during the tasks. Participants underwent functional magnetic resonance imaging during which they viewed pictures of an unknown infant and, for mothers, their own infants. Mothers gazed more and had increased GSR towards infant stimuli and displayed more positive facial expressions to infant laughter, and self-reported more positive ratings of infant vocalizations than control women. At a neural level, mothers showed greater neural response in insula, dorsolateral prefrontal cortex and occipital brain regions within a predefined ‘maternal neural network’ while watching images of their own vs unknown infants. This specific neural response to own infants correlated with less negative ratings of own vs unknown infants’ signals of distress. Differences between mothers and control women without young children could be interpreted as neurocognitive adaptation to motherhood in the mothers.     

The brain basis of social synchrony

As a social species, humans evolved to detect information from the social behavior of others. Yet, the mechanisms used to evaluate social interactions, the brain networks implicated in such recognition, and whether individual differences in own social behavior determine response to similar behavior in others remain unknown. Here we examined social synchrony as a potentially important mechanism in the evaluation of social behavior and utilized the parenting context, an evolutionarily salient setting of significant consequences for infant survival, to test this issue. The brain response of healthy postpartum mothers to three mother–infant interaction vignettes was assessed. Videos included a typical synchronous interaction and two pathological interactions of mothers diagnosed with postpartum depression and anxiety that showed marked deviations from social synchrony. Mothers’ own interactions with their 4- to 6-month-old infants were videotaped and micro-coded for synchrony. Results indicated that the recognition of social synchrony involved activations in the dorsal anterior cingulate cortex (dACC), fusiform, cuneus, inferior parietal lobule, supplementary motor area and NAcc. Mother’s own synchrony with her infant correlated with her dACC response to synchrony in others. Findings are consistent with models suggesting that social action underpins social recognition and highlight social synchrony and the mother–infant bond as one prototypical context for studying the brain basis of social understanding.     

Cognitive influences on the affective representation of touch and the sight of touch in the human brain

We show that the affective experience of touch and the sight of touch can be modulated by cognition, and investigate in an fMRI study where top-down cognitive modulations of bottom-up somatosensory and visual processing of touch and its affective value occur in the human brain. The cognitive modulation was produced by word labels, ‘Rich moisturizing cream’ or ‘Basic cream’, while cream was being applied to the forearm, or was seen being applied to a forearm. The subjective pleasantness and richness were modulated by the word labels, as were the fMRI activations to touch in parietal cortex area 7, the insula and ventral striatum. The cognitive labels influenced the activations to the sight of touch and also the correlations with pleasantness in the pregenual cingulate/orbitofrontal cortex and ventral striatum. Further evidence of how the orbitofrontal cortex is involved in affective aspects of touch was that touch to the forearm [which has C fiber Touch (CT) afferents sensitive to light touch] compared with touch to the glabrous skin of the hand (which does not) revealed activation in the mid-orbitofrontal cortex. This is of interest as previous studies have suggested that the CT system is important in affiliative caress-like touch between individuals.     

Cerebral hemodynamic and ventilatory responses to hypoxia,hypercapnia, and hypocapnia during 5 days at 4,350?m

This study investigated the changes in cerebral near-infrared spectroscopy (NIRS) signals, cerebrovascular and ventilatory responses to hypoxia and CO₂ during altitude exposure. At sea level (SL), after 24 hours and 5 days at 4,350 m, 11 healthy subjects were exposed to normoxia, isocapnic hypoxia, hypercapnia, and hypocapnia. The following parameters were measured: prefrontal tissue oxygenation index (TOI), oxy- (HbO₂), deoxy- and total hemoglobin (HbTot) concentrations with NIRS, blood velocity in the middle cerebral artery (MCAv) with transcranial Doppler and ventilation. Smaller prefrontal deoxygenation and larger ΔHbTot in response to hypoxia were observed at altitude compared with SL (day 5: ΔHbO₂−0.6±1.1 versus −1.8±1.3 μmol/cmper mm Hg and ΔHbTot 1.4±1.3 versus 0.7±1.1 μmol/cm per mm Hg). The hypoxic MCAv and ventilatory responses were enhanced at altitude. Prefrontal oxygenation increased less in response to hypercapnia at altitude compared with SL (day 5: ΔTOI 0.3±0.2 versus 0.5±0.3% mm Hg). The hypercapnic MCAv and ventilatory responses were decreased and increased, respectively, at altitude. Hemodynamic responses to hypocapnia did not change at altitude. Short-term altitude exposure improves cerebral oxygenation in response to hypoxia but decreases it during hypercapnia. Although these changes may be relevant for conditions such as exercise or sleep at altitude, they were not associated with symptoms of acute mountain sickness.     

Cerebral metabolic rate of oxygen during transition from wakefulness to sleep measured with high temporal resolution OxFlow MRI with concurrent EEG

During slow-wave sleep, synaptic transmissions are reduced with a concomitant reduction in brain energy consumption. We used 3 Tesla MRI to noninvasively quantify changes in the cerebral metabolic rate of O₂ (CMRO₂) during wakefulness and sleep, leveraging the ‘OxFlow’ method, which provides venous O₂ saturation (SvO₂) along with cerebral blood flow (CBF). Twelve healthy subjects (31.3 ± 5.6 years, eight males) underwent 45–60 min of continuous scanning during wakefulness and sleep, yielding one image set every 3.4 s. Concurrent electroencephalography (EEG) data were available in eight subjects. Mean values of the metabolic parameters measured during wakefulness were stable, with coefficients of variation below 7% (average values: CMRO₂ = 118 ± 12 µmol O₂/min/100 g, SvO₂ = 67.0 ± 3.7% HbO₂, CBF = 50.6 ±4.3 ml/min/100 g). During sleep, on average, CMRO₂ decreased 21% (range: 14%–32%; average nadir = 98 ± 16 µmol O₂/min/100 g), while EEG slow-wave activity, expressed in terms of δ-power, increased commensurately. Following sleep onset, CMRO₂ was found to correlate negatively with relative δ-power (r = −0.6 to −0.8, P < 0.005), and positively with heart rate (r = 0.5 to 0.8, P < 0.0005). The data demonstrate that OxFlow MRI can noninvasively measure dynamic changes in cerebral metabolism associated with sleep, which should open new opportunities to study sleep physiology in health and disease.     

Vicarious praise and pain: parental neural responses to social feedback about their adolescent child

Social feedback, such as praise or critique, profoundly impacts our mood and social interactions. It is unknown, however, how parents experience praise and critique about their child and whether their mood and neural responses to such ‘vicarious’ social feedback are modulated by parents’ perceptions of their child. Parents (n = 60) received positive, intermediate and negative feedback words (i.e. personality characteristics) about their adolescent child during a magnetic resonance imaging scan. After each word, parents indicated their mood. After positive feedback their mood improved and activity in ventromedial prefrontal cortex and posterior cingulate cortex/precuneus increased. Negative feedback worsened parents’ mood, especially when perceived as inapplicable to their child, and increased activity in anterior cingulate cortex, anterior insula, dorsomedial prefrontal cortex and precuneus. Parents who generally viewed their child more positively showed amplified mood responses to both positive and negative feedback and increased activity in dorsal striatum, inferior frontal gyrus and insula in response to negative feedback. These findings suggest that vicarious feedback has similar effects and engages similar brain regions as observed during feedback about the self and illustrates this is dependent on parents’ beliefs of their child’s qualities and flaws. Potential implications for parent–child dynamics and children’s own self-views are discussed.     

Regional hyperperfusion in older adults with objectively-defined subtle cognitive decline

Although cerebral blood flow (CBF) alterations are associated with Alzheimer’s disease (AD), CBF patterns across prodromal stages of AD remain unclear. Therefore, we investigated patterns of regional CBF in 162 Alzheimer’s Disease Neuroimaging Initiative participants characterized as cognitively unimpaired (CU; n = 80), objectively-defined subtle cognitive decline (Obj-SCD; n = 31), or mild cognitive impairment (MCI; n = 51). Arterial spin labeling MRI quantified regional CBF in a priori regions of interest: hippocampus, inferior temporal gyrus, inferior parietal lobe, medial orbitofrontal cortex, and rostral middle frontal gyrus. Obj-SCD participants had increased hippocampal and inferior parietal CBF relative to CU and MCI participants and increased inferior temporal CBF relative to MCI participants. CU and MCI groups did not differ in hippocampal or inferior parietal CBF, but CU participants had increased inferior temporal CBF relative to MCI participants. There were no CBF group differences in the two frontal regions. Thus, we found an inverted-U pattern of CBF signal across prodromal AD stages in regions susceptible to early AD pathology. Hippocampal and inferior parietal hyperperfusion in Obj-SCD may reflect early neurovascular dysregulation, whereby higher CBF is needed to maintain cognitive functioning relative to MCI participants, yet is also reflective of early cognitive inefficiencies that distinguish Obj-SCD from CU participants.     

Teacher–student neural coupling during teaching and learning

Human communication is remarkably versatile, enabling teachers to share highly abstracted and novel information with their students. What neural processes enable such transfer of information across brains during naturalistic teaching and learning? Here, a teacher was scanned in functional magnetic resonance imaging while giving an oral lecture with slides on a scientific topic followed by a review lecture. Students were then scanned while watching either the intact Lecture and Review (N = 20) or a temporally scrambled version of the lecture (N = 20). Using intersubject correlation, we observed widespread Teacher–Student neural coupling spanning sensory cortex and language regions along the superior temporal sulcus as well as higher-level regions including posterior medial cortex (PMC), superior parietal lobule, and dorsolateral and dorsomedial prefrontal cortex. Teacher–student alignment in higher-level areas was not observed when learning was disrupted by temporally scrambling the lecture. Moreover, teacher–student coupling in PMC was significantly correlated with learning: the more closely the student’s brain mirrored the teacher’s brain, the more the student improved their learning score. Together, these results suggest that the alignment of neural responses between teacher and students may reflect effective communication of complex information across brains in classroom settings.     

Maternal mindfulness and anxiety during pregnancy affect infants’ neural responses to sounds

Maternal anxiety during pregnancy has been consistently shown to negatively affect offspring neurodevelopmental outcomes. However, little is known about the impact of positive maternal traits/states during pregnancy on the offspring. The present study was aimed at investigating the effects of the mother’s mindfulness and anxiety during pregnancy on the infant’s neurocognitive functioning at 9 months of age. Mothers reported mindfulness using the Freiburg Mindfulness Inventory and anxiety using the Symptom Checklist (SCL-90) at ±20.7 weeks of gestation. Event-related brain potentials (ERPs) were measured from 79 infants in an auditory oddball paradigm designed to measure auditory attention—a key aspect of early neurocognitive functioning. For the ERP responses elicited by standard sounds, higher maternal mindfulness was associated with lower N250 amplitudes (P < 0.01, η² = 0.097), whereas higher maternal anxiety was associated with higher N250 amplitudes (P < 0.05, η² = 0.057). Maternal mindfulness was also positively associated with the P150 amplitudes (P < 0.01, η² = 0.130). These results suggest that infants prenatally exposed to higher levels of maternal mindfulness devote fewer attentional resources to frequently occurring irrelevant sounds. The results show that positive traits and experiences of the mother during pregnancy may also affect the unborn child. Emphasizing the beneficial effects of a positive psychological state during pregnancy may promote healthy behavior in pregnant women.