Maternal prenatal depressive symptoms and child brain responses to affective touch at two years of age.

BACKGROUND: Touch is an essential form of mother-child interaction, instigating better social bonding and emotional stability. METHODS: We used diffuse optical tomography to explore the relationship between total haemoglobin (HbT) responses to affective touch in the child's brain at two years of age and maternal self-reported prenatal depressive symptoms (EPDS). Affective touch was implemented via slow brushing of the child's right forearm at 3 cm/s and non-affective touch via fast brushing at 30 cm/s and HbT responses were recorded on the left hemisphere. RESULTS: We discovered a cluster in the postcentral gyrus exhibiting a negative correlation (Pearson's r = -0.84, p = 0.015 corrected for multiple comparisons) between child HbT response to affective touch and EPDS at gestational week 34. Based on region of interest (ROI) analysis, we found negative correlations between child responses to affective touch and maternal prenatal EPDS at gestational week 14 in the precentral gyrus, Rolandic operculum and secondary somatosensory cortex. The responses to non-affective touch did not correlate with EPDS in these regions. LIMITATIONS: The number of mother-child dyads was 16. However, by utilising high-density optode arrangements, individualised anatomical models, and video and accelerometry to monitor movement, we were able to minimize methodological sources of variability in the data. CONCLUSIONS: The results show that maternal depressive symptoms during pregnancy may be associated with reduced child responses to affective touch in the temporoparietal cortex. Responses to affective touch may be considered as potential biomarkers for psychosocial development in children. Early identification of and intervention in maternal depression may be important already during early pregnancy.

Imaging affective and non-affective touch processing in two-year-old children.

Touch is an important component of early parent-child interaction and plays a critical role in the socio-emotional development of children. However, there are limited studies on touch processing amongst children in the age range from one to three years. The present study used frequency-domain diffuse optical tomography (DOT) to investigate the processing of affective and non-affective touch over left frontotemporal brain areas contralateral to the stimulated forearm in two-year-old children. Affective touch was administered by a single stroke with a soft brush over the child's right dorsal forearm at 3 cm/s, while non-affective touch was provided by multiple brush strokes at 30 cm/s. We found that in the insula, the total haemoglobin (HbT) response to slow brushing was significantly greater than the response to fast brushing (slow > fast). Additionally, a region in the postcentral gyrus, Rolandic operculum and superior temporal gyrus exhibited greater response to fast brushing than slow brushing (fast > slow). These findings confirm that an adult-like pattern of haemodynamic responses to affective and non-affective touch can be recorded in two-year-old subjects using DOT. To improve the accuracy of modelling light transport in the two-year-old subjects, we used a published age-appropriate atlas and deformed it to match the exterior shape of each subject's head. We estimated the combined scalp and skull, and grey matter (GM) optical properties by fitting simulated data to calibrated and coupling error corrected phase and amplitude measurements. By utilizing a two-compartment cerebrospinal fluid (CSF) model, the accuracy of estimation of GM optical properties and the localization of activation in the insula was improved. The techniques presented in this paper can be used to study neural development of children at different ages and illustrate that the technology is well-tolerated by most two-year-old children and not excessively sensitive to subject movement. The study points the way towards exciting possibilities in functional imaging of deeper functional areas near sulci in small children.

Relationship between maternal pregnancy-related anxiety and infant brain responses to emotional speech - a pilot study.

BACKGROUND: Maternal pregnancy-related anxiety (PRA) is reportedly related to neurodevelopmental outcomes of infants. However, the relationship between maternal PRA and the processing of emotions in the infant brain has not been extensively studied with neuroimaging. The objective of the present pilot study is to investigate the relationship between maternal PRA and infant hemodynamic responses to emotional speech at two months of age. METHODS: The study sample included 19 mother-infant dyads from a general sample of a population of Caucasian mothers. Self-reported Pregnancy-Related Anxiety Questionnaire (PRAQ-R2) data was collected from mothers during pregnancy at gestational weeks (gwks) 24 (N = 19) and 34 (N = 18). When their infants were two months old, the infants' brains functional responses to emotional speech in the left fronto-temporoparietal cortex were recorded using diffuse optical tomography (DOT). RESULTS: Maternal PRAQ-R2 scores at gwk 24 correlated negatively with the total hemoglobin (HbT) responses to sad speech on both sides of the temporoparietal junction (Spearman's rank correlation coefficient ρ = -0.87). The correlation was significantly greater at gwk 24 than gwk 34 (ρ = -0.42). LIMITATIONS: The field of view of the measurement did not include the right hemisphere or parts of the frontal cortex. The sample size is moderate and the mothers were relatively highly educated, thus there may be some differences between the study sample and the general population. CONCLUSIONS: Maternal pregnancy-related anxiety may affect child brain emotion processing development. Further research is needed to understand the functional and developmental significance of the findings.

Hemodynamic responses to emotional speech in two-month-old infants imaged using diffuse optical tomography.

Emotional speech is one of the principal forms of social communication in humans. In this study, we investigated neural processing of emotional speech (happy, angry, sad and neutral) in the left hemisphere of 21 two-month-old infants using diffuse optical tomography. Reconstructed total hemoglobin (HbT) images were analysed using adaptive voxel-based clustering and region-of-interest (ROI) analysis. We found a distributed happy > neutral response within the temporo-parietal cortex, peaking in the anterior temporal cortex; a negative HbT response to emotional speech (the average of the emotional speech conditions < baseline) in the temporo-parietal cortex, neutral > angry in the anterior superior temporal sulcus (STS), happy > angry in the superior temporal gyrus and posterior superior temporal sulcus, angry < baseline in the insula, superior temporal sulcus and superior temporal gyrus and happy < baseline in the anterior insula. These results suggest that left STS is more sensitive to happy speech as compared to angry speech, indicating that it might play an important role in processing positive emotions in two-month-old infants. Furthermore, happy speech (relative to neutral) seems to elicit more activation in the temporo-parietal cortex, thereby suggesting enhanced sensitivity of temporo-parietal cortex to positive emotional stimuli at this stage of infant development.

Emotional Processing in the First 2 Years of Life: A Review of Near-Infrared Spectroscopy Studies.

Emotional stimuli processing during childhood helps us to detect salient cues in our environment and prepares us for our social life. In early childhood, the emotional valences of auditory and visual input are salient and relevant cues of social aspects of the environment, and it is of special interest to understand how exactly the processing of emotional stimuli develops. Near-infrared spectroscopy (NIRS) is a noninvasive neuroimaging tool that has proven valuable in studying emotional processing in children. After conducting a systematic search of PubMed, Web of Science, and Embase databases, we examined 50 NIRS studies performed to study emotional stimuli processing in children in the first 2 years of age. We found that the majority of these studies are done in infants and the most commonly used stimuli are visual and auditory. Many of the reviewed studies suggest the involvement of bilateral temporal areas in emotional processing of visual and auditory stimuli. It is unclear which neural activation patterns reflect maturation and at what age the emotional encoding reaches those typically seen in adults. Our review provides an overview of the database on emotional processing in children up to 2 years of age. Furthermore, it demonstrates the need to include the less-studied age range of 1 to 2 years, and suggests the use of combined audio-visual stimuli and longitudinal studies for future research on emotional processing in children. Thus, NIRS might be a vital tool to study the associations between the early pattern of neural responses and socioemotional development later in life.

Affective and non-affective touch evoke differential brain responses in 2-month-old infants.

Caressing touch is an effective way to communicate emotions and to create social bonds. It is also one of the key mediators of early parental bonding. The caresses are generally thought to represent a social form of touching and indeed, slow, gentle brushing is encoded in specialized peripheral nerve fibers, the C-tactile (CT) afferents. In adults, areas such as the posterior insula and superior temporal sulcus are activated by affective, slow stroking touch but not by fast stroking stimulation. However, whether these areas are activated in infants, after social tactile stimulation, is unknown. In this study, we compared the total hemoglobin responses measured with diffuse optical tomography (DOT) in the left hemisphere following slow and fast stroking touch stimulation in 16 2-month-old infants. We compared slow stroking (optimal CT afferent stimulation) to fast stroking (non-optimal CT stimulation). Activated regions were delineated using two methods: one based on contrast between the two conditions, and the other based on voxel-based statistical significance of the difference between the two conditions. The first method showed a single activation cluster in the temporal cortex with center of gravity in the middle temporal gyrus where the total hemoglobin increased after the slow stroking relative to the fast stroking (p = 0.04 uncorrected). The second method revealed a cluster in the insula with an increase in total hemoglobin in the insular cortex in response to slow stroking relative to fast stroking (p = 0.0005 uncorrected; p = 0.04 corrected for multiple comparisons). These activation clusters encompass areas that are involved in processing of affective, slow stroking touch in the adult brain. We conclude that the infant brain shows a pronounced and adult-like response to slow stroking touch compared to fast stroking touch in the insular cortex but the expected response in the primary somatosensory cortex was not found at this age. The results imply that emotionally valent touch is encoded in the brain in adult-like manner already soon after birth and this suggests a potential for involvement of touch in bonding with the caretaker.

Effect of task-related extracerebral circulation on diffuse optical tomography: experimental data and simulations on the forehead.

The effect of task-related extracerebral circulatory changes on diffuse optical tomography (DOT) of brain activation was evaluated using experimental data from 14 healthy human subjects and computer simulations. Total hemoglobin responses to weekday-recitation, verbal-fluency, and hand-motor tasks were measured with a high-density optode grid placed on the forehead. The tasks caused varying levels of mental and physical stress, eliciting extracerebral circulatory changes that the reconstruction algorithm was unable to fully distinguish from cerebral hemodynamic changes, resulting in artifacts in the brain activation images. Crosstalk between intra- and extracranial layers was confirmed by the simulations. The extracerebral effects were attenuated by superficial signal regression and depended to some extent on the heart rate, thus allowing identification of hemodynamic changes related to brain activation during the verbal-fluency task. During the hand-motor task, the extracerebral component was stronger, making the separation less clear. DOT provides a tool for distinguishing extracerebral components from signals of cerebral origin. Especially in the case of strong task-related extracerebral circulatory changes, however, sophisticated reconstruction methods are needed to eliminate crosstalk artifacts.

Magnetic-stimulation-related physiological artifacts in hemodynamic near-infrared spectroscopy signals.

Hemodynamic responses evoked by transcranial magnetic stimulation (TMS) can be measured with near-infrared spectroscopy (NIRS). This study demonstrates that cerebral neuronal activity is not their sole contributor. We compared bilateral NIRS responses following brain stimulation to those from the shoulders evoked by shoulder stimulation and contrasted them with changes in circulatory parameters. The left primary motor cortex of ten subjects was stimulated with 8-s repetitive TMS trains at 0.5, 1, and 2 Hz at an intensity of 75% of the resting motor threshold. Hemoglobin concentration changes were measured with NIRS on the stimulated and contralateral hemispheres. The photoplethysmograph (PPG) amplitude and heart rate were recorded as well. The left shoulder of ten other subjects was stimulated with the same protocol while the hemoglobin concentration changes in both shoulders were measured. In addition to PPG amplitude and heart rate, the pulse transit time was recorded. The brain stimulation reduced the total hemoglobin concentration (HbT) on the stimulated and contralateral hemispheres. The shoulder stimulation reduced HbT on the stimulated shoulder but increased it contralaterally. The waveforms of the HbT responses on the stimulated hemisphere and shoulder correlated strongly with each other (r = 0.65-0.87). All circulatory parameters were also affected. The results suggest that the TMS-evoked NIRS signal includes components that do not result directly from cerebral neuronal activity. These components arise from local effects of TMS on the vasculature. Also global circulatory effects due to arousal may affect the responses. Thus, studies involving TMS-evoked NIRS responses should be carefully controlled for physiological artifacts and effective artifact removal methods are needed to draw inferences about TMS-evoked brain activity.

Accelerometer-based method for correcting signal baseline changes caused by motion artifacts in medical near-infrared spectroscopy.

In medical near-infrared spectroscopy (NIRS), movements of the subject often cause large step changes in the baselines of the measured light attenuation signals. This prevents comparison of hemoglobin concentration levels before and after movement. We present an accelerometer-based motion artifact removal (ABAMAR) algorithm for correcting such baseline motion artifacts (BMAs). ABAMAR can be easily adapted to various long-term monitoring applications of NIRS. We applied ABAMAR to NIRS data collected in 23 all-night sleep measurements and containing BMAs from involuntary movements during sleep. For reference, three NIRS researchers independently identified BMAs from the data. To determine whether the use of an accelerometer improves BMA detection accuracy, we compared ABAMAR to motion detection based on peaks in the moving standard deviation (SD) of NIRS data. The number of BMAs identified by ABAMAR was similar to the number detected by the humans, and 79% of the artifacts identified by ABAMAR were confirmed by at least two humans. While the moving SD of NIRS data could also be used for motion detection, on average 2 out of the 10 largest SD peaks in NIRS data each night occurred without the presence of movement. Thus, using an accelerometer improves BMA detection accuracy in NIRS.

Correlation of visual-evoked hemodynamic responses and potentials in human brain.

The interaction of brain hemodynamics and neuronal activity has been intensively studied in recent years to yield better understanding of brain function. We investigated the relationship between visual-evoked hemodynamic responses (HDRs), measured with near-infrared spectroscopy (NIRS), and neuronal activity in humans, approximated with the stimulus train duration or with visual-evoked potentials (VEPs). Concentration changes of oxyhemoglobin (HbO(2)) and deoxyhemoglobin (HbR) in tissue and VEPs were recorded simultaneously over the occipital lobe of ten healthy subjects to 3, 6, and 12 s pattern-reversing checkerboard stimulus trains having a reversal frequency of 2 Hz. We found that the area-under-the-curves (Sigma) of HbO(2) and HbR were linearly correlated with the stimulus train duration and with the SigmaVEP summed over the 3, 6, and 12 s stimulus train durations. The correlation was stronger between the SigmaHbO(2) or the SigmaHbR and the SigmaVEP than between the SigmaHbO(2) or the SigmaHbR and the stimulus train duration. The SigmaVEPs explained 55% of the SigmaHbO(2) and 74% of the SigmaHbR variance, whereas the stimulus train duration explained only 45% of the SigmaHbO(2) and 51% of the SigmaHbR variance. We used Sigma of the NIRS responses and VEPs because we wanted to incorporate all possible processes (e.g., attention, habituation, etc.) affecting the responses. The results indicate that the relationship between brain HDRs and VEPs is approximately linear for 3-12 s long stimulus trains consisting of checkerboard patterns reversing at 2 Hz. To interpret hemodynamic responses, the measurement of evoked potentials is beneficial compared to the use of indirect parameters such as the stimulus duration. In addition, interindividual differences in the HbO(2) and HbR responses may be partly explained with differences in the VEPs.

Hemodynamic responses to speech and music in newborn infants.

We used near-infrared spectroscopy (NIRS) to study responses to speech and music on the auditory cortices of 13 healthy full-term newborn infants during natural sleep. The purpose of the study was to investigate the lateralization of speech and music responses at this stage of development. NIRS data was recorded from eight positions on both hemispheres simultaneously with electroencephalography, electrooculography, electrocardiography, pulse oximetry, and inclinometry. In 11 subjects, statistically significant (P < 0.02) oxygenated (HbO2) and total hemoglobin (HbT) responses were recorded. Both stimulus types elicited significant HbO2 and HbT responses on both hemispheres in five subjects. Six of the 11 subjects had positive HbO2 and HbT responses to both stimulus types, whereas one subject had negative responses. Mixed positive and negative responses were observed in four neonates. On both hemispheres, speech and music responses were significantly correlated (r = 0.64; P = 0.018 on the left hemisphere (LH) and r = 0.60; P = 0.029 on the right hemisphere (RH)). On the group level, the average response to the speech stimuli was statistically significantly greater than zero in the LH, whereas responses on the RH or to the music stimuli did not differ significantly from zero. This suggests a more coherent response to speech on the LH. However, significant differences in lateralization of the responses or mean response amplitudes of the two stimulus types were not observed on the group level.

Comparison between a time-domain and a frequency-domain system for optical tomography.

The quality of phase and amplitude data from two medical optical tomography systems were compared. The two systems are a 32-channel time-domain system developed at University College London (UCL) and a 16-channel frequency-domain system developed at Helsinki University of Technology (HUT). Difference data measured from an inhomogeneous and a homogeneous phantom were compared with a finite-element method (diffusion equation) and images of scattering and absorption were reconstructed based on it. The measurements were performed at measurement times between 1 and 30 s per source. The mean rms errors in the data measured by the HUT system were 3.4% for amplitude and 0.51 deg for phase, while the corresponding values for the UCL data were 6.0% and 0.46 deg, respectively. The reproducibility of the data measured with the two systems was tested with a measurement time of 5 s per source. It was 0.4% in amplitude for the HUT system and 4% for the UCL system, and 0.08 deg in phase for both systems. The image quality of the reconstructions from the data measured with the two systems were compared with several quantitative criteria. In general a higher contrast was observed in the images calculated from the HUT data.

Bilateral hemodynamic responses to auditory stimulation in newborn infants.

We studied hemodynamic auditory evoked responses of 20 healthy full-term neonates with near-infrared spectroscopy. The instrument used allows the measurements to be performed simultaneously above both auditory cortices. The stimulation consisted of 5-s trains of sound (700-ms interstimulus interval) with a 25-s silent interval. In response to the stimulation, a significant increase in concentration of oxygenated hemoglobin was detected in 14 out of 21 measurements. The mean latency of the largest response was 9.63+/-2.20 s (mean+/-SD) and the mean amplitude was 1.02+/-0.53 microM. The response amplitude was significantly larger in active (1.28+/-0.59 microM) than in quiet sleep (0.76+/-0.32 microM). The latency of the oxygenated hemoglobin concentration response was significantly shorter (r=-0.70 and p=0.0023) for infants with higher gestational age.

An application of perturbation Monte Carlo in optical tomography.

Haemodynamic changes related to activation of the human visual cortex were studied using optical imaging. The change in oxyhaemoglobin concentration in the visual cortex was estimated using a perturbation Monte Carlo (pMC) method. Comparison to a topographic map obtained using the modified Beer-Lambert law and interpolation is given.