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Neglectful maternal caregiving involves altered brain volume in empathy-related areas

Published online by Cambridge University Press:  17 December 2019

María José Rodrigo Open the ORCID record for María José Rodrigo [Opens in a new window] ,
Inmaculada León ,
Lorna García-Pentón ,
Juan Andrés Hernández-Cabrera  and
Ileana Quiñones
María José Rodrigo*
Affiliation:
Instituto Universitario de Neurociencia, La Laguna, Canary Islands, Spain Facultad de Psicología. Universidad de La Laguna, La Laguna, Canary Islands, Spain
Inmaculada León
Affiliation:
Instituto Universitario de Neurociencia, La Laguna, Canary Islands, Spain Facultad de Psicología. Universidad de La Laguna, La Laguna, Canary Islands, Spain
Lorna García-Pentón
Affiliation:
Department of Psychology at Scarborough; University of Toronto, Toronto, Canada
Juan Andrés Hernández-Cabrera
Affiliation:
Instituto Universitario de Neurociencia, La Laguna, Canary Islands, Spain Facultad de Psicología. Universidad de La Laguna, La Laguna, Canary Islands, Spain
Ileana Quiñones
Affiliation:
Basque Center on Cognition, Brain, and Language, Donostia-San Sebastián, Basque Country, Spain.
*
Author for Correspondence: María José Rodrigo, Facultad de Psicología, Campus de Guajara, Universidad de La Laguna, La Laguna, Canary Islands, Spain; E-mail; mjrodri@ull.es
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Abstract

The maternal brain undergoes adaptations to sensitive caregiving that are critical for infant well-being. We investigated structural alterations associated with neglectful caregiving and their effects on mother–child interactive behavior. High-resolution 3D volumetric images were obtained on 25 neglectful (NM) and 23 non-neglectful control (CM) mothers. Using voxel-based morphometry, we compared differences in gray and white matter (GM and WM, respectively) volume. Mothers completed an empathy scale and participated with their children in a play task (Emotional Availability Scale, EA). Neglectful mothers showed smaller GM volume in the right insula, anterior/middle cingulate (ACC/MCC), and right inferior frontal gyrus and less WM volume in bilateral frontal regions than did CM. A greater GM volume was observed in the right fusiform and cerebellum in NM than in CM. Regression analyses showed a negative effect of greater fusiform GM volume and a positive effect of greater right frontal WM volume on EA. Mediation analyses showed the role of emotional empathy in the positive effect of the insula and right inferior frontal gyrus and in the negative effect of the cerebellum on EA. Neglectful mothering involves alterations in emotional empathy-related areas and in frontal areas associated with poor mother–child interactive bonding, indicating how critical these areas are for sensitive caregiving.

Keywords

empathymaternal neglectmother–child interactionvolume alterationsvoxel-based morphometry
Type
Regular Articles
Information
Development and Psychopathology , Volume 32 , Special Issue 4: Conceptualizing and Interrogating Autism Spectrum Disorder from a Developmental Psychopathology Framework , October 2020 , pp. 1534 - 1543
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Copyright
Copyright © Cambridge University Press 2019

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References

Abraham, E., Hendler, T., Shapira-Lichter, I., Kanat-Maymon, Y., Zagoory-Sharon, O., & Feldman, R. (2014). Father's brain is sensitive to childcare experiences. Proceedings of the National Academy of Sciences, 111, 9792–9797.CrossRefGoogle ScholarPubMed
Adamaszek, M., D'Agata, F., Ferrucci, R., Habas, C., Keulen, S., Kirkby, K., … Verhoeven, J. (2017). Consensus paper: Cerebellum and emotion. The Cerebellum, 16, 552–576.CrossRefGoogle ScholarPubMed
Altenhofen, S., Clyman, R., Little, C., Baker, M., & Biringen, Z. (2013). Attachment security in three-year-olds who entered substitute care in infancy. Infant Mental Health Journal, 34, 435–445. doi:10.1002/imhj.21401CrossRefGoogle ScholarPubMed
Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. Neuroimage, 38, 95–113. doi:10.1016/j.neuroimage.2007.07.007CrossRefGoogle ScholarPubMed
Ashburner, J., & Friston, K. J. (2000). Voxel-based morphometry—the methods. Neuroimage, 11, 805–821. doi:10.1006/nimg.2000.0582CrossRefGoogle Scholar
Banissy, M. J., Kanai, R., Walsh, V., & Rees, G. (2012). Inter-individual differences in empathy are reflected in human brain structure. Neuroimage, 62, 2034–2039. doi:10.1016/j.neuroimage.2012.05.081CrossRefGoogle ScholarPubMed
Barba-Müller, E., Craddock, S., Carmona, S., & Hoekzema, E. (2019). Brain plasticity in pregnancy and the postpartum period: Links to maternal caregiving and mental health. Archives of Women's Mental Health, 22, 289–299. doi:10.1007/s00737-018-0889-zCrossRefGoogle ScholarPubMed
Barnett, D., Manly, J. T., & Cicchetti, D. (1993). Defining child maltreatment: The interface between policy and research. Child Abuse, Child Development, and Social Policy, 8, 7–73.Google Scholar
Belsley, D. A. (1991). A guide to using the collinearity diagnostics. Computer Science in Economics and Management, 4, 33–50. doi:10.1007/BF00426854Google Scholar
Biringen, Z. (2000). Emotional availability: Conceptualization and research findings. American Journal of Orthopsychiatry, 70(1), 104–114. doi:10.1037/h0087711CrossRefGoogle ScholarPubMed
Biringen, Z., Derscheid, D., Vliegen, N., Closson, L., & Easterbrooks, M. A. (2014). Emotional availability (EA): Theoretical background, empirical research using the EA Scales, and clinical applications. Developmental Review, 34, 114–167. doi:10.1016/j.dr.2014.01.002CrossRefGoogle Scholar
Davis, M. H. (1980). A multidimensional approach to individual differences in empathy. JSAS Catalog of Selected Documents in Psychology, 10, 85.Google Scholar
Easterbrooks, M. A., & Biringen, Z. (2005). The Emotional Availability Scales: Methodological refinements of the construct and clinical implications related to gender and at-risk interactions. Infant Mental Health Journal: Official Publication of The World Association for Infant Mental Health, 26, 291–294.CrossRefGoogle ScholarPubMed
Eres, R., Decety, J., Louis, W. R., & Molenberghs, P. (2015). Individual differences in local gray matter density are associated with differences in affective and cognitive empathy. NeuroImage, 117, 305–310. doi:10.1016/j.neuroimage.2015.05.038CrossRefGoogle ScholarPubMed
Fan, Y., Duncan, N. W., de Greck, M., & Northoff, G. (2011). Is there a core neural network in empathy? An fMRI based quantitative meta-analysis. Neuroscience & Biobehavioral Reviews, 35(3), 903–911. doi:10.1016/j.neubiorev.2010.10.009CrossRefGoogle Scholar
Ferrando, L., Bobes, J., Gibert, J., Soto, M., & Soto, O. (2000). MINI Entrevista Neuropsiquiátrica Internacional (MINI International Neuropsychiatric Interview, MINI). Instrumentos de Detección y Orientación Diagnóstica. Spanish Version 5.0. DSM-IV. Madrid: Instituto IAP.Google Scholar
Gingnell, M., Bannbers, E., Moes, H., Engman, J., Sylvén, S., Skalkidou, A., … Sundström-Poromaa, I. (2015). Emotion reactivity is increased 4–6 weeks postpartum in healthy women: A longitudinal fMRI study. PloS One, 10, e0128964. doi:10.1371/journal.pone.0128964CrossRefGoogle ScholarPubMed
Gläscher, J., & Gitelman, D. (2008). Contrast weights in flexible factorial design with multiple groups of subjects. Sml, Editor.Google Scholar
Hoekzema, E., Barba-Müller, E., Pozzobon, C., Picado, M., Lucco, F., García-García, D., … Vilarroya, O. (2017). Pregnancy leads to long-lasting changes in human brain structure. Nature Neuroscience, 20, 287–296.CrossRefGoogle ScholarPubMed
Jiang, H., Van Zijl, P. C., Kim, J., Pearlson, G. D., & Mori, S. (2006). DtiStudio: Resource program for diffusion tensor computation and fiber bundle tracking. Computer Methods and Programs in Biomedicine, 81, 106–116. doi:10.1016/j.cmpb.2005.08.004CrossRefGoogle ScholarPubMed
Kim, P., Leckman, J. F., Mayes, L. C., Newman, M.-A., Feldman, R., & Swain, J. E. (2010). Perceived quality of maternal care in childhood and structure and function of mothers’ brain. Developmental Science, 13, 662–673. doi:10.1111/j.1467-7687.2009.00923.xCrossRefGoogle ScholarPubMed
Kim, P., Strathearn, L., & Swain, J. E. (2016). The maternal brain and its plasticity in humans. Hormones and Behavior, 77, 113–123. doi:10.1016/j.yhbeh.2015.08.001CrossRefGoogle ScholarPubMed
León, I., Rodrigo, M. J., El-Deredy, W., Modroño, C., Hernández-Cabrera, J. A., & Quiñones, I. (2019). Limbic-visual attenuation to crying faces underlies neglectful mothering. Scientific Reports, 9, Article 6373.Retrieved from doi:10.1038/s41598-019-42908-1CrossRefGoogle ScholarPubMed
León, I., Rodrigo, M. J., Quiñones, I., Hernández, J. A., Lage, A., Padrón, I., & Bobes, M. A. (2014). Electrophysiological responses to affective stimuli in neglectful mothers. PloS One, 9, e87808. Retrieved from doi:10.1371/journal.pone.0087808CrossRefGoogle ScholarPubMed
Lin, H.C., & McFatter, R. (2012). Empathy and distress: Two distinct but related emotions in response to infant crying. Infant Behavior and Development, 35, 887–897. doi:10.1016/j.infbeh.2012.08.001CrossRefGoogle ScholarPubMed
Mielke, E. L., Neukel, C., Bertsch, K., Reck, C., Möhler, E., & Herpertz, S. C. (2016). Maternal sensitivity and the empathic brain: Influences of early life maltreatment. Journal of Psychiatric Research, 77, 59–66. doi:10.1016/j.jpsychires.2016.02.013CrossRefGoogle ScholarPubMed
Mutschler, I., Reinbold, C., Wankerl, J., Seifritz, E., & Ball, T. (2013). Structural basis of empathy and the domain general region in the anterior insular cortex. Frontiers in Human Neuroscience, 7, 177. doi:10.3389/fnhum.2013.00177CrossRefGoogle ScholarPubMed
Nichols, T., & Hayasaka, S. (2003). Controlling the familywise error rate in functional neuroimaging: A comparative review. Statistical Methods in Medical Research, 12, 419–446. doi:10.1191/0962280203sm341raCrossRefGoogle ScholarPubMed
Nishitani, S., Doi, H., Koyama, A., & Shinohara, K. (2011). Differential prefrontal response to infant facial emotions in mothers compared with non-mothers. Neuroscience Research, 70, 183–188. doi:10.1016/j.neures.2011.02.007CrossRefGoogle ScholarPubMed
Oishi, K., Faria, A. V., Van Zijl, P. C., & Mori, S. (2010). MRI atlas of human white matter. Academic Press.Google Scholar
Papoušek, H., & Papoušek, M. (1987). Intuitive parenting: A dialectic counterpart to the infant's integrative competence. In Osofsky, J. D. (Ed.), Wiley series on personality processes. Handbook of infant development (pp. 669–720). Oxford, England: John Wiley & Sons.Google Scholar
Parkinson, C., & Wheatley, T. (2012). Relating anatomical and social connectivity: White matter microstructure predicts emotional empathy. Cerebral Cortex, 24, 614–625. doi:10.1093/cercor/bhs347CrossRefGoogle ScholarPubMed
Pérez-Albéniz, A., De Paúl, J., Etxeberría, J., Montes, M. P., & Torres, E. (2003). Adaptación de interpersonal reactivity index (IRI) al español. Psicothema, 15, 267–272.Google Scholar
Petersen, A., Joseph, J., & Feit, M. (2014). New directions in child abuse and neglect research. Report of the Committee on Child Maltreatment Research, Policy, and Practice for the Next Decade: Phase II. Washington, DC: National Academies Press.Google Scholar
Rajapakse, J. C., Giedd, J. N., & Rapoport, J. L. (1997). Statistical approach to segmentation of single-channel cerebral MR images. IEEE Transactions on Medical Imaging, 16, 176–186. doi:10.1109/42.563663CrossRefGoogle ScholarPubMed
R Core Team. (2019). R: A Language and Environment for Statistical Computing. Retrieved from https://www.R-project.org/Google Scholar
Rocchetti, M., Radua, J., Paloyelis, Y., Xenaki, L.-A., Frascarelli, M., Caverzasi, E., … Fusar-Poli, P. (2014). Neurofunctional maps of the ‘maternal brain'and the effects of oxytocin: A multimodal voxel-based meta-analysis. Psychiatry and Clinical Neurosciences, 68, 733–751. doi:10.1111/pcn.12185CrossRefGoogle ScholarPubMed
Rodrigo, M. J., León, I., Góngora, D., Hernández, J. A., Byrne, S., & Bobes, A. (2016). Inferior fronto-temporo-occipital connectivity: A missing link between maltreated girls and neglectful mothers. Social Cognitive and Affective Neuroscience, 11, 1658–1665. doi:10.1093/scan/nsw080CrossRefGoogle ScholarPubMed
Rodrigo, M. J., León, I., Quiñones, I., Lage, A., Byrne, S., & Bobes, M. A. (2011). Brain and personality bases of insensitivity to infant cues in neglectful mothers: An event-related potential study. Development and Psychopathology, 23, 163–176. doi:10.1017/S0954579410000714CrossRefGoogle Scholar
Rutherford, H. J., Wallace, N. S., Laurent, H. K., & Mayes, L. C. (2015). Emotion regulation in parenthood. Developmental Review, 36, 1–14. doi:10.1016/j.dr.2014.12.008CrossRefGoogle ScholarPubMed
Shamay-Tsoory, S. G., Aharon-Peretz, J., & Perry, D. (2009). Two systems for empathy: A double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain, 132, 617–627. doi:10.1093/brain/awn279CrossRefGoogle ScholarPubMed
Silver, M., Moore, C. M., Villamarin, V., Jaitly, N., Hall, J. E., Rothschild, A. J., & Deligiannidis, K. M. (2018). White matter integrity in medication-free women with peripartum depression: A tract-based spatial statistics study. Neuropsychopharmacology, 43, 1573–1580. doi:10.1038/s41386-018-0023-yCrossRefGoogle ScholarPubMed
Stern, J. A., Borelli, J. L., & Smiley, P. A. (2015). Assessing parental empathy: A role for empathy in child attachment. Attachment & Human Development, 17, 1–22. doi:10.1080/14616734.2014.969749CrossRefGoogle ScholarPubMed
Stoltenborgh, M., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2013). The neglect of child neglect: A meta-analytic review of the prevalence of neglect. Social Psychiatry and Psychiatric Epidemiology, 48(3), 345–355. doi:10.1007/s00127-012-0549-yCrossRefGoogle ScholarPubMed
Teicher, M. H., Samson, J. A., Anderson, C. M., & Ohashi, K. (2016). The effects of childhood maltreatment on brain structure, function and connectivity. Nature Reviews Neuroscience, 17, 652–666. doi:10.1038/nrn.2016.111CrossRefGoogle ScholarPubMed
Tingley, D., Yamamoto, T., Hirose, K., Keele, L., & Imai, K. (2014). Mediation: R package for causal mediation analysis. Journal of Statistical Software, 59. doi:10.18637/jss.v059.i05CrossRefGoogle Scholar
Tohka, J., Zijdenbos, A., & Evans, A. (2004). Fast and robust parameter estimation for statistical partial volume models in brain MRI. Neuroimage, 23, 84–97. doi:10.1016/j.neuroimage.2004.05.007CrossRefGoogle ScholarPubMed
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., … Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage, 15, 273–289. doi:10.1006/nimg.2001.0978CrossRefGoogle ScholarPubMed
Upshaw, M. B., Kaiser, C. R., & Sommerville, J. A. (2015). Parents’ empathic perspective taking and altruistic behavior predicts infants’ arousal to others’ emotions. Frontiers in Psychology, 6, Article 360. doi:10.3389/fpsyg.2015.00360CrossRefGoogle ScholarPubMed
Weiner, K. S., & Zilles, K. (2016). The anatomical and functional specialization of the fusiform gyrus. Neuropsychologia, 83, 48–62. doi:10.1016/j.neuropsychologia.2015.06.033CrossRefGoogle ScholarPubMed
Weinfield, N. S., Sroufe, L. A., Egeland, B., & Carlson, E. (2008). Individual differences in infant-caregiver attachment: Conceptual and empirical aspects of security. In Cassidy, J., & Shaver, P. R. (Eds.), Handbook of attachment: Theory, research, and clinical applications (2nd ed., pp. 78–101). New York: Guilford Press.Google Scholar
Yeh, F.-C., & Tseng, W.-Y. I. (2011). NTU-90: A high angular resolution brain atlas constructed by q-space diffeomorphic reconstruction. Neuroimage, 58, 91–99. doi:10.1016/j.neuroimage.2011.06.021CrossRefGoogle ScholarPubMed
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