Significant increases of the amygdala between immediate and late postpartum: Pronounced effects within the superficial subregion.


Journal

Journal of neuroscience research
ISSN: 1097-4547
Titre abrégé: J Neurosci Res
Pays: United States
ID NLM: 7600111

Informations de publication

Date de publication:
09 2021
Historique:
revised: 08 04 2021
received: 22 01 2021
accepted: 02 05 2021
pubmed: 9 6 2021
medline: 11 2 2022
entrez: 8 6 2021
Statut: ppublish

Résumé

Research exploring the underlying neuroanatomical correlates of early motherhood seems to suggest that the period after giving birth is marked by tissue increases in the mother's brain. While some studies point to the amygdala as one of the areas undergoing postpartum changes, existing analyses did not discriminate between the different subregions of this functionally heterogeneous structure. Thus, to further extend this understudied field of research and to better understand the potential role of the amygdala when transitioning to motherhood, we applied an advanced region-of-interest technique that enabled us to analyze the amygdala as a whole as well as its different subareas, specifically the left and right centromedian (CM), laterobasal (LB), and superficial (SF) regions. Comparing the brains of 14 healthy women between immediate postpartum (within 1-2 days of childbirth) and late postpartum (at 4-6 weeks after childbirth), we revealed increases of the amygdala. However, effects manifested differentially across subareas, with particularly strong effects for the SF region, moderate effects for the CM region, and no effects for the LB region. These findings might reflect region-specific adaptations of the mother's brain tuning into the distinct and ever-changing needs of a newborn, either as a cause for it or as a consequence thereof.

Identifiants

pubmed: 34101893
doi: 10.1002/jnr.24855
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2261-2270

Informations de copyright

© 2021 Wiley Periodicals LLC.

Références

Aggleton, J. P. (2000). The amygdala: A functional analysis. Oxford University Press.
Alexander, R., Aragon, O. R., Bookwala, J., Cherbuin, N., Gatt, J. M., Kahrilas, I. J., Kastner, N., Lawrence, A., Lowe, L., Morrison, R. G., Mueller, S. C., Nusslock, R., Papadelis, C., Polnaszek, K. L., Helene Richter, S., Silton, R. L., & Styliadis, C. (2021). The neuroscience of positive emotions and affect: Implications for cultivating happiness and wellbeing. Neuroscience and Biobehavioral Reviews, 121, 220-249. https://doi.org/10.1016/j.neubiorev.2020.12.002
Amano, T., Duvarci, S., Popa, D., & Pare, D. (2011). The fear circuit revisited: Contributions of the basal amygdala nuclei to conditioned fear. Journal of Neuroscience, 31, 15481-15489. https://doi.org/10.1523/JNEUROSCI.3410-11.2011
Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., Habel, U., Schneider, F., & Zilles, K. (2005). Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: Intersubject variability and probability maps. Anatomy and Embryology, 210, 343-352. https://doi.org/10.1007/s00429-005-0025-5
Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. Neuroimage, 38, 95-113. https://doi.org/10.1016/j.neuroimage.2007.07.007
Ashburner, J., & Friston, K. J. (2000). Voxel-based morphometry-The methods. Neuroimage, 11, 805-821. https://doi.org/10.1006/nimg.2000.0582
Babaev, O., Piletti Chatain, C., & Krueger-Burg, D. (2018). Inhibition in the amygdala anxiety circuitry. Experimental & Molecular Medicine, 50, 1-16. https://doi.org/10.1038/s12276-018-0063-8
Barba-Muller, 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. https://doi.org/10.1007/s00737-018-0889-z
Brockett, A. T., Vazquez, D., & Roesch, M. R. (2021). Prediction errors and valence: From single units to multidimensional encoding in the amygdala. Behavioral Brain Research, 404, 113176. https://doi.org/10.1016/j.bbr.2021.113176
Burgdorf, J., & Panksepp, J. (2006). The neurobiology of positive emotions. Neuroscience and Biobehavioral Reviews, 30, 173-187. https://doi.org/10.1016/j.neubiorev.2005.06.001
Bzdok, D., Laird, A. R., Zilles, K., Fox, P. T., & Eickhoff, S. B. (2013). An investigation of the structural, connectional, and functional subspecialization in the human amygdala. Human Brain Mapping, 34, 3247-3266. https://doi.org/10.1002/hbm.22138
Carmona, S., Martinez-Garcia, M., Paternina-Die, M., Barba-Muller, E., Wierenga, L. M., Aleman-Gomez, Y., Pretus, C., Marcos-Vidal, L., Beumala, L., Cortizo, R., Pozzobon, C., Picado, M., Lucco, F., Garcia-Garcia, D., Soliva, J. C., Tobena, A., Peper, J. S., Crone, E. A., Ballesteros, A., … Hoekzema, E. (2019). Pregnancy and adolescence entail similar neuroanatomical adaptations: A comparative analysis of cerebral morphometric changes. Human Brain Mapping, 40, 2143-2152. https://doi.org/10.1002/hbm.24513
Costafreda, S. G., Brammer, M. J., David, A. S., & Fu, C. H. (2008). Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies. Brain Research Reviews, 58, 57-70. https://doi.org/10.1016/j.brainresrev.2007.10.012
Davis, M., Walker, D. L., Miles, L., & Grillon, C. (2010). Phasic vs sustained fear in rats and humans: Role of the extended amygdala in fear vs anxiety. Neuropsychopharmacology, 35, 105-135. https://doi.org/10.1038/npp.2009.109
Dufford, A. J., Erhart, A., & Kim, P. (2019). Maternal brain resting-state connectivity in the postpartum period. Journal of Neuroendocrinology, 31, e12737. https://doi.org/10.1111/jne.12737
Ehret, G., & Buckenmaier, J. (1994). Estrogen-receptor occurrence in the female mouse brain: Effects of maternal experience, ovariectomy, estrogen and anosmia. Journal of Physiology-Paris, 88, 315-329. https://doi.org/10.1016/0928-4257(94)90012-4
Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., & Zilles, K. (2005). A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage, 25, 1325-1335. https://doi.org/10.1016/j.neuroimage.2004.12.034
Garavan, H., Pendergrass, J. C., Ross, T. J., Stein, E. A., & Risinger, R. C. (2001). Amygdala response to both positively and negatively valenced stimuli. Neuroreport, 12, 2779-2783. https://doi.org/10.1097/00001756-200108280-00036
Gingnell, M., Bannbers, E., Moes, H., Engman, J., Sylven, S., Skalkidou, A., Kask, K., Wikstrom, J., & Sundstrom-Poromaa, I. (2015). Emotion reactivity is increased 4-6 weeks postpartum in healthy women: A longitudinal fMRI study. PLoS ONE, 10, e0128964. https://doi.org/10.1371/journal.pone.0128964
Good, C. D., Johnsrude, I. S., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. (2001). A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage, 14, 21-36. https://doi.org/10.1006/nimg.2001.0786
Goossens, L., Kukolja, J., Onur, O. A., Fink, G. R., Maier, W., Griez, E., Schruers, K., & Hurlemann, R. (2009). Selective processing of social stimuli in the superficial amygdala. Human Brain Mapping, 30, 3332-3338. https://doi.org/10.1002/hbm.20755
Haruno, M., & Frith, C. D. (2010). Activity in the amygdala elicited by unfair divisions predicts social value orientation. Nature Neuroscience, 13, 160-161. https://doi.org/10.1038/nn.2468
Hochberg, Y., & Benjamini, Y. (1990). More powerful procedures for multiple significance testing. Statistics in Medicine, 9, 811-818. https://doi.org/10.1002/sim.4780090710
Hoekzema, E., Barba-Muller, E., Pozzobon, C., Picado, M., Lucco, F., Garcia-Garcia, D., Soliva, J. C., Tobena, A., Desco, M., Crone, E. A., Ballesteros, A., Carmona, S., & Vilarroya, O. (2017). Pregnancy leads to long-lasting changes in human brain structure. Nature Neuroscience, 20, 287-296. https://doi.org/10.1038/nn.4458
Hunter, M. D., Eickhoff, S. B., Pheasant, R. J., Douglas, M. J., Watts, G. R., Farrow, T. F., Hyland, D., Kang, J., Wilkinson, I. D., Horoshenkov, K. V., & Woodruff, P. W. (2010). The state of tranquility: Subjective perception is shaped by contextual modulation of auditory connectivity. Neuroimage, 53, 611-618. https://doi.org/10.1016/j.neuroimage.2010.06.053
Hurlemann, R., Rehme, A. K., Diessel, M., Kukolja, J., Maier, W., Walter, H., & Cohen, M. X. (2008). Segregating intra-amygdalar responses to dynamic facial emotion with cytoarchitectonic maximum probability maps. Journal of Neuroscience Methods, 172, 13-20. https://doi.org/10.1016/j.jneumeth.2008.04.004
Kedo, O., Zilles, K., Palomero-Gallagher, N., Schleicher, A., Mohlberg, H., Bludau, S., & Amunts, K. (2018). Receptor-driven, multimodal mapping of the human amygdala. Brain Structure and Function, 223, 1637-1666.
Kim, P., Leckman, J. F., Mayes, L. C., Feldman, R., Wang, X., & Swain, J. E. (2010). The plasticity of human maternal brain: Longitudinal changes in brain anatomy during the early postpartum period. Behavioral Neuroscience, 124, 695-700. https://doi.org/10.1037/a0020884
Koepp, M. J., Hammers, A., Lawrence, A. D., Asselin, M. C., Grasby, P. M., & Bench, C. J. (2009). Evidence for endogenous opioid release in the amygdala during positive emotion. Neuroimage, 44, 252-256. https://doi.org/10.1016/j.neuroimage.2008.08.032
Kurth, F., Cherbuin, N., & Luders, E. (2019). Age but no sex effects on subareas of the amygdala. Human Brain Mapping, 40, 1697-1704. https://doi.org/10.1002/hbm.24481
Kurth, F., Jancke, L., & Luders, E. (2017). Sexual dimorphism of Broca's region: More gray matter in female brains in Brodmann areas 44 and 45. Journal of Neuroscience Research, 95, 626-632.
Kurth, F., Jancke, L., & Luders, E. (2018). Integrating cytoarchitectonic tissue probabilities with MRI-based signal intensities to calculate volumes of interest. In G. Spalletta, T. Gili, & F. Piras (Eds.), Brain morphometry: Methods and clinical applications (pp. 121-129). Springer.
LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155-184. https://doi.org/10.1146/annurev.neuro.23.1.155
Lisofsky, N., Gallinat, J., Lindenberger, U., & Kuhn, S. (2019). Postpartal neural plasticity of the maternal brain: Early renormalization of pregnancy-related decreases? Neurosignals, 27, 12-24.
Lonstein, J. S. (2007). Regulation of anxiety during the postpartum period. Frontiers in Neuroendocrinology, 28, 115-141. https://doi.org/10.1016/j.yfrne.2007.05.002
Luders, E., Gingnell, M., Poromaa, I. S., Engman, J., Kurth, F., & Gaser, C. (2018). Potential brain age reversal after pregnancy: Younger brains at 4-6 weeks postpartum. Neuroscience, 386, 309-314.
Luders, E., Kurth, F., Gingnell, M., Engman, J., Yong, E. L., Poromaa, I. S., & Gaser, C. (2020). From baby brain to mommy brain: Widespread gray matter gain after giving birth. Cortex, 126, 334-342. https://doi.org/10.1016/j.cortex.2019.12.029
Martinez-Garcia, M., Paternina-Die, M., Barba-Muller, E., Martin de Blas, D., Beumala, L., Cortizo, R., Pozzobon, C., Marcos-Vidal, L., Fernandez-Pena, A., Picado, M., Belmonte-Padilla, E., Masso-Rodriguez, A., Ballesteros, A., Desco, M., Vilarroya, O., Hoekzema, E., & Carmona, S. (2021). Do pregnancy-induced brain changes reverse? The brain of a mother six years after parturition. Brain Sciences, 11(2), 168.
Moreno, N., & Gonzalez, A. (2007). Evolution of the amygdaloid complex in vertebrates, with special reference to the anamnio-amniotic transition. Journal of Anatomy, 211, 151-163. https://doi.org/10.1111/j.1469-7580.2007.00780.x
Mulder, M. J., Keuken, M. C., Bazin, P. L., Alkemade, A., & Forstmann, B. U. (2019). Size and shape matter: The impact of voxel geometry on the identification of small nuclei. PLoS ONE, 14, e0215382. https://doi.org/10.1371/journal.pone.0215382
Namburi, P., Al-Hasani, R., Calhoon, G. G., Bruchas, M. R., & Tye, K. M. (2016). Architectural representation of valence in the limbic system. Neuropsychopharmacology, 41, 1697-1715. https://doi.org/10.1038/npp.2015.358
Namburi, P., Beyeler, A., Yorozu, S., Calhoon, G. G., Halbert, S. A., Wichmann, R., Holden, S. S., Mertens, K. L., Anahtar, M., Felix-Ortiz, A. C., Wickersham, I. R., Gray, J. M., & Tye, K. M. (2015). A circuit mechanism for differentiating positive and negative associations. Nature, 520, 675-678. https://doi.org/10.1038/nature14366
Numan, M., Bress, J. A., Ranker, L. R., Gary, A. J., Denicola, A. L., Bettis, J. K., & Knapp, S. E. (2010). The importance of the basolateral/basomedial amygdala for goal-directed maternal responses in postpartum rats. Behavioral Brain Research, 214, 368-376. https://doi.org/10.1016/j.bbr.2010.06.006
Oatridge, A., Holdcroft, A., Saeed, N., Hajnal, J. V., Puri, B. K., Fusi, L., & Bydder, G. M. (2002). Change in brain size during and after pregnancy: Study in healthy women and women with preeclampsia. American Journal of Neuroradiology, 23, 19-26.
Paul, S., Austin, J., Elliott, R., Ellison-Wright, I., Wan, M. W., Drake, R., Downey, D., Elmadih, A., Mukherjee, I., Heaney, L., Williams, S., & Abel, K. M. (2019). Neural pathways of maternal responding: Systematic review and meta-analysis. Archives of Women's Mental Health, 22, 179-187. https://doi.org/10.1007/s00737-018-0878-2
Pawluski, J. L., Lonstein, J. S., & Fleming, A. S. (2017). The neurobiology of postpartum anxiety and depression. Trends in Neurosciences, 40, 106-120. https://doi.org/10.1016/j.tins.2016.11.009
Pereira, M., & Ferreira, A. (2016). Neuroanatomical and neurochemical basis of parenting: Dynamic coordination of motivational, affective and cognitive processes. Hormones and Behavior, 77, 72-85. https://doi.org/10.1016/j.yhbeh.2015.08.005
Pessoa, L. (2010). Emotion and cognition and the amygdala: From “what is it?” to “what's to be done?”. Neuropsychologia, 48, 3416-3429. https://doi.org/10.1016/j.neuropsychologia.2010.06.038
Sacher, J., Chechko, N., Dannlowski, U., Walter, M., & Derntl, B. (2020). The peripartum human brain: Current understanding and future perspectives. Frontiers in Neuroendocrinology, 59, 100859. https://doi.org/10.1016/j.yfrne.2020.100859
Scalia, F., & Winans, S. S. (1975). The differential projections of the olfactory bulb and accessory olfactory bulb in mammals. Journal of Comparative Neurology, 161, 31-55. https://doi.org/10.1002/cne.901610105
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., Hergueta, T., Baker, R., & Dunbar, G. C. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry, 59(Suppl. 20), 22-33.
Spielberger, C. D., Gorsuch, R. L., & Lushene, R. E. (1983). Manual for the State-Trait Anxiety (STAI Form Y). Consulting Psychologist Press.
Styliadis, C., Ioannides, A. A., Bamidis, P. D., & Papadelis, C. (2014). Amygdala responses to valence and its interaction by arousal revealed by MEG. International Journal of Psychophysiology, 93, 121-133. https://doi.org/10.1016/j.ijpsycho.2013.05.006
Swain, J. E., Lorberbaum, J. P., Kose, S., & Strathearn, L. (2007). Brain basis of early parent-infant interactions: Psychology, physiology, and in vivo functional neuroimaging studies. Journal of Child Psychology and Psychiatry, 48, 262-287. https://doi.org/10.1111/j.1469-7610.2007.01731.x
Tohka, J., Zijdenbos, A., & Evans, A. (2004). Fast and robust parameter estimation for statistical partial volume models in brain MRI. Neuroimage, 23, 84-97. https://doi.org/10.1016/j.neuroimage.2004.05.007
Yilmazer-Hanke, D. (2015). Amygdala. In A. Toga (Ed.), Brain mapping: An encyclopedic reference (pp. 341-346). Academic Press.

Auteurs

Eileen Luders (E)

School of Psychology, University of Auckland, Auckland, New Zealand.
Laboratory of Neuro Imaging, School of Medicine, University of Southern California, Los Angeles, CA, USA.

Christian Gaser (C)

Department of Psychiatry, Jena University Hospital, Jena, Germany.
Department of Neurology, Jena University Hospital, Jena, Germany.

Malin Gingnell (M)

Department of Psychology, Uppsala University, Uppsala, Sweden.
Department of Women's and Children's Health, Uppsala University, Uppsala, Sweden.

Jonas Engman (J)

Department of Psychology, Uppsala University, Uppsala, Sweden.

Inger Sundström Poromaa (I)

Department of Women's and Children's Health, Uppsala University, Uppsala, Sweden.

Florian Kurth (F)

School of Psychology, University of Auckland, Auckland, New Zealand.

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