Maternal deprivation and milk replacement affect the integrity of gray and white matter in the developing lamb brain.

DTI MRI T1-weighted artificial rearing mothering sheep white and gray matter

Journal

Developmental neurobiology
ISSN: 1932-846X
Titre abrégé: Dev Neurobiol
Pays: United States
ID NLM: 101300215

Informations de publication

Date de publication:
03 2022
Historique:
revised: 17 01 2022
received: 07 05 2021
accepted: 27 01 2022
pubmed: 28 2 2022
medline: 1 4 2022
entrez: 27 2 2022
Statut: ppublish

Résumé

The psychoendocrine evaluation of lamb development has demonstrated that maternal deprivation and milk replacement alters health, behavior, and endocrine profiles. While lambs are able to discriminate familiar and non-familiar conspecifics (mother or lamb), only lambs reared with their mother develop such clear social discrimination or preference. Lambs reared without mother display no preference for a specific lamb from its own group. Differences in exploratory and emotional behaviors between mother-reared and mother-deprived lambs have also been reported. As these behavioural abilities are supported by the brain, we hypothesize that rearing with maternal deprivation and milk replacement leads to altered brain development and maturation. To test this hypothesis, we examined brain morphometric and microstructural variables extracted from in vivo T1-weighted and diffusion-weighted magnetic resonance images acquired longitudinally (1 week, 1.5 months, and 4.5 months of age) in mother-reared and mother-deprived lambs. From the morphometric variables the caudate nuclei volume was found to be smaller for mother-deprived than for mother-reared lambs. T1-weighted signal intensity and radial diffusivity were higher for mother-deprived than for mother-reared lambs in both the white and gray matters. The fractional anisotropy of the white matter was lower for mother-deprived than for mother-reared lambs. Based on these morphometric and microstructural characteristics we conclude that maternal deprivation delays and affects lamb brain growth and maturation.

Identifiants

pubmed: 35220679
doi: 10.1002/dneu.22869
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

214-232

Informations de copyright

© 2022 Wiley Periodicals LLC.

Références

Andropoulos, D. B. (2018). Effect of anesthesia on the developing brain: Infant and fetus. Fetal Diagnosis and Therapy, 43(1), 1-11. https://doi.org/10.1159/000475928
Avants, B. B., Tustison, N. J., Stauffer, M., Song, G., Wu, B., & Gee, J. C. (2014). The Insight ToolKit image registration framework. Frontiers in Neuroinformatics, 8, 44. https://doi.org/10.3389/fninf.2014.00044
Barkovich, A. J., Kjos, B. O., Jackson, D. E., & Norman, D. (1988). Normal maturation of the neonatal and infant brain: MR imaging at 1.5 T. Radiology, 166(1), 173-180. https://doi.org/10.1148/radiology.166.1.3336675
Barlow, R. M. (1969). The foetal sheep: Morphogenesis of the nervous system and histochemical aspects of myelination. The Journal of Comparative Neurology, 135(3), 249-261. https://doi.org/10.1002/cne.901350302
Bernstein, R. M., & Hinde, K. (2016). Bioactive factors in milk across lactation: Maternal effects and influence on infant growth in rhesus macaques (Macaca mulatta): Macaque milk bioactive factors. American Journal of Primatology, 78(8), 838-850. https://doi.org/10.1002/ajp.22544
Berry, M. J., Jaquiery, A. L., Oliver, M. H., Harding, J. E., & Bloomfield, F. H. (2016). Neonatal milk supplementation in lambs has persistent effects on growth and metabolic function that differ by sex and gestational age. British Journal of Nutrition, 116(11), 1912-1925. https://doi.org/10.1017/S0007114516004013
Black-Rubio, C. M., Cibils, A. F., & Gould, W. R. (2007). Maternal influence on feeding site avoidance behaviour of lambs. Applied Animal Behaviour Science, 105(1-3), 122-139. https://doi.org/10.1016/j.applanim.2006.06.004
Boivin, X., Nowak, R., & Garcia, A. T. (2001). The presence of the dam affects the efficiency of gentling and feeding on the early establishment of the stockperson-lamb relationship. Applied Animal Behaviour Science, 72(2), 89-103. https://doi.org/10.1016/S0168-1591(00)00201-X
Castillo-Melendez, M., Baburamani, A. A., Cabalag, C., Yawno, T., Witjaksono, A., Miller, S. L., & Walker, D. W. (2013). Experimental modelling of the consequences of brief late gestation asphyxia on newborn lamb behaviour and brain structure. PLoS ONE, 8(11), e77377. https://doi.org/10.1371/journal.pone.0077377
Chaillou, E., Tillet, Y., & Andersson, F. (2012). MRI Techniques and new animal models for imaging the brain. In T. Mantamadiotis (Ed.), When things go wrong-diseases and disorders of the human brain. InTech. https://doi.org/10.5772/35834
Cohen, R. A., Grieve, S., Hoth, K. F., Paul, R. H., Sweet, L., Tate, D., Gunstad, J., Stroud, L., McCaffery, J., Hitsman, B., Niaura, R., Clark, C. R., MacFarlane, A., Bryant, R., Gordon, E., & Williams, L. M. (2006). Early life stress and morphometry of the adult anterior cingulate cortex and caudate nuclei. Biological Psychiatry, 59, 975-982. https://doi.org/10.1016/j.biopsych.2005.12.016
Coplan, J. D., Abdallah, C. G., Tang, C. Y., Mathew, S. J., Martinez, J., Hof, P. R., Smith, E. L. P., Dwork, A. J., Perera, T. D., Pantol, G., Carpenter, D., Rosenblum, L. A., Shungu, D. C., Gelernter, J., Kaffman, A., Jackowski, A., Kaufman, J., & Gorman, J. M. (2010). The role of early life stress in development of the anterior limb of the internal capsule in nonhuman primates. Neuroscience Letters, 480(2), 93-96. https://doi.org/10.1016/j.neulet.2010.06.012
Damián, J. P., Beracochea, F., Hötzel, M. J., Banchero, G., & Ungerfeld, R. (2015). Reproductive and sexual behaviour development of dam or artificially reared male lambs. Physiology & Behavior, 147, 47-53. https://doi.org/10.1016/j.physbeh.2015.04.004
Damián, J. P., Beracochea, F., Machado, S., Hötzel, M. J., Banchero, G., & Ungerfeld, R. (2018). Growing without a mother results in poorer sexual behaviour in adult rams. Animal, 12(1), 98-105. https://doi.org/10.1017/S1751731117001574
De Matteo, R., Blasch, N., Stokes, V., Davis, P., & Harding, R. (2010). Induced preterm birth in sheep: A suitable model for studying the developmental effects of moderately preterm birth. Reproductive Sciences, 17(8), 724-733. https://doi.org/10.1177/1933719110369182
Deoni, S. C. L., Dean, D. C., Piryatinsky, I., O'Muircheartaigh, J., Waskiewicz, N., Lehman, K., Han, M., & Dirks, H. (2013). Breastfeeding and early white matter development: A cross-sectional study. NeuroImage, 82, 77-86. https://doi.org/10.1016/j.neuroimage.2013.05.090
Deoni, S., Dean, D., Joelson, S., O'Regan, J., & Schneider, N. (2018). Early nutrition influences developmental myelination and cognition in infants and young children. NeuroImage, 178, 649-659. https://doi.org/10.1016/j.neuroimage.2017.12.056
Dubois, J., Dehaene-Lambertz, G., Kulikova, S., Poupon, C., Hüppi, P. S., & Hertz-Pannier, L. (2014). The early development of brain white matter: A review of imaging studies in fetuses, newborns and infants. Neuroscience, 276, 48-71. https://doi.org/10.1016/j.neuroscience.2013.12.044
Dubois, J., Hertz-Pannier, L., Dehaene-Lambertz, G., Cointepas, Y., & Le Bihan, D. (2006). Assessment of the early organization and maturation of infants’ cerebral white matter fiber bundles: A feasibility study using quantitative diffusion tensor imaging and tractography. NeuroImage, 30(4), 1121-1132. https://doi.org/10.1016/j.neuroimage.2005.11.022
Dunlop, S. A., Quinlivan, J. A., Beazley, L. D., & Newnham, J. P. (1997). Repeated prenatal corticosteroids delay myelination in the ovine central nervous system. The Journal of Maternal-Fetal Medicine, 6(6), 309-313. https://doi.org/10.1002/(SICI)1520-6661(199711/12)6:6<309::AID-MFM1>3.0.CO;2-S
Finnie, J. W. (2012). Comparative approach to understanding traumatic injury in the immature, postnatal brain of domestic animals. Australian Veterinary Journal, 90(8), 301-307. https://doi.org/10.1111/j.1751-0813.2012.00955.x
Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J.-P., Frith, C. D., & Frackowiak R. S. J. (1994). Statistical parametric maps in functional imaging: A general linear approach. Human brain mapping, 2(4), 189-210. https://onlinelibrary.wiley.com/doi/10.1002/hbm.460020402
Fleming, A. S., Gonzalez, A., Lovic, V., Rees, S., & Melo, A. (2002). Mothering begets mothering: The transmission of behavior and its neurobiology across generations. Pharmacology Biochemistry and Behavior, 73(1), 61-75. https://doi.org/10.1016/S0091-3057(02)00793-1
Flood, T. F., Bhatt, P. R., Jensen, A., Maloney, J. A., Stence, N. V., & Mirsky, D. M. (2019). Age-dependent signal intensity changes in the structurally normal pediatric brain on unenhanced T1-weighted MR imaging. American Journal of Neuroradiology, 40(11), 1824-1828. https://doi.org/10.3174/ajnr.A6254
Gaudin, S., Chaillou, E., Wycke, M.-A., Cornilleau, F., Moussu, C., Calandreau, L., Lainé, A.-L., & Nowak, R. (2018). All bonds are not alike: A psychoendocrine evaluation of infant attachment. Developmental Psychobiology, 60(1), 90-103. https://doi.org/10.1002/dev.21552
Geeraert, B. L., Lebel, R. M., & Lebel, C. (2019). A multiparametric analysis of white matter maturation during late childhood and adolescence. Human Brain Mapping, 40(15), 4345-4356. https://doi.org/10.1002/hbm.24706
Giedd, J. N., & Rapoport, J. L. (2010). Structural MRI of pediatric brain development: what have we learned and where are we going? Neuron, 67(5), 728-734. https://doi.org/10.1016/j.neuron.2010.08.040
Grahn, J. A., Parkinson, J. A., & Owen, A. M. (2008). The cognitive functions of the caudate nucleus. Progress in Neurobiology, 86(3), 141-155. https://doi.org/10.1016/j.pneurobio.2008.09.004
Guesdon, V., Nowak, R., Meurisse, M., Boivin, X., Cornilleau, F., Chaillou, E., & Lévy, F. (2016). Behavioral evidence of heterospecific bonding between the lamb and the human caregiver and mapping of associated brain network. Psychoneuroendocrinology, 71, 159-169. https://doi.org/10.1016/j.psyneuen.2016.05.020
Hasboun, D., Chantôme, M., Zouaoui, A., Sahel, M., Baulac, M., Marsault, C., Duyme, M., & Dormont, D. (1996). Évaluation du volume cérébral: Reproductibilité et précision d'une technique 3D IRM. Bulletins et Mémoires de la Société d'anthropologie de Paris, 8(1), 43-56. https://doi.org/10.3406/bmsap.1996.2427
Hernández-Castellano, L. E., Suárez-Trujillo, A., Martell-Jaizme, D., Cugno, G., Argüello, A., & Castro, N. (2015). The effect of colostrum period management on BW and immune system in lambs: From birth to weaning. Animal, 9(10), 1672-1679. https://doi.org/10.1017/S175173111500110X
Huang, W. L., Harper, C. G., Evans, S. F., Newnham, J. P., & Dunlop, S. A. (2001). Repeated prenatal corticosteroid administration delays myelination of the corpus callosum in fetal sheep. International Journal of Developmental Neuroscience, 19(4), 415-425. https://doi.org/10.1016/S0736-5748(01)00026-0
Hüppi, P. S., & Dubois, J. (2006). Diffusion tensor imaging of brain development. Seminars in Fetal and Neonatal Medicine, 11(6), 489-497. https://doi.org/10.1016/j.siny.2006.07.006
Isaacs, E. B., Gadian, D. G., Sabatini, S., Chong, W. K., Quinn, B. T., Fischl, B. R., & Lucas, A. (2008). The effect of early human diet on caudate volumes and IQ. Pediatric Research, 63(3), 308-314. https://doi.org/10.1203/PDR.0b013e318163a271
Jenkinson, M., Beckmann, C. F., Behrens, T. E. J., Woolrich, M. W., & Smith, S. M. (2012). FSL. NeuroImage, 62(2), 782-790. https://doi.org/10.1016/j.neuroimage.2011.09.015
Jevtovic-Todorovic, V. (2005). General anesthetics and the developing brain: Friends or foes? Journal of Neurosurgical Anesthesiology, 17(4), 204-206. https://doi.org/10.1097/01.ana.0000178111.26972.16
Jezzard, P. & Balaban R. S. (1995). Correction for geometric distorsion in echo planar images from B0 field variation. Magnetic Resonance in Medicine 34(1), 65-73. https://doi.org/10.1002/mrm.1910340111
Khan, A., & Ahmad, R. (1997). Maternal immunoglobulins transfer and neonatal lamb mortality-A review. Pakistan Veterinary Journal, 17(4), 161-167.
Latham, N. R., & Mason, G. J. (2008). Maternal deprivation and the development of stereotypic behaviour. Applied Animal Behaviour Science, 110(1-2), 84-108. https://doi.org/10.1016/j.applanim.2007.03.026
Li, G., Wang, L., Yap, P., Wang, F., Wu, Z., Meng, Y., Dong, P., Kim, J., Shi, F., Rekik, I., Lin, W., & Shen, D., (2019). Computational neuroanatomy of baby brains: A review. NeuroImage, 185, 906-925. https://doi.org/10.1016/j.neuroimage.2018.03.042
Ligout, S., & Porter, R. H. (2004). Effect of maternal presence on the development of social relationships among lambs. Applied Animal Behaviour Science, 88(1-2), 47-59. https://doi.org/10.1016/j.applanim.2004.03.010
Liu, Z., Neuringer, M., Erdman, J. W., Kuchan, M. J., Renner, L., Johnson, E. E., Wang, X., & Kroenke, C. D. (2019). The effects of breastfeeding versus formula-feeding on cerebral cortex maturation in infant rhesus macaques. NeuroImage, 184, 372-385. https://doi.org/10.1016/j.neuroimage.2018.09.015
Luby, J., Belden, A., Botteron, K., Marrus, N., Harms, M. P., Babb, C., Nishino, T., & Barch, D. (2013). The effects of poverty on childhood brain development: The mediating effect of caregiving and stressful life events. JAMA Pediatrics, 167(12), 1135. https://doi.org/10.1001/jamapediatrics.2013.3139
Malhotra, A., Sepehrizadeh, T., Dhollander, T., Wright, D., Castillo-Melendez, M., Sutherland, A. E., Pham, Y., Ditchfield, M., Polglase, G. R., de Veer, M., Jenkin, G., Pannek, K., Shishegar, R., & Miller, S. L. (2019). Advanced MRI analysis to detect white matter brain injury in growth restricted newborn lambs. NeuroImage: Clinical, 24, 101991. https://doi.org/10.1016/j.nicl.2019.101991
Manjón, J. V., Coupé, P., Martí-Bonmatí, L., Collins, D. L., & Robles, M. (2010). Adaptive non-local means denoising of MR images with spatially varying noise levels: Spatially adaptive nonlocal denoising. Journal of Magnetic Resonance Imaging, 31(1), 192-203. https://doi.org/10.1002/jmri.22003
McIntosh, G. H., Baghurst, K. I., Potter, B. J., & Hetzel, B. S. (1979). Foetal brain development in the sheep. Neuropathology and Applied Neurobiology, 5(2), 103-114. https://doi.org/10.1111/j.1365-2990.1979.tb00664.x
Menant, O., Andersson, F., Zelena, D., & Chaillou, E. (2016). The benefits of magnetic resonance imaging methods to extend the knowledge of the anatomical organisation of the periaqueductal gray in mammals. Journal of Chemical Neuroanatomy, 77, 110-120. https://doi.org/10.1016/j.jchemneu.2016.06.003
Mukherjee, P., Miller, J. H., Shimony, J. S., Philip, J. V., Nehra, D., Snyder, A. Z., Conturo, T. E., Neil, J. J., & McKinstry, R. C. (2002). Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. American Journal of Neuroradiology, 23(9), 1445-1456.
Napolitano, F. (2003). Lambs prevented from suckling their mothers display behavioral, immune and endocrine disturbances. Physiology & Behavior, 78(1), 81-89. https://doi.org/10.1016/S0031-9384(02)00892-2
Napolitano, F., Cifuni, G. F., Pacelli, C., Riviezzi, A. M., & Girolami, A. (2002). Effect of artificial rearing on lamb welfare and meat quality. Meat Science, 60(3), 307-315. https://doi.org/10.1016/S0309-1740(01)00140-1
Napolitano, F., Marino, V., De Rosa, G., Capparelli, R., & Bordi, A. (1995). Influence of artificial rearing on behavioral and immune response of lambs. Applied Animal Behaviour Science, 45(3-4), 245-253. https://doi.org/10.1016/0168-1591(95)00637-8
Nowak, R., Keller, M., & Lévy, F. (2011). Mother-young relationships in sheep: A model for a multidisciplinary approach of the study of attachment in mammals. Journal of Neuroendocrinology, 23(11), 1042-1053. https://doi.org/10.1111/j.1365-2826.2011.02205.x
Nowak, R., Murphy, T. M., Lindsay, D. R., Alster, P., Andersson, R., & S-Moberg, K. U. (1997). Development of a preferential relationship with the mother by the newborn lamb: Importance of the sucking activity. Physiology and Behavior, 62(4), 681-688. https://doi.org/10.1016/s0031-9384(97)00079-6
Nowak, R., & Poindron, P. (2006). From birth to colostrum: Early steps leading to lamb survival. Reproduction Nutrition Development, 46(4), 431-446. https://doi.org/10.1051/rnd:2006023
Olutoye, O. A., Lazar, D. A., Akinkuotu, A. C., Adesina, A., & Olutoye, O. O. (2015). Potential of the ovine brain as a model for anesthesia-induced neuroapoptosis. Pediatric Surgery International, 31(9), 865-869. https://doi.org/10.1007/s00383-015-3751-7
O'Muircheartaigh, J., Dean, D. C., Ginestet, C. E., Walker, L., Waskiewicz, N., Lehman, K., Dirks, H., Piryatinsky, I., & Deoni, S. C. L. (2014). White matter development and early cognition in babies and toddlers: White matter development and early cognition. Human Brain Mapping, 35(9), 4475-4487. https://doi.org/10.1002/hbm.22488
Patterson, D. S., Sweasey, D., & Hebert, C. N. (1971). Changes occurring in the chemical composition of the central nervous system during foetal and post-natal development of the sheep. Journal of Neurochemistry, 18(11), 2027-2040. https://doi.org/10.1111/j.1471-4159.1971.tb05062.x
Petit, B., Boissy, A., Zanella, A., Chaillou, E., Andanson, S., Bes, S., Lévy, F., & Coulon, M. (2015). Stress during pregnancy alters dendritic spine density and gene expression in the brain of new-born lambs. Behavioural Brain Research, 291, 155-163. https://doi.org/10.1016/j.bbr.2015.05.025
Polkowska, J., & Wańkowska, M. (2010). Effects of maternal deprivation on the somatotrophic axis and neuropeptide Y in the hypothalamus and pituitary in female lambs. The histomorphometric study. Folia Histochemica et Cytobiologica, 48(2), 299-305. https://doi.org/10.2478/v10042-010-0024-0
Pryce, C. R. (1995). Determinants of motherhood in human and nonhuman primates. A biosocial model. Motherhood in Humans and Nonhuman Primates, 1-15. https://doi.org/10.1159/000424482
Saint-Dizier, H., Lévy, F., & Ferreira, G. (2007). Influence of the mother in the development of flavored-food preference in lambs. Developmental Psychobiology, 49(1), 98-106. https://doi.org/10.1002/dev.20197
Sánchez, M. M., Hearn, E. F., Do, D., Rilling, J. K., & Herndon, J. G. (1998). Differential rearing affects corpus callosum size and cognitive function of rhesus monkeys. Brain Research, 812(1-2), 38-49. https://doi.org/10.1016/S0006-8993(98)00857-9
Schack-Nielsen, L., & Michaelsen, K. F. (2007). Advances in our understanding of the biology of human milk and its effects on the offspring. The Journal of Nutrition, 137(2), 503S-510S. https://doi.org/10.1093/jn/137.2.503S
Scott, J. A., Grayson, D., Fletcher, E., Lee, A., Bauman, M. D., Schumann, C. M., Buonocore, M. H., & Amaral, D. G. (2016). Longitudinal analysis of the developing rhesus monkey brain using magnetic resonance imaging: Birth to adulthood. Brain Structure and Function, 221(5), 2847-2871. https://doi.org/10.1007/s00429-015-1076-x
Serag, A., Aljabar, P., Counsell, S., Boardman, J., Hajnal, J. V., & Rueckert, D. (2011). Tracking developmental changes in subcortical structures of the preterm brain using multi-modal MRI. 2011 IEEE International Symposium on Biomedical Imaging: From nano to macro, 349-352. https://doi.org/10.1109/ISBI.2011.5872421
Sevi, A., Napolitano, F., Casamassima, D., Annicchiarico, G., Quarantelli, T., & De Paola, R. (1999). Effect of gradual transition from maternal to reconstituted milk on behavioural, endocrine and immune responses of lambs. Applied Animal Behaviour Science, 64(4), 249-259. https://doi.org/10.1016/S0168-1591(99)00042-8
Shroff, M. M., Soares-Fernandes, J. P., Whyte, H., & Raybaud, C. (2010). MR Imaging for diagnostic evaluation of encephalopathy in the newborn. RadioGraphics, 30(3), 763-780. https://doi.org/10.1148/rg.303095126
Singh, D. K., Ling, E.-A., & Kaur, C. (2018). Hypoxia and myelination deficits in the developing brain. International Journal of Developmental Neuroscience: The Official Journal of the International Society for Developmental Neuroscience, 70, 3-11. https://doi.org/10.1016/j.ijdevneu.2018.06.012
Spinelli, S., Chefer, S., Suomi, S. J., Higley, J. D., Barr, C. S., & Stein, E. (2009). Early-life stress induces long-term morphologic changes in primate brain. Archives of General Psychiatry, 66(6), 658-665. https://doi.org/10.1001/archgenpsychiatry.2009.52
Suomi, S. J. (1997). Early determinants of behaviour: Evidence from primate studies. British Medical Bulletin, 53(1), 170-184. https://doi.org/10.1093/oxfordjournals.bmb.a011598
Tang, A. C., Reeb-Sutherland, B. C., Romeo, R. D., & McEwen, B. S. (2014). On the causes of early life experience effects: Evaluating the role of mom. Frontiers in Neuroendocrinology, 35(2), 245-251. https://doi.org/10.1016/j.yfrne.2013.11.002
Thorhallsdottir, A. G., Provenza, F. D., & Balph, D. F. (1990). Ability of lambs to learn about novel foods while observing or participating with social models. Applied Animal Behaviour Science, 25(1-2), 25-33. https://doi.org/10.1016/0168-1591(90)90066-M
Turley, S. D., Burns, D. K., & Rosenfeld, C. R. (1996). Brain does not utilize low density lipoprotein-cholesterol during fetal and neonatal development in the sheep. Journal of Lipid Research, 37, 1953-1961.
Wańkowska, M., Starzec, A., Counis, R., & Polkowska, J. (2006). Effects of maternal deprivation on the adrenocorticotrophic and gonadotrophic axes in the hypothalamo-pituitary unit of preweanling female sheep: The histomorphometric approach. Journal of Chemical Neuroanatomy, 31(1), 51-58. https://doi.org/10.1016/j.jchemneu.2005.08.006
Westlye, L. T., Walhovd, K. B., Dale, A. M., Bjørnerud, A., Due-Tønnessen, P., Engvig, A., Grydeland, H., Tamnes, C. K., Østby, Y., & Fjell, A. M. (2010). Differentiating maturational and aging-related changes of the cerebral cortex by use of thickness and signal intensity. NeuroImage, 52(1), 172-185. https://doi.org/10.1016/j.neuroimage.2010.03.056
White, N. M. (2009). Some highlights of research on the effects of caudate nucleus lesions over the past 200 years. Behavioural Brain Research, 199(1), 3-23. https://doi.org/10.1016/j.bbr.2008.12.003
Williamson, J. M., & Lyons, D. A. (2018). Myelin dynamics throughout life: an ever-changing landscape? Frontiers in Cellular Neuroscience, 12, 424. https://doi.org/10.3389/fncel.2018.00424
Yushkevich, P. A., Piven, J., Hazlett, H. C., Smith, R. G., Ho, S., Gee, J. C., & Gerig, G. (2006). User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. NeuroImage, 31(3), 1116-1128. https://doi.org/10.1016/j.neuroimage.2006.01.015
Zelena, D., Menant, O., Andersson, F., & Chaillou, E. (2018). Periaqueductal gray and emotions: The complexity of the problem and the light at the end of the tunnel, the magnetic resonance imaging. Endocrine Regulations, 52(4), 222-238. https://doi.org/10.2478/enr-2018-0027
Zhang, Y., Brady, M., & Smith, S. (2001). Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Transactions on Medical Imaging, 20(1), 45-57. https://doi.org/10.1109/42.906424

Auteurs

Scott A Love (SA)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Emmanuelle Haslin (E)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Manon Bellardie (M)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Frédéric Andersson (F)

UMR 1253, iBrain, Université de Tours, Inserm, Tours, France.

Laurent Barantin (L)

UMR 1253, iBrain, Université de Tours, Inserm, Tours, France.

Isabelle Filipiak (I)

UMR 1253, iBrain, Université de Tours, Inserm, Tours, France.

Hans Adriaensen (H)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Csilla L Fazekas (CL)

Institute of Experimental Medicine, Budapest, Hungary.
János Szentágothai Doctoral School of Neurosciences, Semmelweis University, Budapest, Hungary.

Laurène Leroy (L)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Dóra Zelena (D)

Institute of Experimental Medicine, Budapest, Hungary.
Centre for Neuroscience, Szentágothai Research Centre, Institute of Physiology, Medical School, University of Pécs, Pécs, Hungary.

Mélody Morisse (M)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Frédéric Elleboudt (F)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Christian Moussu (C)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Frédéric Lévy (F)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Raymond Nowak (R)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

Elodie Chaillou (E)

CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France.

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