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Mitra, A.; Snyder, A.Z.; Tagliazucchi, E.; Laufs, H.; Elison, J.; Emerson, R.W.; Shen, M.D.; Wolff, J.J.; Botteron, K.N.; Dager, S.; Estes, A.M.; Evans, A.C.; Gerig, G.; Hazlett, H.C.; Paterson, S.J.; Schultz, R.T.; Styner, M.A.; Zwaigenbaum, L. (...) Raichle, M. "Resting-state fMRI in sleeping infants more closely resembles adult sleep than adult wakefulness" (2017) PLoS ONE. 12(11)
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Abstract:

Resting state functional magnetic resonance imaging (rs-fMRI) in infants enables important studies of functional brain organization early in human development. However, rs-fMRI in infants has universally been obtained during sleep to reduce participant motion artifact, raising the question of whether differences in functional organization between awake adults and sleeping infants that are commonly attributed to development may instead derive, at least in part, from sleep. This question is especially important as rs-fMRI differences in adult wake vs. sleep are well documented. To investigate this question, we compared functional connectivity and BOLD signal propagation patterns in 6, 12, and 24 month old sleeping infants with patterns in adult wakefulness and non-REM sleep. We find that important functional connectivity features seen during infant sleep closely resemble those seen during adult sleep, including reduced default mode network functional connectivity. However, we also find differences between infant and adult sleep, especially in thalamic BOLD signal propagation patterns. These findings highlight the importance of considering sleep state when drawing developmental inferences in infant rs-fMRI. © 2017 Mitra et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Registro:

Documento: Artículo
Título:Resting-state fMRI in sleeping infants more closely resembles adult sleep than adult wakefulness
Autor:Mitra, A.; Snyder, A.Z.; Tagliazucchi, E.; Laufs, H.; Elison, J.; Emerson, R.W.; Shen, M.D.; Wolff, J.J.; Botteron, K.N.; Dager, S.; Estes, A.M.; Evans, A.C.; Gerig, G.; Hazlett, H.C.; Paterson, S.J.; Schultz, R.T.; Styner, M.A.; Zwaigenbaum, L.; Chappell, C.; Estes, A.; Shaw, D.; Botteron, K.; McKinstry, R.; Constantino, J.; Pruett, J.; Schultz, R.; Paterson, S.; Collins, D.L.; Pike, G.B.; Fonov, V.; Kostopoulos, P.; Das, S.; Styner, M.; Gu, H.; Schlaggar, B.L.; Piven, J.; Pruett, J.R., Jr.; Raichle, M.
Filiación:Department of Radiology, Washington University School of Medicine, Saint Louis, MO, United States
Department of Neurology, Washington University School of Medicine, Saint Louis, MO, United States
Departamento de Fisica, Universidad de Buenos Aires, Buenos Aires, Argentina
Department of Neurology, Christian-Albrechts-University, Kiel, Germany
Institute of Child Development, University of Minnesota, Minneapolis, MN, United States
Department of Psychiatry, University of North Carolina, Chapel Hill, NC, United States
Department of Radiology, University of Washington, Seattle, WA, United States
Department of Psychology, University of Washington, Seattle, WA, United States
Montreal Neurological Institute, McGill University, Montreal, QC, Canada
Department of Psychiatry, New York University, New York, NY, United States
Department of Pediatrics, University of Pennsylvania, Philadelphia, PA, United States
Department of Pediatrics, University of Alberta, Edmonton, AB, Canada
Department of Psychiatry, Washington University School of Medicine, Saint Louis, MO, United States
University of North Carolina, United States
IBIS Network PI, United States
University of Washington, United States
Washington University, United States
Children’s Hospital of Philadelphia, United States
University of Alberta, Canada
University of Minnesota, United States
Data Coordinating Center, Montreal Neurological Institute, Canada
Image Processing Core, New York University, United States
University of North Carolina, United States
Statistical Analysis Core, United States
Palabras clave:BOLD signal; child; controlled study; default mode network; drawing; female; functional connectivity; functional magnetic resonance imaging; human; human experiment; infant; male; nonREM sleep; preschool child; rest; thalamus; wakefulness; adult; anatomy and histology; brain; connectome; electroencephalography; growth, development and aging; nuclear magnetic resonance imaging; physiology; principal component analysis; sleep; statistics and numerical data; wakefulness; Adult; Brain; Child, Preschool; Connectome; Electroencephalography; Humans; Infant; Magnetic Resonance Imaging; Principal Component Analysis; Sleep; Wakefulness
Año:2017
Volumen:12
Número:11
DOI: http://dx.doi.org/10.1371/journal.pone.0188122
Título revista:PLoS ONE
Título revista abreviado:PLoS ONE
ISSN:19326203
CODEN:POLNC
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_19326203_v12_n11_p_Mitra

Referencias:

  • Lin, W., Zhu, Q., Gao, W., Chen, Y., Toh, C.H., Styner, M., Functional connectivity MR imaging reveals cortical functional connectivity in the developing brain (2008) AJNR Am J Neuroradiol, 29 (10), pp. 1883-1889. , https://doi.org/10.3174/ajnr.A1256, PMID: 18784212; PubMed Central PMCID: PMC2583167
  • Fransson, P., Skiold, B., Engstrom, M., Hallberg, B., Mosskin, M., Aden, U., Spontaneous brain activity in the newborn brain during natural sleep—an fMRI study in infants born at full term (2009) Pediatr Res, 66 (3), pp. 301-305. , https://doi.org/10.1203/PDR.0b013e3181b1bd84, PMID: 19531974
  • Pruett, J.R., Jr., Kandala, S., Hoertel, S., Snyder, A.Z., Elison, J.T., Nishino, T., Accurate age classification of 6 and 12 month-old infants based on resting-state functional connectivity magnetic resonance imaging data (2015) Dev Cogn Neurosci, 12, pp. 123-133. , https://doi.org/10.1016/j.dcn.2015.01.003, PMID: 25704288; PubMed Central PMCID: PMC4385423
  • Gao, W., Zhu, H., Giovanello, K.S., Smith, J.K., Shen, D., Gilmore, J.H., Evidence on the emergence of the brain’s default network from 2-week-old to 2-year-old healthy pediatric subjects (2009) Proc Natl Acad Sci U S A, 106 (16), pp. 6790-6795. , https://doi.org/10.1073/pnas.0811221106, PMID: 19351894; PubMed Central PMCID: PMC2672537
  • Smyser, C.D., Snyder, A.Z., Shimony, J.S., Mitra, A., Inder, T.E., Neil, J.J., Resting-State Network Complexity and Magnitude Are Reduced in Prematurely Born Infants (2014) Cereb Cortex, , https://doi.org/10.1093/cercor/bhu251, PMID: 25331596
  • Gao, W., Lin, W., Grewen, K., Gilmore, J.H., Functional Connectivity of the Infant Human Brain: Plastic and Modifiable (2016) Neuroscientist, , https://doi.org/10.1177/1073858416635986, PMID: 26929236
  • Fransson, P., Skiold, B., Horsch, S., Nordell, A., Blennow, M., Lagercrantz, H., Resting-state networks in the infant brain (2007) Proc Natl Acad Sci U S A, 104 (39), pp. 15531-15536. , https://doi.org/10.1073/pnas.0704380104, Epub 2007/09/20. doi: 0704380104 [pii] PMID: 17878310; PubMed Central PMCID: PMC2000516
  • Wylie, K.P., Rojas, D.C., Ross, R.G., Hunter, S.K., Maharajh, K., Cornier, M.A., Reduced brain resting-state network specificity in infants compared with adults (2014) Neuropsychiatric Disease and Treatment, 10, pp. 1349-1359. , https://doi.org/10.2147/NDT.S63773, PMID: 25092980; PubMed Central PMCID: PMC4114919
  • Horovitz, S.G., Braun, A.R., Carr, W.S., Picchioni, D., Balkin, T.J., Fukunaga, M., Decoupling of the brain’s default mode network during deep sleep (2009) Proc Natl Acad Sci U S A, 106 (27), pp. 11376-11381. , https://doi.org/10.1073/pnas.0901435106, Epub 2009/06/25. doi: 0901435106 [pii] PMID: 19549821; PubMed Central PMCID: PMC2708777
  • Mitra, A., Snyder, A.Z., Tagliazucchi, E., Laufs, H., Raichle, M.E., Propagated infra-slow intrinsic brain activity reorganizes across wake and slow wave sleep (2015) eLife, 4. , https://doi.org/10.7554/eLife.10781, PMID: 26551562
  • Picchioni, D., Duyn, J.H., Horovitz, S.G., Sleep and the functional connectome (2013) Neuroimage, 80, pp. 387-396. , https://doi.org/10.1016/j.neuroimage.2013.05.067, PMID: 23707592; PubMed Central PMCID: PMC3733088
  • Samann, P.G., Wehrle, R., Hoehn, D., Spoormaker, V.I., Peters, H., Tully, C., Development of the brain’s default mode network from wakefulness to slow wave sleep (2011) Cereb Cortex, 21 (9), pp. 2082-2093. , https://doi.org/10.1093/cercor/bhq295, Epub 2011/02/19. doi: bhq295 [pii] PMID: 21330468
  • Larson-Prior, L.J., Zempel, J.M., Nolan, T.S., Prior, F.W., Snyder, A.Z., Raichle, M.E., Cortical network functional connectivity in the descent to sleep (2009) Proc Natl Acad Sci U S A, 106 (11), pp. 4489-4494. , https://doi.org/10.1073/pnas.0900924106, Epub 2009/03/04. doi: 0900924106 [pii] PMID: 19255447; PubMed Central PMCID: PMC2657465
  • Mitra, A., Snyder, A.Z., Blazey, T., Raichle, M.E., Lag threads organize the brain’s intrinsic activity (2015) Proc Natl Acad Sci U S A, 112 (17), pp. E2235-E2244. , https://doi.org/10.1073/pnas.1503960112, PMID: 25825720; PubMed Central PMCID: PMC4418865
  • Mitra, A., Snyder, A.Z., Hacker, C.D., Raichle, M.E., Lag structure in resting-state fMRI (2014) J Neurophysiol, 111 (11), pp. 2374-2391. , https://doi.org/10.1152/jn.00804.2013, PMID: 24598530; PubMed Central PMCID: PMC4097876
  • Mitra, A., Raichle, M.E., How networks communicate: Propagation patterns in spontaneous brain activity (2016) Philos Trans R Soc Lond B Biol Sci, 371, p. 1705. , https://doi.org/10.1098/rstb.2015.0546, PMID: 27574315; PubMed Central PMCID: PMC5003863
  • Fox, M.D., Raichle, M.E., Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging (2007) Nat Rev Neurosci, 8 (9), pp. 700-711. , https://doi.org/10.1038/nrn2201, Epub 2007/08/21. doi: nrn2201 [pii] PMID: 17704812
  • Mitra, A., Snyder, A.Z., Hacker, C.D., Pahwa, M., Tagliazucchi, E., Laufs, H., Human cortical-hippocampal dialogue in wake and slow-wave sleep (2016) Proc Natl Acad Sci U S A, , https://doi.org/10.1073/pnas.1607289113, PMID: 27791089
  • Tagliazucchi, E., Von Wegner, F., Morzelewski, A., Brodbeck, V., Jahnke, K., Laufs, H., Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep (2013) Proc Natl Acad Sci U S A, 110 (38), pp. 15419-15424. , https://doi.org/10.1073/pnas.1312848110, PMID: 24003146; PubMed Central PMCID: PMC3780893
  • Estes, A., Zwaigenbaum, L., Gu, H., St John, T., Paterson, S., Elison, J.T., Behavioral, cognitive, and adaptive development in infants with autism spectrum disorder in the first 2 years of life (2015) Journal of Neu-Rodevelopmental Disorders, 7 (1), p. 24. , https://doi.org/10.1186/s11689-015-9117-6, PMID: 26203305; PubMed Central PMCID: PMC4511527
  • Lord, C., Risi, S., Lambrecht, L., Cook, E.H., Jr., Leventhal, B.L., DiLavore, P.C., The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism (2000) J Autism Dev Disord, 30 (3), pp. 205-223. , PMID: 11055457
  • Power, J.D., Mitra, A., Laumann, T.O., Snyder, A.Z., Schlaggar, B.L., Petersen, S.E., Methods to detect, characterize, and remove motion artifact in resting state fMRI (2014) Neuroimage, 84, pp. 320-341. , https://doi.org/10.1016/j.neuroimage.2013.08.048, Epub 2013/09/03. PMID: 23994314; PubMed Central PMCID: PMC3849338
  • Smyser, C.D., Inder, T.E., Shimony, J.S., Hill, J.E., Degnan, A.J., Snyder, A.Z., Longitudinal analysis of neural network development in preterm infants (2010) Cereb Cortex, 20 (12), pp. 2852-2862. , https://doi.org/10.1093/cercor/bhq035, Epub 2010/03/20. doi: bhq035 [pii] PMID: 20237243; PubMed Central PMCID: PMC2978240
  • Allen, P.J., Polizzi, G., Krakow, K., Fish, D.R., Lemieux, L., Identification of EEG events in the MR scanner: The problem of pulse artifact and a method for its subtraction (1998) Neuroimage, 8 (3), pp. 229-239. , https://doi.org/10.1006/nimg.1998.0361, PMID: 9758737
  • Iber, C., (2007) The AASM Manual for The Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications, , American Academy of Sleep Medicine
  • Shulman, G.L., Pope, D.L., Astafiev, S.V., McAvoy, M.P., Snyder, A.Z., Corbetta, M., Right hemisphere dominance during spatial selective attention and target detection occurs outside the dorsal frontoparietal network (2010) J Neurosci, 30 (10), pp. 3640-3651. , https://doi.org/10.1523/JNEUROSCI.4085-09.2010, Epub 2010/03/12. doi: 30/10/3640 [pii] PMID: 20219998; PubMed Central PMCID: PMC2872555
  • Ojemann, J.G., Akbudak, E., Snyder, A.Z., McKinstry, R.C., Raichle, M.E., Conturo, T.E., Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts (1997) Neuroimage, 6 (3), pp. 156-167. , https://doi.org/10.1006/nimg.1997.0289, Epub 1997/11/05. PMID: 9344820
  • Hallquist, M.N., Hwang, K., Luna, B., The nuisance of nuisance regression: Spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity (2013) Neuroimage, 82, pp. 208-225. , https://doi.org/10.1016/j.neuroimage.2013.05.116, Epub 2013/06/12. PMID: 23747457; PubMed Central PMCID: PMC3759585
  • Fox, M.D., Zhang, D., Snyder, A.Z., Raichle, M.E., The global signal and observed anticorrelated resting state brain networks (2009) Journal of Neurophysiology, 101 (6), pp. 3270-3283. , https://doi.org/10.1152/jn.90777.2008, Epub 2009/04/03. PMID: 19339462; PubMed Central PMCID: PMC2694109
  • Murphy, K., Fox, M.D., Towards a consensus regarding global signal regression for resting state functional connectivity MRI (2016) Neuroimage, , Epub 2016/11/27
  • Fonov, V., Evans, A.C., Botteron, K., Almli, C.R., McKinstry, R.C., Collins, D.L., Unbiased average age-appropriate atlases for pediatric studies (2011) Neuroimage, 54 (1), pp. 313-327. , https://doi.org/10.1016/j.neuroimage.2010.07.033, Epub 2010/07/27. PMID: 20656036; PubMed Central PMCID: PMC2962759
  • Jenkinson, M., Beckmann, C.F., Behrens, T.E., Woolrich, M.W., Smith, S.M., (2012) Fsl. Neuroimage, 62 (2), pp. 782-790. , https://doi.org/10.1016/j.neuroimage.2011.09.015, Epub 2011/10/08. PMID: 21979382
  • Gholipour, A., Kehtarnavaz, N., Gopinath, K., Briggs, R., Panahi, I., Average field map image template for Echo-Planar image analysis (2008) Conference Proceedings: Annual International Conference of The IEEE Engineering in Medicine and Biology Society IEEE Engineering in Medicine and Biology Society Conference, 2008, pp. 94-97. , https://doi.org/10.1109/IEMBS.2008.4649099, Epub 2009/01/24. PMID: 19162602
  • Hacker, C.D., Laumann, T.O., Szrama, N.P., Baldassarre, A., Snyder, A.Z., Leuthardt, E.C., Resting state network estimation in individual subjects (2013) Neuroimage, 82 C, pp. 616-633. , https://doi.org/10.1016/j.neuroimage.2013.05.108, Epub 2013/06/06. doi: PMID: 23735260
  • Schneider, G., Havenith, M.N., Nikolic, D., Spatiotemporal structure in large neuronal networks detected from cross-correlation (2006) Neural Comput, 18 (10), pp. 2387-2413. , https://doi.org/10.1162/neco.2006.18.10.2387, Epub 2006/08/16. PMID: 16907631
  • Nikolic, D., Non-parametric detection of temporal order across pairwise measurements of time delays (2007) J Comput Neurosci, 22 (1), pp. 5-19. , https://doi.org/10.1007/s10827-006-9441-7, Epub 2006/09/26. PMID: 16998643
  • Margulies, D.S., Ghosh, S.S., Goulas, A., Falkiewicz, M., Huntenburg, J.M., Langs, G., Situating the default-mode network along a principal gradient of macroscale cortical organization (2016) Proc Natl Acad Sci U S A, 113 (44), pp. 12574-12579. , https://doi.org/10.1073/pnas.1608282113, PMID: 27791099; PubMed Central PMCID: PMC5098630
  • Hagne, I., Development of the sleep EEG in normal infants during the first year of life (1972) Acta Paediatrica, 61 (S232), pp. 25-53
  • Eisermann, M., Kaminska, A., Moutard, M.L., Soufflet, C., Plouin, P., Normal EEG in childhood: From neonates to adolescents (2013) Neurophysiologie Clinique = Clinical Neurophysiology, 43 (1), pp. 35-65. , https://doi.org/10.1016/j.neucli.2012.09.091, Epub 2013/01/08. PMID: 23290174
  • Roffwarg, H.P., Muzio, J.N., Dement, W.C., Ontogenetic development of the human sleep-dream cycle (1966) Science, 152 (3722), pp. 604-619. , https://doi.org/10.1126/science.152.3722.604, PMID: 17779492
  • Carskadon, M.A., Dement, W.C., Normal human sleep: An overview (2000) Principles and Practice of Sleep Medicine, 4, pp. 13-23
  • Braun, A.R., Balkin, T.J., Wesenten, N.J., Carson, R.E., Varga, M., Baldwin, P., Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study (1997) Brain, 120, pp. 1173-1197. , PMID: 9236630
  • Chugani, H.T., Phelps, M.E., Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography (1986) Science, 231 (4740), pp. 840-843. , Epub 1986/02/21. PMID: 3945811
  • Conel, J.R., (1939) The Postnatal Development of The Human Cerebral Cortex, , Cambridge, MA: Harvard University Press
  • Friedrichs-Maeder, C.L., Griffa, A., Schneider, J., Huppi, P.S., Truttmann, A., Hagmann, P., Exploring the role of white matter connectivity in cortex maturation (2017) PLoS One, 12 (5). , https://doi.org/10.1371/journal.pone.0177466, Epub 2017/05/26. PMID: 28545040; PubMed Central PMCID: PMC5435226
  • Lee, W., Morgan, B.R., Shroff, M.M., Sled, J.G., Taylor, M.J., The development of regional functional connectivity in preterm infants into early childhood (2013) Neuroradiology, 55, pp. 105-111. , https://doi.org/10.1007/s00234-013-1232-z, Epub 2013/07/25. PMID: 23881450
  • Doria, V., Beckmann, C.F., Arichi, T., Merchant, N., Groppo, M., Turkheimer, F.E., Emergence of resting state networks in the preterm human brain (2010) Proc Natl Acad Sci U S A, 107 (46), pp. 20015-20020. , https://doi.org/10.1073/pnas.1007921107, Epub 2010/11/03. doi: 1007921107 [pii] PMID: 21041625; PubMed Central PMCID: PMC2993415
  • Smyser, C.D., Dosenbach, N.U., Smyser, T.A., Snyder, A.Z., Rogers, C.E., Inder, T.E., Prediction of brain maturity in infants using machine-learning algorithms (2016) Neuroimage, 136, pp. 1-9. , https://doi.org/10.1016/j.neuroimage.2016.05.029, Epub 2016/05/18. PMID: 27179605; PubMed Central PMCID: PMC4914443
  • Gao, W., Gilmore, J.H., Shen, D., Smith, J.K., Zhu, H., Lin, W., The synchronization within and interaction between the default and dorsal attention networks in early infancy (2013) Cereb Cortex, 23 (3), pp. 594-603. , https://doi.org/10.1093/cercor/bhs043, Epub 2012/03/01. PMID: 22368080; PubMed Central PMCID: PMC3563337
  • Power, J.D., Mitra, A., Laumann, T.O., Snyder, A.Z., Schlaggar, B.L., Petersen, S.E., Methods to detect, characterize, and remove motion artifact in resting state fMRI (2013) Neuroimage, 84 C, pp. 320-341. , https://doi.org/10.1016/j.neuroimage.2013.08.048, Epub 2013/09/03. doi: PMID: 23994314
  • Power, J.D., Plitt, M., Laumann, T.O., Martin, A., Sources and implications of whole-brain fMRI signals in humans (2016) Neuroimage

Citas:

---------- APA ----------
Mitra, A., Snyder, A.Z., Tagliazucchi, E., Laufs, H., Elison, J., Emerson, R.W., Shen, M.D.,..., Raichle, M. (2017) . Resting-state fMRI in sleeping infants more closely resembles adult sleep than adult wakefulness. PLoS ONE, 12(11).
http://dx.doi.org/10.1371/journal.pone.0188122
---------- CHICAGO ----------
Mitra, A., Snyder, A.Z., Tagliazucchi, E., Laufs, H., Elison, J., Emerson, R.W., et al. "Resting-state fMRI in sleeping infants more closely resembles adult sleep than adult wakefulness" . PLoS ONE 12, no. 11 (2017).
http://dx.doi.org/10.1371/journal.pone.0188122
---------- MLA ----------
Mitra, A., Snyder, A.Z., Tagliazucchi, E., Laufs, H., Elison, J., Emerson, R.W., et al. "Resting-state fMRI in sleeping infants more closely resembles adult sleep than adult wakefulness" . PLoS ONE, vol. 12, no. 11, 2017.
http://dx.doi.org/10.1371/journal.pone.0188122
---------- VANCOUVER ----------
Mitra, A., Snyder, A.Z., Tagliazucchi, E., Laufs, H., Elison, J., Emerson, R.W., et al. Resting-state fMRI in sleeping infants more closely resembles adult sleep than adult wakefulness. PLoS ONE. 2017;12(11).
http://dx.doi.org/10.1371/journal.pone.0188122