The role of functional magnetic resonance imaging in the study of brain development, injury, and recovery in the newborn.

Development of brain functions and the structural-functional correlates of brain injury remain difficult to evaluate in the young infant. Thus, new noninvasive methods capable of early functional diagnosis are needed. This review describes the use of functional magnetic resonance imaging (fMRI) for studying localization of brain function in the developing brain when standard clinical investigations are not available or conclusive. This promising neuroimaging technique has been successfully used in healthy newborns and in newborns with brain injury using different paradigms, including passive visual, somato-sensorial, and auditory stimulation. We summarize the major findings of previous fMRI studies in young infants, describe ongoing methodological challenges, and propose exciting future developments in using resting-state protocols and functional connectivity techniques to assist in evaluating early life brain function and its recovery from injury.

[1]  B. Bernal,et al.  Visual functional magnetic resonance imaging in patients with Sturge-Weber syndrome. , 2004, Pediatric neurology.

[2]  Karl J. Friston,et al.  Degeneracy and cognitive anatomy , 2002, Trends in Cognitive Sciences.

[3]  J. Lurito,et al.  Multiple sclerosis: low-frequency temporal blood oxygen level-dependent fluctuations indicate reduced functional connectivity initial results. , 2002, Radiology.

[4]  S. Rombouts,et al.  Consistent resting-state networks across healthy subjects , 2006, Proceedings of the National Academy of Sciences.

[5]  Todd B. Parrish,et al.  Altered Effective Connectivity within the Language Network in Primary Progressive Aphasia , 2007, The Journal of Neuroscience.

[6]  F. Duffy,et al.  Early experience alters brain function and structure. , 2004, Pediatrics.

[7]  Todd B. Parrish,et al.  Hemodynamic response function in patients with stroke-induced aphasia: Implications for fMRI data analysis , 2007, NeuroImage.

[8]  Stefano F. Cappa,et al.  Bilingual aphasia and language control: A follow-up fMRI and intrinsic connectivity study , 2009, Brain and Language.

[9]  Augustinus A. M. Hart,et al.  Functional MRI of visual cortex in sedated 18 month-old infants with or without periventricular leukomalacia. , 2001 .

[10]  J. Démonet,et al.  Functional MRI Follow-Up Study of Language Processes in Healthy Subjects and During Recovery in a Case of Aphasia , 2004, Stroke.

[11]  Marlene C. Richter,et al.  The shape of the fMRI BOLD response in children and adults changes systematically with age , 2003, NeuroImage.

[12]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[13]  Ravi S. Menon,et al.  On the characteristics of functional magnetic resonance imaging of the brain. , 1998, Annual review of biophysics and biomolecular structure.

[14]  Elizabeth Redcay,et al.  Functional neuroimaging of speech perception during a pivotal period in language acquisition. , 2008, Developmental science.

[15]  Vesa Kiviniemi,et al.  Endogenous brain fluctuations and diagnostic imaging , 2008, Human brain mapping.

[16]  L. Stokowski.  ENSURING SAFETY FOR INFANTS UNDERGOING MAGNETIC RESONANCE IMAGING , 2005, Advances in neonatal care : official journal of the National Association of Neonatal Nurses.

[17]  Michael B. Miller,et al.  Individual variability in brain activations associated with episodic retrieval: a role for large-scale databases. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[18]  Peter Fransson,et al.  Resting-state networks in the infant brain , 2007, Proceedings of the National Academy of Sciences.

[19]  Kaoru Sakatani,et al.  Comparison of blood-oxygen-level-dependent functional magnetic resonance imaging and near-infrared spectroscopy recording during functional brain activation in patients with stroke and brain tumors. , 2007, Journal of biomedical optics.

[20]  R. Lazar,et al.  Variability in recovery from aphasia , 2008, Current neurology and neuroscience reports.

[21]  B. J. Casey,et al.  Functional MRI in Pediatrics , 2000 .

[22]  Thomas E. Nichols,et al.  Controlling the familywise error rate in functional neuroimaging: a comparative review , 2003, Statistical methods in medical research.

[23]  Juergen Hennig,et al.  Visual Processing in Infants and Children Studied Using Functional MRI , 1999, Pediatric Research.

[24]  J. Daly,et al.  Answering the Call: The Influence of Neuroimaging and Electrophysiological Evidence on Rehabilitation , 2007, Physical Therapy.

[25]  V. Calhoun,et al.  Aberrant "default mode" functional connectivity in schizophrenia. , 2007, The American journal of psychiatry.

[26]  F. Baylis,et al.  Ethical Challenges and Interpretive Difficulties with Non-Clinical Applications of Pediatric fMRI , 2009, The American journal of bioethics : AJOB.

[27]  S. H. A. Chen,et al.  Ethical issues in the clinical application of fMRI: Factors affecting the validity and interpretation of activations , 2002, Brain and Cognition.

[28]  R. Bluhm,et al.  Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. , 2007, Schizophrenia bulletin.

[29]  K. Joseph,et al.  Trends in Preterm Birth and Perinatal Mortality Among Singletons: United States, 1989 Through 2000 , 2005, Obstetrics and gynecology.

[30]  Marvin D. Nelson,et al.  Somatosensory lateralization in the newborn brain , 2006, NeuroImage.

[31]  Yufeng Wang,et al.  Discriminative Analysis of Brain Function at Resting-State for Attention-Deficit/Hyperactivity Disorder , 2005, MICCAI.

[32]  E Rostrup,et al.  Functional magnetic resonance imaging of the normal and abnormal visual system in early life. , 2000, Neuropediatrics.

[33]  Takamitsu Yamamoto,et al.  Evoked-cerebral blood oxygenation changes in false-negative activations in BOLD contrast functional MRI of patients with brain tumors , 2004, NeuroImage.

[34]  A M Dale,et al.  Event-related functional MRI: past, present, and future. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Mario Dzemidzic,et al.  Resting state corticolimbic connectivity abnormalities in unmedicated bipolar disorder and unipolar depression , 2009, Psychiatry Research: Neuroimaging.

[36]  Tianzi Jiang,et al.  Enhanced resting-state brain activities in ADHD patients: A fMRI study , 2008, Brain and Development.

[37]  N. Logothetis.  What we can do and what we cannot do with fMRI , 2008, Nature.

[38]  Dana Byrd,et al.  Special considerations for functional magnetic resonance imaging of pediatric populations , 2006, Journal of magnetic resonance imaging : JMRI.

[39]  J K Smith,et al.  Functional Connectivity MR Imaging Reveals Cortical Functional Connectivity in the Developing Brain , 2008, American Journal of Neuroradiology.

[40]  Asaid Khateb,et al.  Group analysis and the subject factor in functional magnetic resonance imaging: Analysis of fifty right‐handed healthy subjects in a semantic language task , 2008, Human brain mapping.

[41]  William Davis Gaillard,et al.  Developmental Aspects of Pediatric fMRI: Considerations for Image Acquisition, Analysis, and Interpretation , 2001, NeuroImage.

[42]  Bharat Biswal,et al.  Slow vasomotor fluctuation in fMRI of anesthetized child brain , 2000, Magnetic resonance in medicine.

[43]  Nikos K Logothetis,et al.  On the nature of the BOLD fMRI contrast mechanism. , 2004, Magnetic resonance imaging.

[44]  G. Breart,et al.  Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): a longitudinal cohort study , 2008, The Lancet.

[45]  Balázs Gulyás,et al.  Four facets of a single brain: behaviour, cerebral blood flow/metabolism, neuronal activity and neurotransmitter dynamics , 2003, Neuroreport.

[46]  Peter Fransson,et al.  Spontaneous Brain Activity in the Newborn Brain During Natural Sleep—An fMRI Study in Infants Born at Full Term , 2009, Pediatric Research.

[47]  James R. Booth,et al.  Effective brain connectivity in children with reading difficulties during phonological processing , 2008, Brain and Language.

[48]  Zimmerman Ra.  Pediatric cerebrovascular disease. , 2000 .

[49]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[50]  Kevin G. Guise,et al.  Functional connectivity of the sensorimotor area in naturally sleeping infants , 2008, Brain Research.

[51]  Hirohiko Kimura,et al.  Age-Dependent Change in Metabolic Response to Photic Stimulation of the Primary Visual Cortex in Infants: Functional Magnetic Resonance Imaging Study , 2002, Journal of computer assisted tomography.

[52]  Irene Tracey,et al.  Pharmacological fMRI: A New Tool for Drug Development in Humans , 2001 .

[53]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[54]  J C Gore,et al.  Neonatal auditory activation detected by functional magnetic resonance imaging. , 2001, Magnetic resonance imaging.

[55]  Petra S. Huppi,et al.  Combination of event-related fMRI and diffusion tensor imaging in an infant with perinatal stroke , 2004, NeuroImage.

[56]  J. Hirsch,et al.  Brain Mapping in Sedated Infants and Young Children with Passive-Functional Magnetic Resonance Imaging , 1999, Pediatric Neurosurgery.

[57]  F. Gonzalez-Lima,et al.  Structural equation modeling and its application to network analysis in functional brain imaging , 1994 .

[58]  S. Petersen,et al.  Control networks in paediatric Tourette syndrome show immature and anomalous patterns of functional connectivity , 2008, Brain : a journal of neurology.

[59]  Elizabeth Redcay,et al.  Deviant Functional Magnetic Resonance Imaging Patterns of Brain Activity to Speech in 2–3-Year-Old Children with Autism Spectrum Disorder , 2008, Biological Psychiatry.

[60]  Madison M Berl,et al.  Pediatric Functional Magnetic Resonance Imaging (fMRI): Issues and Applications , 2008, Journal of child neurology.

[61]  J. Dubois,et al.  Diffusion tensor imaging of brain development. , 2006, Seminars in fetal & neonatal medicine.

[62]  Scott K Holland,et al.  Practical Aspects of Conducting Large-Scale Functional Magnetic Resonance Imaging Studies in Children , 2002, Journal of child neurology.

[63]  R. Poldrack,et al.  Pediatric Functional Magnetic Resonance Imaging: Progress and Challenges , 2002, Topics in magnetic resonance imaging : TMRI.

[64]  F. Shellock,et al.  MR procedures: biologic effects, safety, and patient care. , 2004, Radiology.

[65]  B. Bernal,et al.  Brain activation in sedated children: auditory and visual functional MR imaging. , 2001, Radiology.

[66]  J Hennig,et al.  Effect of pentobarbital on visual processing in man , 2000, Human brain mapping.

[67]  Ashok Panigrahy,et al.  Advances in Magnetic Resonance Neuroimaging Techniques in the Evaluation of Neonatal Encephalopathy , 2007, Topics in magnetic resonance imaging : TMRI.

[68]  François Lazeyras,et al.  Visual recovery after perinatal stroke evidenced by functional and diffusion MRI: case report , 2005, BMC neurology.

[69]  Functional MRI in pediatric neurobehavioral disorders. , 2005, International review of neurobiology.

[70]  Karl J. Friston,et al.  Detecting subject-specific activations using fuzzy clustering , 2007, NeuroImage.

[71]  S Y Bookheimer,et al.  Methodological issues in pediatric neuroimaging. , 2000, Mental retardation and developmental disabilities research reviews.

[72]  M. Seghier,et al.  Functional MRI of the newborn. , 2006, Seminars in fetal & neonatal medicine.

[73]  H FaroScotto,et al.  Functional MRI : basic principles and clinical applications , 2006 .

[74]  S. Dehaene,et al.  Functional Neuroimaging of Speech Perception in Infants , 2002, Science.

[75]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[76]  P. Matthews,et al.  Neuroimaging: Applications of fMRI in translational medicine and clinical practice , 2006, Nature Reviews Neuroscience.

[77]  Y Yonekura,et al.  A rapid brain metabolic change in infants detected by fMRI , 1997, Neuroreport.

[78]  Tianzi Jiang,et al.  Regional coherence changes in the early stages of Alzheimer’s disease: A combined structural and resting-state functional MRI study , 2007, NeuroImage.

[79]  Rainer Goebel,et al.  Mapping directed influence over the brain using Granger causality and fMRI , 2005, NeuroImage.

[80]  Arie Bos,et al.  Functional Magnetic Resonance Imaging of the Sensorimotor System in Preterm Infants , 2009, Pediatrics.

[81]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[82]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[83]  Ferdinand Binkofski,et al.  Modulation of the BOLD-response in early recovery from sensorimotor stroke , 2004, Neurology.

[84]  Liang Wang,et al.  Altered small‐world brain functional networks in children with attention‐deficit/hyperactivity disorder , 2009, Human brain mapping.

[85]  Egill Rostrup,et al.  Visual Activation in Infants and Young Children Studied by Functional Magnetic Resonance Imaging , 1998, Pediatric Research.

[86]  Abraham Z. Snyder,et al.  A method for using blocked and event-related fMRI data to study “resting state” functional connectivity , 2007, NeuroImage.

[87]  M. P. van den Heuvel,et al.  Normalized Cut Group Clustering of Resting-State fMRI Data , 2008, PloS one.

[88]  Martijn P. van den Heuvel,et al.  FUNCTIONAL CONNECTIVITY IN SCHIZOPHRENIA , 2010, Schizophrenia Research.

[89]  D. W Loring,et al.  Now you see it, now you don’t: statistical and methodological considerations in fMRI , 2002, Epilepsy & Behavior.

[90]  V. Schmithorst,et al.  Functional Magnetic Resonance Imaging in Pediatrics , 2003, Neuropediatrics.

[91]  M. Ernst,et al.  The Role of Functional Neuroimaging in Pediatric Brain Injury , 2006, Pediatrics.