Neonatal hemodynamic response to visual cortex activity: high-density near-infrared spectroscopy study.

The neurodevelopmental outcome of neonatal intensive care unit (NICU) infants is a major clinical concern with many infants displaying neurobehavioral deficits in childhood. Functional neuroimaging may provide early recognition of neural deficits in high-risk infants. Near-infrared spectroscopy (NIRS) has the advantage of providing functional neuroimaging in infants at the bedside. However, limitations in traditional NIRS have included contamination from superficial vascular dynamics in the scalp. Furthermore, controversy exists over the nature of normal vascular, responses in infants. To address these issues, we extend the use of novel high-density NIRS arrays with multiple source-detector distances and a superficial signal regression technique to infants. Evaluations of healthy term-born infants within the first three days of life are performed without sedation using a visual stimulus. We find that the regression technique significantly improves brain activation signal quality. Furthermore, in six out of eight infants, both oxy- and total hemoglobin increases while deoxyhemoglobin decreases, suggesting that, at term, the neurovascular coupling in the visual cortex is similar to that found in healthy adults. These results demonstrate the feasibility of using high-density NIRS arrays in infants to improve signal quality through superficial signal regression, and provide a foundation for further development of high-density NIRS as a clinical tool.

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

[2]  M. D’Esposito,et al.  Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging , 2003, Nature Reviews Neuroscience.

[3]  J. Markham,et al.  Blind identification of evoked human brain activity with independent component analysis of optical data , 2009, Human brain mapping.

[4]  Takashi Kusaka,et al.  Noninvasive optical imaging in the visual cortex in young infants , 2004, Human brain mapping.

[5]  A. Dale,et al.  Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation. , 2003, Optics letters.

[6]  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.

[7]  A. Villringer,et al.  Beyond the Visible—Imaging the Human Brain with Light , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[8]  David A Boas,et al.  Assessment of Infant Brain Development With Frequency-Domain Near-Infrared Spectroscopy , 2007, Pediatric Research.

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

[10]  Y Yonekura,et al.  A milestone for normal development of the infantile brain detected by functional MRI , 2000, Neurology.

[11]  D. Delpy,et al.  Measurement of Cranial Optical Path Length as a Function of Age Using Phase Resolved Near Infrared Spectroscopy , 1994 .

[12]  Janette Atkinson,et al.  Regional Hemodynamic Responses to Visual Stimulation in Awake Infants , 1998, Pediatric Research.

[13]  David A. Boas,et al.  Factors affecting the accuracy of near-infrared spectroscopy concentration calculations for focal changes in oxygenation parameters , 2003, NeuroImage.

[14]  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.

[15]  D. G. Albrecht,et al.  Spikes versus BOLD: what does neuroimaging tell us about neuronal activity? , 2000, Nature Neuroscience.

[16]  K von Siebenthal,et al.  The effect of behavioural states on visual evoked responses in preterm and full-term newborns. , 1995, Neuropediatrics.

[17]  R. Poldrack,et al.  Can the cerebral metabolic rate of oxygen be estimated with near-infrared spectroscopy? , 2003, Physics in medicine and biology.

[18]  D. Boas,et al.  Diffuse optical tomography system to image brain activation with improved spatial resolution and validation with functional magnetic resonance imaging. , 2006, Applied optics.

[19]  Hellmuth Obrig,et al.  Separability and cross talk: optimizing dual wavelength combinations for near-infrared spectroscopy of the adult head , 2004, NeuroImage.

[20]  Saroj Saigal,et al.  An overview of mortality and sequelae of preterm birth from infancy to adulthood , 2008, The Lancet.

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

[22]  Robert J. Ogg,et al.  BOLD responses to visual stimulation in survivors of childhood cancer , 2005, NeuroImage.

[23]  G. Taga,et al.  Brain imaging in awake infants by near-infrared optical topography , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[24]  T. Loenneker,et al.  How depth of anesthesia influences the blood oxygenation level-dependent signal from the visual cortex of children. , 2006, AJNR. American journal of neuroradiology.

[25]  D. Delpy,et al.  Characterization of the near infrared absorption spectra of cytochrome aa3 and haemoglobin for the non-invasive monitoring of cerebral oxygenation. , 1988, Biochimica et biophysica acta.

[26]  A. Hart,et al.  Functional MRI of visual cortex in sedated 18 month‐old infants with or without periventricular leukomalacia , 2001, Developmental medicine and child neurology.

[27]  Norihiro Sadato,et al.  Difference in the metabolic response to photic stimulation of the lateral geniculate nucleus and the primary visual cortex of infants: a fMRI study , 2000, Neuroscience Research.

[28]  P. Apkarian Temporal frequency responsivity shows multiple maturational phases: State-dependent visual evoked potential luminance flicker fusion from birth to 9 months , 1993, Visual Neuroscience.

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

[30]  C. Iadecola Neurovascular regulation in the normal brain and in Alzheimer's disease , 2004, Nature Reviews Neuroscience.

[31]  M. Mintun,et al.  Brain work and brain imaging. , 2006, Annual review of neuroscience.

[32]  David A. Boas,et al.  Evidence that cerebral blood volume can provide brain activation maps with better spatial resolution than deoxygenated hemoglobin , 2005, NeuroImage.

[33]  M. Constantine-Paton,et al.  Development of hemodynamic responses and functional connectivity in rat somatosensory cortex , 2008, Nature Neuroscience.

[34]  Simon R. Arridge,et al.  Three-dimensional whole-head optical tomography of passive motor evoked responses in the neonate , 2006, NeuroImage.

[35]  Martin Wolf,et al.  Hemodynamic response to visual stimulation in newborn infants using functional near‐infrared spectroscopy , 2008, Human brain mapping.

[36]  Marvin D. Nelson,et al.  Functional MRI in neonates using neonatal head coil and MR compatible incubator , 2003, NeuroImage.

[37]  Fumitaka Homae,et al.  Functional activation in diverse regions of the developing brain of human infants , 2008, NeuroImage.

[38]  Y Hoshi,et al.  Visuospatial imagery is a fruitful strategy for the digit span backward task: a study with near-infrared optical tomography. , 2000, Brain research. Cognitive brain research.

[39]  A. Hielscher,et al.  Three-dimensional optical tomography of hemodynamics in the human head. , 2001, Optics express.

[40]  R. Saager,et al.  Direct characterization and removal of interfering absorption trends in two-layer turbid media. , 2005, Journal of the Optical Society of America. A, Optics, image science, and vision.

[41]  S Arridge,et al.  Measurement of optical path length for cerebral near-infrared spectroscopy in newborn infants. , 1990, Developmental neuroscience.

[42]  Arthur W. Toga,et al.  Temporal and Topographical Characterization of Language Cortices Using Intraoperative Optical Intrinsic Signals , 2000, NeuroImage.

[43]  E Rostrup,et al.  Visual cortex reactivity in sedated children examined with perfusion MRI (FAIR). , 2002, Magnetic resonance imaging.

[44]  A. Villringer,et al.  Illuminating the BOLD signal: combined fMRI-fNIRS studies. , 2006, Magnetic resonance imaging.

[45]  Martin Schweiger,et al.  Three-dimensional whole-head optical passive motor evoked responses in the tomography of neonate , 2006 .

[46]  L. Doyle,et al.  Preterm Birth 3 An overview of mortality and sequelae of preterm birth from infancy to adulthood , 2009 .

[47]  David A Boas,et al.  Increased Cerebral Blood Volume and Oxygen Consumption in Neonatal Brain Injury , 2009, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

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

[49]  Hamid Dehghani,et al.  Retinotopic mapping of adult human visual cortex with high-density diffuse optical tomography , 2007, Proceedings of the National Academy of Sciences.

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