Prefrontal Hemodynamics in Toddlers at Rest: A Pilot Study of Developmental Variability

Afrouz A Anderson, Elizabeth Smith, Fatima A Chowdhry, Audrey Thurm, Emma Condy, Lauren Swineford, Stacy S Manwaring, Franck Amyot, Dennis Matthews, Amir H Gandjbakhche, Afrouz A Anderson, Elizabeth Smith, Fatima A Chowdhry, Audrey Thurm, Emma Condy, Lauren Swineford, Stacy S Manwaring, Franck Amyot, Dennis Matthews, Amir H Gandjbakhche

Abstract

Functional near infrared spectroscopy (fNIRS) is a non-invasive functional neuroimaging modality. Although, it is amenable to use in infants and young children, there is a lack of fNIRS research within the toddler age range. In this study, we used fNIRS to measure cerebral hemodynamics in the prefrontal cortex (PFC) in 18-36 months old toddlers (n = 29) as part of a longitudinal study that enrolled typically-developing toddlers as well as those "at risk" for language and other delays based on presence of early language delays. In these toddlers, we explored two hemodynamic response indices during periods of rest during which time audiovisual children's programming was presented. First, we investigate Lateralization Index, based on differences in oxy-hemoglobin saturation from left and right prefrontal cortex. Then, we measure oxygenation variability (OV) index, based on variability in oxygen saturation at frequencies attributed to cerebral autoregulation. Preliminary findings show that lower cognitive (including language) abilities are associated with fNIRS measures of both lower OV index and more extreme Lateralization index values. These preliminary findings show the feasibility of using fNIRS in toddlers, including those at risk for developmental delay, and lay the groundwork for future studies.

Keywords: Near-infrared spectroscopy; autoregulation; cognitive development; hemodynamics; toddler neuroimaging.

Figures

Figure 1
Figure 1
Schematic of fNIRS sensor with four sources and 10 detectors (16 source-detector pairs).
Figure 2
Figure 2
Correlation between OV index values combined across Left and Right prefrontal cortex and Composite-DQ across all toddlers exhibiting trend of higher OV index in toddlers with higher Composite-DQ.
Figure 3
Figure 3
Correlation between Composite DQ and Laterality Index (based on percent difference between left and right activation) for each subject: negative values indicate right lateralization while positive values show left lateralization. Higher values in the positive and negative direction indicate the greater activation in left or right PFC, respectively.
Figure 4
Figure 4
Correlation between Absloute values of Laterlization Index and Composite-DQ indicating higher differences between left and right PFC activation in subjects with lower Composite-DQ.

References

    1. Amyot F., Zimmermann T., Riley J., Kainerstorfer J. M., Chernomordik V., Mooshagian E., et al. . (2012). Normative database of judgment of complexity task with functional near infrared spectroscopy–application for TBI. Neuroimage 60, 879–883. 10.1016/j.neuroimage.2012.01.104
    1. Anderson A. A., Smith E., Chernomordik V., Ardeshirpour Y., Chowdhry F., Thurm A., et al. . (2014). Prefrontal cortex hemodynamics and age: a pilot study using functional near infrared spectroscopy in children. Front. Neurosci. 8:393. 10.3389/fnins.2014.00393
    1. Aslin R. N., Mehler J. (2005). Near-infrared spectroscopy for functional studies of brain activity in human infants: promise, prospects, and challenges. J. Biomed. Opt. 10:11009. 10.1117/1.1854672
    1. Ayaz H. (2010). Functional Near Infrared Spectroscopy based Brain Computer Interface. Ph.D. thesis, Drexel University, Philadelphia, PA.
    1. Ayaz H., Izzetoglu M., Shewokis P. A., Onaral B. (2010). Sliding-window motion artifact rejection for functional near-infrared spectroscopy. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2010, 6567–6570. 10.1109/iembs.2010.5627113
    1. Baird A. A., Kagan J., Gaudette T., Walz K. A., Hershlag N., Boas D. A. (2002). Frontal lobe activation during object permanence: data from near-infrared spectroscopy. Neuroimage 16, 1120–1125. 10.1006/nimg.2002.1170
    1. Bassan H., Gauvreau K., Newburger J. W., Tsuji M., Limperopoulos C., Soul J. S., et al. . (2005). Identification of pressure passive cerebral perfusion and its mediators after infant cardiac surgery. Pediatr. Res. 57, 35–41. 10.1203/01.PDR.0000147576.84092.F9
    1. Bishop D. V., Holt G., Whitehouse A. J., Groen M. (2014). No population bias to left-hemisphere language in 4-year-olds with language impairment. Peer J. 2:e507 10.7717/peerj.507
    1. Boas D. A., Dale A. M., Franceschini M. A. (2004). Diffuse optical imaging of brain activation: approaches to optimizing image sensitivity, resolution, and accuracy. Neuroimage 23(Suppl. 1), S275–S288. 10.1016/j.neuroimage.2004.07.011
    1. Boashash B. (1992). Estimating and interpreting the instantaneous frequency of a signal. I. Fundamentals. Proc. IEEE 80, 520–538. 10.1109/5.135376
    1. Boschin E. A., Piekema C., Buckley M. J. (2015). Essential functions of primate frontopolar cortex in cognition. Proc. Natl. Acad. Sci. U.S.A. 112, E1020–E1027. 10.1073/pnas.1419649112
    1. Bryden P. J., Pryde K. M., Roy E. A. (2000). A performance measure of the degree of hand preference. Brain Cogn. 44, 402–414. 10.1006/brcg.1999.1201
    1. Burgess P. W., Wu H. C. (2013). Rostral prefrontal cortex (Brodmann area10): metacognition in the brain, in Principles of Frontal Lobe Function 2nd Edn., Stuss D. T., Knight R. T. (New York, NY: Oxford University Press; ), 524–534.
    1. Casey B. J., Jones R. M., Hare T. A. (2008). The adolescent brain. Ann. N. Y. Acad. Sci. 1124, 111–126. 10.1196/annals.1440.010
    1. Chernomordik V., Amyot F., Kenney K., Wassermann E., Diaz-Arrastia R., Gandjbakhche A. (2016). Abnormality of low frequency cerebral hemodynamics oscillations in TBI population. Brain Res. 1639, 194–199. 10.1016/j.brainres.2016.02.018
    1. Chiron C., Raynaud C., Maziere B., Zilbovicius M., Laflamme L., Masure M. C., et al. . (1992). Changes in regional cerebral blood flow during brain maturation in children and adolescents. J. Nucl. Med. 33, 696–703.
    1. Christoff k. (2009). Human thought and the lateral prefrontal cortex, in Neural Correlates of Thinking, eds Eduard Kraft D. B. G., Pöppel E. (Berlin Heidelberg: Springer Berlin Heidelberg; ), 219–252.
    1. Cipolla M. J. (2009). The Cerebral Circulation. San Rafael, CA: Morgan & Claypool Life Sciences.
    1. Cui X., Bray S., Reiss A. L. (2010). Functional near infrared spectroscopy (NIRS) signal improvement based on negative correlation between oxygenated and deoxygenated hemoglobin dynamics. Neuroimage 49, 3039–3046. 10.1016/j.neuroimage.2009.11.050
    1. Davidson M. C., Amso D., Anderson L. C., Diamond A. (2006). Development of cognitive control and executive functions from 4 to 13 years: evidence from manipulations of memory, inhibition, and task switching. Neuropsychologia 44, 2037–2078. 10.1016/j.neuropsychologia.2006.02.006
    1. Dumontheil I., Burgess P. W., Blakemore S. J. (2008). Development of rostral prefrontal cortex and cognitive and behavioural disorders. Dev. Med. Child Neurol. 50, 168–181. 10.1111/j.1469-8749.2008.02026.x
    1. Durston S., Davidson M. C., Tottenham N., Galvan A., Spicer J., Fossella J. A., et al. (2006). A shift from diffuse to focal cortical activity with development. Dev. Sci. 9, 1–8. 10.1111/j.1467-7687.2005.00454.x
    1. Elsabbagh M., Volein A., Holmboe K., Tucker L., Csibra G., Baron-Cohen S., et al. . (2009). Visual orienting in the early broader autism phenotype: disengagement and facilitation. J. Child Psychol. Psychiatry 50, 637–642. 10.1111/j.1469-7610.2008.02051.x
    1. Fekete T., Beacher F. D., Cha J., Rubin D., Mujica-Parodi L. R. (2014). Small-world network properties in prefrontal cortex correlate with predictors of psychopathology risk in young children: a NIRS study. Neuroimage 85(Pt 1), 345–353. 10.1016/j.neuroimage.2013.07.022
    1. Friedrich M., Friederici A. D. (2005). Semantic sentence processing reflected in the event-related potentials of one- and two-year-old children. Neuroreport 16, 1801–1804. 10.1097/01.wnr.0000185013.98821.62
    1. Funane T., Atsumori H., Katura T., Obata A. N., Sato H., Tanikawa Y., et al. . (2014). Quantitative evaluation of deep and shallow tissue layers' contribution to fNIRS signal using multi-distance optodes and independent component analysis. Neuroimage 85(Pt 1), 150–165. 10.1016/j.neuroimage.2013.02.026
    1. Gabard-Durnam L., Tierney A. L., Vogel-Farley V., Tager-Flusberg H., Nelson C. A. (2015). Alpha asymmetry in infants at risk for autism spectrum disorders. J. Autism Dev. Disord. 45, 473–480. 10.1007/s10803-013-1926-4
    1. Gomez D. M., Berent I., Benavides-Varela S., Bion R. A., Cattarossi L., Nespor M., et al. . (2014). Language universals at birth. Proc. Natl. Acad. Sci. U.S.A. 111, 5837–5841. 10.1073/pnas.1318261111
    1. Gratton E., Toronov V., Wolf U., Wolf M., Webb A. (2005). Measurement of brain activity by near-infrared light. J. Biomed. Opt. 10:11008. 10.1117/1.1854673
    1. Greve D., Goldenholz D., Kaskhedikar G., Polimeni J., Moran L., Schwartz C., et al. (2009). BOLD physiological noise reduction using spatio-spectral-temporal correlations with NIRS. in Paper presented at the Proceedings of the International Society of Magnetic Resonance in Medicine (Honolulu, HI: ).
    1. Hare T. A., Casey B. J. (2005). The neurobiology and development of cognitive and affective control. Cognition Brain Behav. 9, 273–286.
    1. Huppert T. J., Hoge R. D., Diamond S. G., Franceschini M. A., Boas D. A. (2006). A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans. Neuroimage 29, 368–382. 10.1016/j.neuroimage.2005.08.065
    1. Izzetoglu M., Bunce S. C., Izzetoglu K., Onaral B., Pourrezaei K. (2007). Functional brain imaging using near-infrared technology. IEEE Eng. Med. Biol. Mag. 26, 38–46. 10.1109/MEMB.2007.384094
    1. Jennings J. R., Kamarck T., Stewart C., Eddy M., Johnson P. (1992). Alternate cardiovascular baseline assessment techniques: vanilla or resting baseline. Psychophysiology 29, 742–750. 10.1111/j.1469-8986.1992.tb02052.x
    1. Jentschke S., Friederici A. D., Koelsch S. (2014). Neural correlates of music-syntactic processing in two-year old children. Dev. Cogn. Neurosci. 9, 200–208. 10.1016/j.dcn.2014.04.005
    1. Kainerstorfer J. M., Sassaroli A., Tgavalekos K. T., Fantini S. (2015). Cerebral autoregulation in the microvasculature measured with near-infrared spectroscopy. J. Cereb. Blood Flow Metab. 35, 959–966. 10.1038/jcbfm.2015.5
    1. Kawakubo Y., Kono T., Takizawa R., Kuwabara H., Ishii-Takahashi A., Kasai K. (2011). Developmental changes of prefrontal activation in humans: a near-infrared spectroscopy study of preschool children and adults. PLoS ONE 6:e25944. 10.1371/journal.pone.0025944
    1. Kawano M., Kanazawa T., Kikuyama H., Tsutsumi A., Kinoshita S., Kawabata Y., et al. . (2016). Correlation between frontal lobe oxy-hemoglobin and severity of depression assessed using near-infrared spectroscopy. J. Affect. Disord. 205, 154–158. 10.1016/j.jad.2016.07.013
    1. Keehn B., Wagner J. B., Tager-Flusberg H., Nelson C. A. (2013). Functional connectivity in the first year of life in infants at-risk for autism: a preliminary near-infrared spectroscopy study. Front. Hum. Neurosci. 7:444. 10.3389/fnhum.2013.00444
    1. Kikuchi M., Yoshimura Y., Shitamichi K., Ueno S., Hiraishi H., Munesue T., et al. . (2013). Anterior prefrontal hemodynamic connectivity in conscious 3- to 7-year-old children with typical development and autism spectrum disorder. PLoS ONE 8:e56087. 10.1371/journal.pone.0056087
    1. Kilroy E., Liu C. Y., Yan L., Kim Y. C., Dapretto M., Mendez M. F., et al. . (2011). Relationships between cerebral blood flow and IQ in typically developing children and adolescents. J. Cogn. Sci. 12, 151–170. 10.17791/jcs.2011.12.2.151
    1. Kreplin U., Fairclough S. H. (2013). Activation of the rostromedial prefrontal cortex during the experience of positive emotion in the context of esthetic experience. An fNIRS study. Front. Hum. Neurosci. 7:879. 10.3389/fnhum.2013.00879
    1. Kwon H., Reiss A. L., Menon V. (2002). Neural basis of protracted developmental changes in visuo-spatial working memory. Proc. Natl. Acad. Sci. U.S.A. 99, 13336–13341. 10.1073/pnas.162486399
    1. Lam J. M., Hsiang J. N., Poon W. S. (1997). Monitoring of autoregulation using laser Doppler flowmetry in patients with head injury. J. Neurosurg. 86, 438–445.
    1. Li Y., Grabell A. S., Wakschlag L. S., Huppert T. J., Perlman S. B. (in press). The neural substrates of cognitive flexibility are related to individual differences in preschool irritability: a fNIRS investigation. Dev. Cogn. Neurosci. 10.1016/j.dcn.2016.07.002
    1. Li Y., Yu D. (2016). Weak network efficiency in young children with Autism Spectrum Disorder: Evidence from a functional near-infrared spectroscopy study. Brain Cogn. 108, 47–55. 10.1016/j.bandc.2016.07.006
    1. Lindell A. K., Hudry K. (2013). Atypicalities in cortical structure, handedness, and functional lateralization for language in autism spectrum disorders. Neuropsychol. Rev., 23, 257–270. 10.1007/s11065-013-9234-5
    1. Liu X., Czosnyka M., Donnelly J., Budohoski K. P., Varsos G. V., Nasr N., et al. . (2015). Comparison of frequency and time domain methods of assessment of cerebral autoregulation in traumatic brain injury. J. Cereb. Blood Flow Metab. 35, 248–256. 10.1038/jcbfm.2014.192
    1. Lloyd-Fox S., Papademetriou M., Darboe M. K., Everdell N. L., Wegmuller R., Prentice A. M., et al. . (2014). Functional near infrared spectroscopy (fNIRS) to assess cognitive function in infants in rural Africa. Sci. Rep. 4:4740. 10.1038/srep04740
    1. Lloyd-Fox S., Wu R., Richards J. E., Elwell C. E., Johnson M. H. (2015). Cortical activation to action perception is associated with action production abilities in young infants. Cereb. Cortex, 25, 289–297. 10.1093/cercor/bht207.
    1. Mancini D. M., Bolinger L., Li H., Kendrick K., Chance B., Wilson J. R. (1994). Validation of near-infrared spectroscopy in humans. J. Appl. Physiol. 77, 2740–2747.
    1. May L., Byers-Heinlein K., Gervain J., Werker J. F. (2011). Language and the newborn brain: does prenatal language experience shape the neonate neural response to speech? Front. Psychol. 2:222. 10.3389/fpsyg.2011.00222
    1. Michelotti J., Charman T., Slonims V., Baird G. (2002). Follow-up of children with language delay and features of autism from preschool years to middle childhood. Dev. Med. Child Neurol. 44, 812–819. 10.1111/j.1469-8749.2002.tb00771.x
    1. Miller E. K., Cohen J. D. (2001). An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202. 10.1146/annurev.neuro.24.1.167
    1. Minagawa-Kawai Y., van der Lely H., Ramus F., Sato Y., Mazuka R., Dupoux E. (2011). Optical brain imaging reveals general auditory and language-specific processing in early infant development. Cereb. Cortex 21, 254–261. 10.1093/cercor/bhq082
    1. Muizelaar J. P., Marmarou A., Ward J. D., Kontos H. A., Choi S. C., Becker D. P., et al. . (1991). Adverse effects of prolonged hyperventilation in patients with severe head injury: a randomized clinical trial. J. Neurosurg. 75, 731–739.
    1. Mullen E. M. (ed.). (1995). Mullen Scales of Early Learning. Circle Pines, MN: American Guidance Service.
    1. Nakato E., Otsuka Y., Kanazawa S., Yamaguchi M. K., Watanabe S., Kakigi R. (2009). When do infants differentiate profile face from frontal face? A near-infrared spectroscopic study. Hum. Brain Mapp. 30, 462–472. 10.1002/hbm.20516
    1. Naseer N., Hong K. S. (2013). Classification of functional near-infrared spectroscopy signals corresponding to the right- and left-wrist motor imagery for development of a brain-computer interface. Neurosci. Lett. 553, 84–89. 10.1016/j.neulet.2013.08.021
    1. Nielsen J. A., Zielinski B. A., Fletcher P. T., Alexander A. L., Lange N., Bigler E. D., et al. . (2014). Abnormal lateralization of functional connectivity between language and default mode regions in autism. Mol. Autism 5:8. 10.1186/2040-2392-5-8
    1. Obrig H., Neufang M., Wenzel R., Kohl M., Steinbrink J., Einhaupl K., et al. . (2000). Spontaneous low frequency oscillations of cerebral hemodynamics and metabolism in human adults. Neuroimage 12, 623–639. 10.1006/nimg.2000.0657
    1. Oliver B., Dale P. S., Plomin R. (2004). Verbal and nonverbal predictors of early language problems: an analysis of twins in early childhood back to infancy. J. Child Lang. 31, 609–631. 10.1017/S0305000904006221
    1. Pena M., Maki A., Kovacic D., Dehaene-Lambertz G., Koizumi H., Bouquet F., et al. . (2003). Sounds and silence: an optical topography study of language recognition at birth. Proc. Natl. Acad. Sci. U.S.A. 100, 11702–11705. 10.1073/pnas.1934290100
    1. Perlman S. B., Huppert T. J., Luna B. (2016). Functional near-infrared spectroscopy evidence for development of prefrontal engagement in working memory in early through middle childhood. Cereb. Cortex 26, 2790–2799. 10.1093/cercor/bhv139
    1. Redcay E., Courchesne E. (2008). Deviant functional magnetic resonance imaging patterns of brain activity to speech in 2-3-year-old children with autism spectrum disorder. Biol. Psychiatry 64, 589–598. 10.1016/j.biopsych.2008.05.020
    1. Sassaroli A., deB Frederick B., Tong Y., Renshaw P. F., Fantini S. (2006). Spatially weighted BOLD signal for comparison of functional magnetic resonance imaging and near-infrared imaging of the brain. Neuroimage 33, 505–514. 10.1016/j.neuroimage.2006.07.006
    1. Sassaroli A., Pierro M., Bergethon P. R., Fantini S. (2012). Low-Frequency Spontaneous Oscillations of Cerebral Hemodynamics Investigated With Near-Infrared Spectroscopy: A Review. IEEE J. Selected Top. Q. Electron. 18, 1478–1492. 10.1109/JSTQE.2012.2183581
    1. Sato H., Yahata N., Funane T., Takizawa R., Katura T., Atsumori H., et al. . (2013). A NIRS-fMRI investigation of prefrontal cortex activity during a working memory task. Neuroimage 83, 158–173. 10.1016/j.neuroimage.2013.06.043
    1. Sato Y., Mori K., Koizumi T., Minagawa-Kawai Y., Tanaka A., Ozawa E., et al. . (2011). Functional lateralization of speech processing in adults and children who stutter. Front. Psychol. 2:70. 10.3389/fpsyg.2011.00070
    1. Sato Y., Sogabe Y., Mazuka R. (2010). Development of hemispheric specialization for lexical pitch-accent in Japanese infants. J. Cogn. Neurosci. 22, 2503–2513. 10.1162/jocn.2009.21377
    1. Scharoun S. M., Bryden P. J. (2014). Hand preference, performance abilities, and hand selection in children. Front. Psychol. 5:82. 10.3389/fpsyg.2014.00082
    1. Scholkmann F., Wolf M. (2013). General equation for the differential pathlength factor of the frontal human head depending on wavelength and age. J. Biomed. Opt. 18:105004. 10.1117/1.jbo.18.10.105004
    1. Schoning M., Hartig B. (1996). Age dependence of total cerebral blood flow volume from childhood to adulthood. J. Cereb. Blood Flow Metab. 16, 827–833. 10.1097/00004647-199609000-00007
    1. Silvestrini M., Pasqualetti P., Baruffaldi R., Bartolini M., Handouk Y., Matteis M., et al. . (2006). Cerebrovascular reactivity and cognitive decline in patients with Alzheimer disease. Stroke 37, 1010–1015. 10.1161/01.STR.0000206439.62025.97
    1. Strangman G., Boas D. A., Sutton J. P. (2002a). Non-invasive neuroimaging using near-infrared light. Biol. Psychiatry 52, 679–693. 10.1016/S0006-3223(02)01550-0
    1. Strangman G., Culver J. P., Thompson J. H., Boas D. A. (2002b). A quantitative comparison of simultaneous BOLD fMRI and NIRS recordings during functional brain activation. Neuroimage 17, 719–731. 10.1006/nimg.2002.1227
    1. Tamura R., Kitamura H., Endo T., Abe R., Someya T. (2012). Decreased leftward bias of prefrontal activity in autism spectrum disorder revealed by functional near-infrared spectroscopy. Psychiatry Res. 203, 237–240. 10.1016/j.pscychresns.2011.12.008
    1. Telkemeyer S., Rossi S., Koch S. P., Nierhaus T., Steinbrink J., Poeppel D., et al. . (2009). Sensitivity of newborn auditory cortex to the temporal structure of sounds. J. Neurosci. 29, 14726–14733. 10.1523/JNEUROSCI.1246-09.2009
    1. Themelis G., D'Arceuil H., Diamond S. G., Thaker S., Huppert T. J., Boas D. A., et al. . (2007). Near-infrared spectroscopy measurement of the pulsatile component of cerebral blood flow and volume from arterial oscillations. J. Biomed. Opt. 12:014033. 10.1117/1.2710250
    1. Tierney A. L., Gabard-Durnam L., Vogel-Farley V., Tager-Flusberg H., Nelson C. A. (2012). Developmental trajectories of resting EEG power: an endophenotype of autism spectrum disorder. PLoS ONE 7:e39127. 10.1371/journal.pone.0039127
    1. Tong Y., Lindsey K. P., deB Frederick B. (2011). Partitioning of physiological noise signals in the brain with concurrent near-infrared spectroscopy and fMRI. J. Cereb. Blood Flow Metab. 31, 2352–2362. 10.1038/jcbfm.2011.100
    1. Tsujimoto S. (2008). The prefrontal cortex: functional neural development during early childhood. Neuroscientist 14, 345–358. 10.1177/1073858408316002
    1. Turalska M., Latka M., Czosnyka M., Pierzchala K., West B. J. (2008). Generation of very low frequency cerebral blood flow fluctuations in humans. Acta Neurochirurgica Supplements 102, 43–47. 10.1007/978-3-211-85578-2_9
    1. Udomphorn Y., Armstead W. M., Vavilala M. S. (2008). Cerebral blood flow and autoregulation after pediatric traumatic brain injury. Pediatr. Neurol. 38, 225–234. 10.1016/j.pediatrneurol.2007.09.012
    1. Van Horn J. D., Berman K. F., Weinberger D. R. (1996). Functional lateralization of the prefrontal cortex during traditional frontal lobe tasks. Biol. Psychiatry 39, 389–399. 10.1016/0006-3223(95)00249-9
    1. Vavilala M. S., Lee L. A., Boddu K., Visco E., Newell D. W., Zimmerman J. J., et al. . (2004). Cerebral autoregulation in pediatric traumatic brain injury. Pediatr. Crit. Care Med. 5, 257–263. 10.1097/01.PCC.0000123545.69133.C3
    1. Whitehouse A. J., Bishop D. V. (2008). Cerebral dominance for language function in adults with specific language impairment or autism. Brain, 131(Pt 12), 3193–3200. 10.1093/brain/awn266
    1. Wilcox T., Stubbs J., Hirshkowitz A., Boas D. A. (2012). Functional activation of the infant cortex during object processing. Neuroimage 62, 1833–1840. 10.1016/j.neuroimage.2012.05.039
    1. Wong F. Y., Leung T. S., Austin T., Wilkinson M., Meek J. H., Wyatt J. S., et al. . (2008). Impaired autoregulation in preterm infants identified by using spatially resolved spectroscopy. Pediatrics, 121, e604–e611. 10.1542/peds.2007-1487
    1. Wood J. N., Grafman J. (2003). Human prefrontal cortex: processing and representational perspectives. Nat. Rev. Neurosci. 4, 139–147. 10.1038/nrn1033
    1. Xu M., Yang J., Siok W. T., Tan L. H. (2015). Atypical lateralization of phonological working memory in developmental dyslexia. J. Neurol. 33, 67–77. 10.1016/j.jneuroling.2014.07.004
    1. Yerys B. E., Jankowski K. F., Shook D., Rosenberger L. R., Barnes K. A., Berl M. M., et al. . (2009). The fMRI success rate of children and adolescents: typical development, epilepsy, attention deficit/hyperactivity disorder, and autism spectrum disorders. Hum. Brain Mapp. 30, 3426–3435. 10.1002/hbm.20767
    1. Yeung M. K., Sze S. L., Woo J., Kwok T., Shum D. H., Yu R., et al. . (2016). Altered Frontal lateralization underlies the category fluency deficits in older adults with mild cognitive impairment: a near-infrared spectroscopy study. Front. Aging Neurosci. 8:59. 10.3389/fnagi.2016.00059
    1. Yodh A., Boas D. (2003). Functional imaging with diffusing light. Biomed. Photonics Handbook 21, 21–45. 10.1201/9780203008997.ch21
    1. Yucel M. A., Selb J., Aasted C. M., Lin P. Y., Borsook D., Becerra L., et al. . (2016). Mayer waves reduce the accuracy of estimated hemodynamic response functions in functional near-infrared spectroscopy. Biomed. Opt. Express 7, 3078–3088. 10.1364/BOE.7.003078
    1. Yue Y., Yuan Y., Hou Z., Jiang W., Bai F., Zhang Z. (2013). Abnormal functional connectivity of amygdala in late-onset depression was associated with cognitive deficits. PLoS ONE 8:e75058. 10.1371/journal.pone.0075058
    1. Zhu H., Li J., Fan Y., Li X., Huang D., He S. (2015). Atypical prefrontal cortical responses to joint/non-joint attention in children with autism spectrum disorder (ASD): a functional near-infrared spectroscopy study. Biomed. Opt. Express 6, 690–701. 10.1364/BOE.6.000690

Source: PubMed

赞助者和合作者

医疗条件

药物干预

3
订阅