Functional near infrared spectroscopy (fNIRS) to assess cognitive function in infants in rural Africa

Sarah Lloyd-Fox, M Papademetriou, M K Darboe, N L Everdell, R Wegmuller, A M Prentice, S E Moore, C E Elwell, Sarah Lloyd-Fox, M Papademetriou, M K Darboe, N L Everdell, R Wegmuller, A M Prentice, S E Moore, C E Elwell

Abstract

Cortical mapping of cognitive function during infancy is poorly understood in low-income countries due to the lack of transportable neuroimaging methods. We have successfully piloted functional near infrared spectroscopy (fNIRS) as a neuroimaging tool in rural Gambia. Four-to-eight month old infants watched videos of Gambian adults perform social movements, while haemodynamic responses were recorded using fNIRS. We found distinct regions of the posterior superior temporal and inferior frontal cortex that evidenced either visual-social activation or vocally selective activation (vocal > non-vocal). The patterns of selective cortical activation in Gambian infants replicated those observed within similar aged infants in the UK. These are the first reported data on the measurement of localized functional brain activity in young infants in Africa and demonstrate the potential that fNIRS offers for field-based neuroimaging research of cognitive function in resource-poor rural communities.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1. A photo timeline of the…
Figure 1. A photo timeline of the setup of the NIRS equipment and first infant to take part in the study at the MRC Field Station in Keneba.
Figure 2. An overview of the anatomical…
Figure 2. An overview of the anatomical location of the visual social responses and auditory vocally selective (vocal > non-vocal) responses in the current study in relation to three previous publications using the same stimuli.
The location of activation is similar across all four groups of 4–8 month old infants from the UK and the Gambia. Note that the Gambia data was measured from the right hemisphere only (figure designed by S. Lloyd-Fox).
Figure 3. The visual social stimuli (left…
Figure 3. The visual social stimuli (left panel), the location of the significant group haemodynamic responses (visual social > visual non-social) on an average five to six month old head (middle panel) and an example of the haemodynamic response to the visual social and visual non-social conditions for channel 12 (right panel).
The significant responses are illustrated in red (HbO2) and blue (HHb).
Figure 4. The group haemodynamic responses for…
Figure 4. The group haemodynamic responses for the three auditory contrasts: vocal vs silence (left panel), non-vocal vs silence (middle panel) and vocal > non-vocal (right panel) on an average five to six month old head.
The significant responses are illustrated in red (HbO2) and blue (HHb).
Figure 5. Illustrations of the procedure.
Figure 5. Illustrations of the procedure.
Upper panel: The experimental design showing the order and timing of stimulus presentation for the three conditions (visual-social, vocal and non-vocal). Lower panel: The array design showing the location of the channels (dashed circle), sources (star), detectors (full circle), 2 cm (dashed line) and 4.5 cm (dotted line) channels. The headgear was placed over the right hemisphere with the source optode between channel 4 and 7 centred above the pre-auricular point (T4 according to the 10–20 system).

References

    1. Blasi A. et al. Early Specialization for Voice and Emotion Processing in the Infant Brain. Curr. Biol. 21, 1220–1224 (2011).
    1. Dehaene-Lambertz G., Dehaene S. & Hertz-Pannier L. Functional neuroimaging of speech perception in infants. Science 298, 2013–2015 (2002).
    1. Huotilainen M. et al. Auditory magnetic responses of healthy newborns. Neuroreport 14, 1871–1875 (2003).
    1. Imada T. et al. Infant speech perception activates Broca's area: a developmental magnetoencephalography study. Neuroreport 17, 957–962 (2006).
    1. Tzourio-Mazoyer N. et al. Neural correlates of woman face processing by 2-month-old infants. Neuroimage 15, 454–461 (2002).
    1. Wolff J. J. et al. Differences in White Matter Fiber Tract Development Present From 6 to 24 Months in Infants With Autism. Am. J. Psychiatry 169, 580–600 (2012).
    1. Aslin R. N. & Mehler J. Near-infrared spectroscopy for functional studies of brain activity in human infants: promise, prospects, and challenges. J. Biomed. Opt. 10, 011009 (2005).
    1. Lloyd-Fox S., Blasi A. & Elwell C. E. Illuminating the developing brain: the past, present and future of functional near infrared spectroscopy. Neurosci. Biobehav. Rev. 34, 269–284 (2010).
    1. Fukui Y., Ajichi Y. & Okada E. Monte Carlo prediction of near-infrared light propagation in realistic adult and neonatal head models. Appl. Opt. 42, 2881–2887 (2003).
    1. Steinbrink J. et al. Illuminating the BOLD signal: combined fMRI-fNIRS studies. Magn. Reson. Imaging 24, 495–505 (2006).
    1. Sato H. et al. A NIRS–fMRI investigation of prefrontal cortex activity during a working memory task. Neuroimage 83, 158–173 (2013).
    1. Cristia A. et al. An Online Database of Infant Functional Near InfraRed Spectroscopy Studies: A Community-Augmented Systematic Review. PLoS ONE 8, e58906 (2013).
    1. Gervain J. et al. Near-infrared spectroscopy: A report from the McDonnell infant methodology consortium. Dev. Cogn. Neurosci. 1, 22–46 (2011).
    1. Wilcox T., Bortfeld H., Woods R., Wruck E. & Boas D. A. Using near-infrared spectroscopy to assess neural activation during object processing in infants. J. Biomed. Opt. 10, 011010–9 (2005).
    1. Watanabe H., Homae F., Nakano T. & Taga G. Functional activation in diverse regions of the developing brain of human infants. Neuroimage 43, 346–357 (2008).
    1. Grossmann T. et al. Early cortical specialization for face-to-face communication in human infants. Proc. Biol. Sci. 275, 2803–2811 (2008).
    1. Minagawa-Kawai Y. et al. Prefrontal activation associated with social attachment: facial-emotion recognition in mothers and infants. Cereb. Cortex 19, 284–292 (2009).
    1. Lloyd-Fox S., Wu R., Richards J. E., Elwell C. E. & Johnson M. H. Cortical Activation to Action Perception is Associated with Action Production Abilities in Young Infants. Cereb. Cortex (2013) 10.1093/cercor/bht207.
    1. Shimada S. & Hiraki K. Infant's brain responses to live and televised action. Neuroimage 32, 930–939 (2006).
    1. Otsuka Y. et al. Neural activation to upright and inverted faces in infants measured by near infrared spectroscopy. NeuroImage 34, 399–406 (2007).
    1. Fox S. E., Wagner J. B., Shrock C. L., Tager-Flusberg H. & Nelson C. A. Neural Processing of Facial Identity and Emotion in Infants at High-Risk for Autism Spectrum Disorders. Front. Hum. Neurosci. 7, 1–18 (2013).
    1. Lloyd-Fox S. et al. Reduced neural sensitivity to social stimuli in infants at risk for autism. Proc. R. Soc. B Biol. Sci. 280, 20123026 (2013).
    1. Minagawa-Kawai Y. et al. Cerebral laterality for phonemic and prosodic cue decoding in children with autism. Neuroreport 20, 1219–1224 (2009).
    1. Elsabbagh M. et al. Neural Correlates of Eye Gaze Processing in the Infant Broader Autism Phenotype. Biol. Psychiatry 65, 31–38 (2009).
    1. Elsabbagh M. et al. Infant Neural Sensitivity to Dynamic Eye Gaze Is Associated with Later Emerging Autism. Curr. Biol. 22, 338–342 (2012).
    1. Guiraud J. A. et al. Differential habituation to repeated sounds in infants at high risk for autism. Neuroreport 22, 845 (2011).
    1. Luyster R. J., Wagner J. B., Vogel-Farley V., Tager-Flusberg H. & Nelson C. A. Neural Correlates of Familiar and Unfamiliar Face Processing in Infants at Risk for Autism Spectrum Disorders. Brain Topogr. 24, 220–228 (2011).
    1. McCleery J. P., Akshoomoff N., Dobkins K. R. & Carver L. J. Atypical Face Versus Object Processing and Hemispheric Asymmetries in 10-Month-Old Infants at Risk for Autism. Biol. Psychiatry 66, 950–957 (2009).
    1. Tomalski P. et al. Socioeconomic status and functional brain development–associations in early infancy. Dev. Sci. 16, 676–687 (2013).
    1. UNICEF. Improving child nutrition: the achievable imperative for global progress. (2013).
    1. Victora C. G., Onis M., Hallal P. C., Blössner M. & Shrimpton R. Worldwide Timing of Growth Faltering: Revisiting Implications for Interventions. Pediatrics 125, e473–e480 (2010).
    1. Georgieff M. K. Nutrition and the developing brain: nutrient priorities and measurement. Am. J. Clin. Nutr. 85, 614S–620S (2007).
    1. Kretchmer N., Beard J. L. & Carlson S. The role of nutrition in the development of normal cognition. Am. J. Clin. Nutr. 63, 997S–1001S (1996).
    1. Lee K.-H., Calikoglu A. S., Ye P. & D'Ercole A. J. Insulin-like growth factor-I (IGF-I) ameliorates and IGF binding protein-1 (IGFBP-1) exacerbates the effects of undernutrition on brain growth during early postnatal life: studies in IGF-I and IGFBP-1 transgenic mice. Pediatr. Res. 45, 331–336 (1999).
    1. Beard J. L. & Connor J. R. Iron status and neural functioning. Annu. Rev. Nutr. 23, 41–58 (2003).
    1. Cusick S. E. & Georgieff M. K. Nutrient supplementation and neurodevelopment: timing is the key. Arch. Pediatr. Adolesc. Med. 166, 481–482 (2012).
    1. Mendez M. A. & Adair L. S. Severity and timing of stunting in the first two years of life affect performance on cognitive tests in late childhood. J. Nutr. 129, 1555–1562 (1999).
    1. Powell C. A., Walker S. P., Himes J. H., Fletcher P. D. & Grantham-McGregor S. M. Relationships between physical growth, mental development and nutritional supplementation in stunted children: the Jamaican study. Acta Paediatr. 84, 22–29 (1995).
    1. Martorell R. et al. Weight gain in the first two years of life is an important predictor of schooling outcomes in pooled analyses from five birth cohorts from low-and middle-income countries. J. Nutr. 140, 348–354 (2010).
    1. Currie J. & Almond D. Human capital development before age five. Handb. Labor Econ. 4, 1315–1486 (2011).
    1. Victora C. G. et al. Maternal and child undernutrition: consequences for adult health and human capital. The lancet 371, 340–357 (2008).
    1. Isaacs E. B. Neuroimaging, a new tool for investigating the effects of early diet on cognitive and brain development. Front. Hum. Neurosci. 7, 1–7 (2013).
    1. Kolyva C. et al. Oscillations in cerebral haemodynamics in patients with falciparum malaria. Adv. Exp. Med. Biol. 765, 101–107 (2013).
    1. Lunn P. G. The impact of infection and nutrition on gut function and growth in childhood. in. Proc. -Nutr. Soc. Lond. 59, 147–154 (2000).
    1. Lunn P. G., Northrop-Clewes C. A. & Downes R. M. Intestinal permeability, mucosal injury, and growth faltering in Gambian infants. The Lancet 338, 907–910 (1991).
    1. Van der Merwe L. F. et al. Long-chain PUFA supplementation in rural African infants: a randomized controlled trial of effects on gut integrity, growth, and cognitive development. Am. J. Clin. Nutr. 97, 45–57 (2013).
    1. Lloyd-Fox S., Blasi A., Mercure E., Elwell C. E. & Johnson M. H. The emergence of cerebral specialization for the human voice over the first months of life. Soc. Neurosci. 7, 317–330 (2012).
    1. Lloyd-Fox S. et al. Social perception in infancy: a near infrared spectroscopy study. Child Dev. 80, 986–999 (2009).
    1. Grossmann T., Oberecker R., Koch S. P. & Friederici A. D. The Developmental Origins of Voice Processing in the Human Brain. Neuron 65, 852–858 (2010).
    1. Minagawa-Kawai Y. et al. Optical Brain Imaging Reveals General Auditory and Language-Specific Processing in Early Infant Development. Cereb. Cortex 21, 254–261 (2011).
    1. Lloyd-Fox S., Blasi A., Everdell N., Elwell C. E. & Johnson M. H. Selective cortical mapping of biological motion processing in young infants. J. Cogn. Neurosci. 23, 2521–2532 (2011).
    1. Belin P., Zatorre R. J., Lafaille P., Ahad P. & Pike B. Voice-selective areas in human auditory cortex. Nature 403, 309–312 (2000).
    1. Wilcox T., Hirshkowitz A., Hawkins L. & Boas D. A. The effect of color priming on infant brain and behavior. NeuroImage 10.1016/j.neuroimage.2013.08.045.
    1. Coutts L. V., Cooper C. E., Elwell C. E. & Wilkins A. J. Time course of the haemodynamic response to visual stimulation in migraine, measured using near-infrared spectroscopy. Cephalalgia 32, 621–629 (2012).
    1. Jackson P. A. & Kennedy D. O. The application of near infrared spectroscopy in nutritional intervention studies. Front. Hum. Neurosci. 7 (2013).
    1. Everdell N. L. et al. A frequency multiplexed near-infrared topography system for imaging functional activation in the brain. Rev. Sci. Instrum. 76, 093705 (2005).
    1. Salamon G., Raynaud C., Regis J. & Rumeau C. Magnetic resonance imaging of the pediatric brain. (Raven Press., 1990).
    1. Belin P., Fillion-Bilodeau S. & Gosselin F. The Montreal Affective Voices: A validated set of nonverbal affect bursts for research on auditory affective processing. Behav. Res. Methods 40, 531 (2008).
    1. Obrig H. & Villringer A. Beyond the visible—imaging the human brain with light. J. Cereb. Blood Flow Metab. 23, 1–18 (2003).
    1. Benjamini Y. & Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. Ser. B Methodol. 57, 289–300 (1995).

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться