Abstract
How the newborn brain adapts to its new multisensory environment has been a subject of debate. Although an early theory proposed that the brain acquires multisensory features as a result of postnatal experience, recent studies have demonstrated that the neonatal brain is already capable of processing multisensory information. For multisensory processing to be functional, it is a prerequisite that multisensory convergence among neural connections occur. However, multisensory connectivity has not been examined in human neonates nor are its location(s) or afferent sources understood. We used resting state functional MRI (fMRI) in two independent cohorts of infants to examine the functional connectivity of two cortical areas known to be multisensory in adults: the intraparietal sulcus (IPS) and the superior temporal sulcus (STS). In the neonate, the IPS was found to demonstrate significant functional connectivity with visual association and somatosensory association areas, while the STS showed significant functional connectivity with the visual association areas, primary auditory cortex, and somatosensory association areas. Our findings establish that each of these areas displays functional communication with cortical regions representing various sensory modalities. This demonstrates the presence of cortical areas with converging sensory inputs, representing that the functional architecture needed for multisensory processing is already present within the first weeks of life.
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References
Beauchamp, M. S., Yasar, N. E., Frye, R. E., & Ro, T. (2008). Touch, sound and vision in human superior temporal sulcus. NeuroImage, 41, 1011–1020.
Biagi, L., Crespi, S. A., Tosetti, M., & Morrone, M. C. (2015). BOLD response selective to flow-motion in very young infants. PLoS Biology, 13, e1002260.
Biswal, B., Yetkin, F. Z., Haughton, V. M., & Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magnetic Resonance in Medicine, 34, 537–541.
Bray, S., Arnold, A. E., Iaria, G., & MacQueen, G. (2013). Structural connectivity of visuotopic intraparietal sulcus. NeuroImage, 82, 137–145.
Callaway, E. M., & Katz, L. C. (1990). Emergence and refinement of clustered horizontal connections in cat striate cortex. The Journal of Neuroscience, 10, 1134–1153.
Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magentic resonance neuroimages. Computers and Biomedical Research, 29, 162–173.
Friston, K. J., Frith, C. D., Liddle, P. F., & Frackowiak, R. S. (1993). Functional connectivity: the principal-component analysis of large (PET) data sets. Journal of Cerebral Blood Flow and Metabolism, 13, 5–14.
Gilmore, J. H., Lin, W., Prastawa, M. W., Looney, C. B., Vetsa, Y. S., Knickmeyer, R. C., Evans, D. D., Smith, J. K., Hamer, R. M., Lieberman, J. A., & Gerig, G. (2007). Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. The Journal of Neuroscience, 27, 1255–1260.
Gogolla, N., Takesian, A. E., Feng, G., Fagiolini, M., & Hensch, T. K. (2014). Sensory integration in mouse insular cortex reflects GABA circuit maturation. Neuron, 83, 894–905.
Grefkes, C., & Fink, G. R. (2005). The functional organization of the intraparietal sulcus in humans and monkeys. Journal of Anatomy, 207, 3–17.
Hein, G., & Knight, R. T. (2008). Superior temporal sulcus--It's my area: or is it? Journal of Cognitive Neuroscience, 20, 2125–2136.
Katz, L. C., & Callaway, E. M. (1992). Development of local circuits in mammalian visual cortex. Annual Review of Neuroscience, 15, 31–56.
Larson-Prior, L. J., Zempel, J. M., Nolan, T. S., Prior, F. W., Snyder, A. Z., & Raichle, M. E. (2009). Cortical network functional connectivity in the descent to sleep. Proceedings of the National Academy of Sciences of the United States of America, 106, 4489–4494.
Lewkowicz, D. J., & Ghazanfar, A. A. (2009). The emergence of multisensory systems through perceptual narrowing. Trends in Cognitive Sciences, 13, 470–478.
Lewkowicz, D. J., Leo, I., & Simion, F. (2010). Intersensory perception at birth: newborns match nonhuman primate faces and voices. Infancy, 15, 46–60.
Meltzoff, A. N., & Moore, M. K. (1977). Imitation of facial and manual gestures by human neonates. Science, 198, 75–78.
Pascalis, O., Scott, L. S., Kelly, D. J., Shannon, R. W., Nicholson, E., Coleman, M., & Nelson, C. A. (2005). Plasticity of face processing in infancy. Proceedings of the National Academy of Sciences of the United States of America, 102, 5297–5300.
Piaget, J. (1952). The origings of intelligence in children. New York: International University Press.
Seltzer, B., & Pandya, D. N. (1980). Converging visual and somatic sensory cortical input to the intraparietal sulcus of the rhesus monkey. Brain Research, 192, 339–351.
Seltzer, B., & Pandya, D. N. (1994). Parietal, temporal, and occipital projections to cortex of the superior temporal sulcus in the rhesus monkey: a retrograde tracer study. The Journal of Comparative Neurology, 343, 445–463.
Shi, F., Yap, P. T., Wu, G., Jia, H., Gilmore, J. H., Lin, W., & Shen, D. (2011). Infant brain atlases from neonates to 1- and 2-year-olds. PloS One, 6, e18746.
SPM8. (2016). Statistical parametric mapping. Wellcome Department of Imaging Neuroscience, University College London, UK.
Stein, B. E., & Meredith, M. A. (1993). The merging of the senses. Cambridge, MA: The MIT Press.
Stein, B. E., Stanford, T. R., & Rowland, B. A. (2014). Development of multisensory integration from the perspective of the individual neuron. Nature Reviews. Neuroscience, 15, 520–535.
Streri, A., & Molina, M. (1993). Visual-tactual and tactual-visual transfer between objects and pictures in 2-month-old infants. Perception, 22, 1299–1318.
Uddin, L. Q., Supekar, K., Amin, H., Rykhlevskaia, E., Nguyen, D. A., Greicius, M. D., & Menon, V. (2010). Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cerebral Cortex, 20, 2636–2646.
Wallace, M. T., Carriere, B. N., Perrault Jr., T. J., Vaughan, J. W., & Stein, B. E. (2006). The development of cortical multisensory integration. The Journal of Neuroscience, 26, 11844–11849.
Acknowledgments
This work was supported by the National Institutes of Health (Grant R01-MH064065 & R01-HD053000 to JHG; Grant R01AA013023 & R01AA022455 to AEM).
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All procedures followed were in accordance with the ethical standards of the responsible committee on human experimentation (institutional and national) and with the Helsinki Declaration of 1975, and the applicable revisions at the time of the investigation. Informed consent was obtained from guardians of all patients for being included in the study.
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Sours, C., Raghavan, P., Foxworthy, W.A. et al. Cortical multisensory connectivity is present near birth in humans. Brain Imaging and Behavior 11, 1207–1213 (2017). https://doi.org/10.1007/s11682-016-9586-6
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DOI: https://doi.org/10.1007/s11682-016-9586-6