Cortical response to categorical color perception in infants investigated by near-infrared spectroscopy

Significance There has been much debate on the Sapir–Wharf hypothesis regarding whether language affects our perceptual world. Despite much research on this topic, there remains no clear consensus on whether and how language affects categorical color perception. Here, we provide the first evidence, to our knowledge, that categorical color perception has a universal starting point prior to language acquisition. We measured the neural correlates of categorical color perception in prelinguistic infants. We found increased brain activities to colors in different categories, but not to colors in the same category. These results indicated that different color categories are differently represented in the visual cortex of prelinguistic infants, which implies that color categories may develop in the visual system before language acquisition. Perceptual color space is continuous; however, we tend to divide it into only a small number of categories. It is unclear whether categorical color perception is obtained solely through the development of the visual system or whether it is affected by language acquisition. To address this issue, we recruited prelinguistic infants (5- to 7-mo-olds) to measure changes in brain activity in relation to categorical color differences by using near-infrared spectroscopy (NIRS). We presented two sets of geometric figures to infants: One set altered in color between green and blue, and the other set altered between two different shades of green. We found a significant increase in hemodynamic responses during the between-category alternations, but not during the within-category alternations. These differences in hemodynamic response based on categorical relationship were observed only in the bilateral occipitotemporal regions, and not in the occipital region. We confirmed that categorical color differences yield behavioral differences in infants. We also observed comparable hemodynamic responses to categorical color differences in adults. The present study provided the first evidence, to our knowledge, that colors of different categories are represented differently in the visual cortex of prelinguistic infants, which implies that color categories may develop independently before language acquisition.

[1]  Angela M. Brown,et al.  World Color Survey color naming reveals universal motifs and their within-language diversity , 2009, Proceedings of the National Academy of Sciences.

[2]  Angela M. Brown,et al.  Universality of color names , 2006, Proceedings of the National Academy of Sciences.

[3]  Koichi Mori,et al.  Neural Attunement Processes in Infants during the Acquisition of a Language-Specific Phonemic Contrast , 2007, The Journal of Neuroscience.

[4]  J. Davidoff,et al.  Colour categories in a stone-age tribe , 1999, Nature.

[5]  Angela M. Brown,et al.  Infant color vision and color preferences: A tribute to Davida Teller , 2013, Visual Neuroscience.

[6]  A. Blasi,et al.  Illuminating the developing brain: The past, present and future of functional near infrared spectroscopy , 2010, Neuroscience & Biobehavioral Reviews.

[7]  K. Gegenfurtner,et al.  Is there a lateralized category effect for color? , 2011, Journal of vision.

[8]  Troy A. W. Visser,et al.  Implicit semantic perception in object substitution masking , 2011 .

[9]  D. Teller,et al.  Infant color vision: Infants’ spontaneous color preferences are well behaved , 2007, Vision Research.

[10]  S. Zeki,et al.  The architecture of the colour centre in the human visual brain: new results and a review * , 2000, The European journal of neuroscience.

[11]  Kenichi Ueno,et al.  Hue Selectivity in Human Visual Cortex Revealed by Functional Magnetic Resonance Imaging , 2015, Cerebral cortex.

[12]  Tetsuro Matsuzawa,et al.  Colour naming and classification in a chimpanzee (Pan troglodytes) , 1985 .

[13]  J. Werner,et al.  Spectral efficiency measured by heterochromatic flicker photometry is similar in human infants and adults , 1995, Vision Research.

[14]  J. Pokorny,et al.  Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm , 1975, Vision Research.

[15]  Masako Okamoto,et al.  Three-dimensional probabilistic anatomical cranio-cerebral correlation via the international 10–20 system oriented for transcranial functional brain mapping , 2004, NeuroImage.

[16]  A. Franklin,et al.  New evidence for infant colour categories , 2004 .

[17]  Jennifer L. Campos,et al.  The N2pc component in ERP and the lateralization effect of language on color perception , 2009, Neuroscience Letters.

[18]  I R L Davies,et al.  Lateralization of categorical perception of color changes with color term acquisition , 2008, Proceedings of the National Academy of Sciences.

[19]  J. Davidoff,et al.  Color categories are not universal: replications and new evidence from a stone-age culture. , 2000, Journal of experimental psychology. General.

[20]  D. Heeger,et al.  Categorical Clustering of the Neural Representation of Color , 2013, The Journal of Neuroscience.

[21]  浜中 淑彦 Carl Wernicke;Der aphasische Symptomencomplex--Eine psychologische Studie auf anatomischer Basis(「失語症候群--解剖学的基礎に立つ心理学的研究」,Max Cohn & Weigert,Breslau,1874) , 1975 .

[22]  P. Kay,et al.  Categorical perception of color is lateralized to the right hemisphere in infants, but to the left hemisphere in adults , 2008, Proceedings of the National Academy of Sciences.

[23]  S Yamane,et al.  Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[25]  P. Kay,et al.  Whorf hypothesis is supported in the right visual field but not the left. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  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.

[27]  R. M. Boynton,et al.  Categorical color perception of Japanese observers: Comparison with that of Americans , 1987, Vision Research.

[28]  M. Bornstein,et al.  Color vision and hue categorization in young human infants. , 1976, Journal of experimental psychology. Human perception and performance.

[29]  Tsunehiro Takeda,et al.  MEG recording from the human ventro-occipital cortex in response to isoluminant color stimulation , 2005, Visual Neuroscience.

[30]  Angela M. Brown,et al.  Color names, color categories, and color-cued visual search: sometimes, color perception is not categorical. , 2011, Journal of vision.

[31]  Keiji Uchikawa,et al.  Expression of Color Appearance in Aperture and Surface Color Modes with A Category Rating Estimation Method , 1994 .

[32]  M. Bornstein Qualities of color vision in infancy. , 1975, Journal of experimental child psychology.

[33]  A. Franklin,et al.  Categorical encoding of color in the brain , 2014, Proceedings of the National Academy of Sciences.

[34]  D. Macleod,et al.  Flicker photometric study of chromatic adaption: selective suppression of cone inputs by colored backgrounds. , 1981, Journal of the Optical Society of America.

[35]  Kang-Kwong Luke,et al.  Language regions of brain are operative in color perception , 2009, Proceedings of the National Academy of Sciences.

[36]  P. Kay,et al.  Language, thought and color: recent developments , 2006, Trends in Cognitive Sciences.

[37]  Yumiko Otsuka,et al.  Neural activation to upright and inverted faces in infants measured by near infrared spectroscopy , 2007, NeuroImage.

[38]  P. Kaiser,et al.  Contributions of the opponent mechanisms to brightness and nonlinear models , 1988, Vision Research.

[39]  Bevil R. Conway,et al.  Specialized Color Modules in Macaque Extrastriate Cortex , 2007, Neuron.

[40]  Bevil R. Conway,et al.  Cerebral Cortex Advance Access published December 28, 2005 Color Architecture in Alert Macaque Cortex , 2022 .

[41]  K. Jameson,et al.  Differences in Color Naming and Color Salience in Vietnamese and English , 2003 .

[42]  A. Franklin,et al.  Electrophysiological markers of categorical perception of color in 7-month old infants , 2009, Brain and Cognition.

[43]  P. Kay,et al.  Resolving the question of color naming universals , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Michael Pilling,et al.  The nature of infant color categorization: evidence from eye movements on a target detection task. , 2005, Journal of experimental child psychology.

[45]  Michael C. Frank,et al.  Russian blues reveal effects of language on color discrimination , 2007, Proceedings of the National Academy of Sciences.

[46]  H. Komatsu,et al.  Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex , 2007, Nature Neuroscience.