Abstract
Adult humans, infants, pre-school children, and non-human animals appear to share a system of approximate numerical processing for non-symbolic stimuli such as arrays of dots or sequences of tones. Behavioral studies of adult humans implicate a link between these non-symbolic numerical abilities and symbolic numerical processing (e.g., similar distance effects in accuracy and reaction-time for arrays of dots and Arabic numerals). However, neuroimaging studies have remained inconclusive on the neural basis of this link. The intraparietal sulcus (IPS) is known to respond selectively to symbolic numerical stimuli such as Arabic numerals. Recent studies, however, have arrived at conflicting conclusions regarding the role of the IPS in processing non-symbolic, numerosity arrays in adulthood, and very little is known about the brain basis of numerical processing early in development. Addressing the question of whether there is an early-developing neural basis for abstract numerical processing is essential for understanding the cognitive origins of our uniquely human capacity for math and science. Using functional magnetic resonance imaging (fMRI) at 4-Tesla and an event-related fMRI adaptation paradigm, we found that adults showed a greater IPS response to visual arrays that deviated from standard stimuli in their number of elements, than to stimuli that deviated in local element shape. These results support previous claims that there is a neurophysiological link between non-symbolic and symbolic numerical processing in adulthood. In parallel, we tested 4-y-old children with the same fMRI adaptation paradigm as adults to determine whether the neural locus of non-symbolic numerical activity in adults shows continuity in function over development. We found that the IPS responded to numerical deviants similarly in 4-y-old children and adults. To our knowledge, this is the first evidence that the neural locus of adult numerical cognition takes form early in development, prior to sophisticated symbolic numerical experience. More broadly, this is also, to our knowledge, the first cognitive fMRI study to test healthy children as young as 4 y, providing new insights into the neurophysiology of human cognitive development.
Highlights
Language influences the way we think about number
A random-effects analysis that directly compared activity to number and shape deviants revealed bilateral number-related activity localized to the intraparietal sulcus (IPS) and extending into the inferior and superior parietal lobules consistent with previous studies that tested adults with Arabic numeral stimuli, symbolic arithmetic operations, and number words [21,23], as well as a study of non-symbolic number processing [28] (Figure 2A, Montreal Neurologic Institute (MNI) coordinates x, y, z: 43, À47, 59, BA [Broadman’s area] 1⁄4 40; À31, À66, 62, BA 1⁄4 7)
Between 3 and 7.5 s post-stimulus onset, the IPS produced a significantly greater response to stimuli in which the number of elements changed but the shape remained constant, than to stimuli in which the local element shape changed but the number of elements remained constant. This value was significantly greater than the baseline level of activity across participants (mean 1⁄4 .30%, t (11) 1⁄4 6.63, p, .001) whereas the hemodynamic response (HDR) to shape deviants in this region was significantly lower than baseline (mean 1⁄4À.17%, t (11) 1⁄4 À6.14, p, .001)
Summary
Language influences the way we think about number. substantial evidence indicates that preverbal children and human adults, as well as other animals, share a fundamental mechanism for representing approximate numerical values that is independent of language [1,2,3,4,5,6,7,8,9,10]. Humans appear to possess a common psychological currency for representing numerical value regardless of whether the value is communicated symbolically via Arabic numerals and number words or non-symbolically through the number of visual objects in a set or the number of tones in an auditory sequence [3,11,12,13,14]. These and other findings have led researchers to predict that approximate numerical information, whether symbolic or non-symbolic, is processed by a common neural substrate [15,16,17]. While behavioral studies of adults implicate a link between approximate symbolic and non-symbolic numerical processing, neuro-
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