Numerosity representation is encoded in human subcortex

Significance Despite major neuroanatomical differences, adults, infants, nonhuman primates, and invertebrates possess the ability to evaluate relative quantities. Humans’ ability starts with coarse granularity (distinguishing ratios of numerical quantities of 3:1 or larger), but this becomes increasingly precise over development. This series of experiments demonstrates a role of the subcortex in discriminating numerosities in larger (4:1 or 3:1), but not in smaller ratios. These findings map onto the precision with which newborns evaluate number. Combined with evidence from the development of numerical skills, this study implicates the human subcortex as a possible source of core number knowledge that is both related to phylogenetic numerical competence and serves as the foundation on which more complex ontogenetic numerical skills may be built. Certain numerical abilities appear to be relatively ubiquitous in the animal kingdom, including the ability to recognize and differentiate relative quantities. This skill is present in human adults and children, as well as in nonhuman primates and, perhaps surprisingly, is also demonstrated by lower species such as mosquitofish and spiders, despite the absence of cortical computation available to primates. This ubiquity of numerical competence suggests that representations that connect to numerical tasks are likely subserved by evolutionarily conserved regions of the nervous system. Here, we test the hypothesis that the evaluation of relative numerical quantities is subserved by lower-order brain structures in humans. Using a monocular/dichoptic paradigm, across four experiments, we show that the discrimination of displays, consisting of both large (5–80) and small (1–4) numbers of dots, is facilitated in the monocular, subcortical portions of the visual system. This is only the case, however, when observers evaluate larger ratios of 3:1 or 4:1, but not smaller ratios, closer to 1:1. This profile of competence matches closely the skill with which newborn infants and other species can discriminate numerical quantity. These findings suggest conservation of ontogenetically and phylogenetically lower-order systems in adults’ numerical abilities. The involvement of subcortical structures in representing numerical quantities provokes a reconsideration of current theories of the neural basis of numerical cognition, inasmuch as it bolsters the cross-species continuity of the biological system for numerical abilities.

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