We directly tested the predictions of the approximate number system (ANS) and the object file system in the spontaneous numerical judgments of prosimian primates. Prior work indicates that when human infants and a few species of non-human animals are given a single-trial choice between two sequentially baited buckets they choose the bucket with the greater amount of food but only when the quantities are small. This pattern of results has been interpreted as evidence that a limited capacity object file system is used to track small numbers of objects and that the ANS is not invoked under these circumstances. Here we tested prosimian primates in food choice comparisons that were chosen to contrast predictions of the ANS and object file systems. We found that prosimian primates consistently chose the larger of two sets when they differed by a 1:3 ratio regardless of whether both values were small (≤3), both values were large (>3), or there was one small and one large value. Prosimians were not able to robustly discriminate quantities that differed by a 1:2 ratio for the same three conditions, nor did they show a preference for small quantities that differed by a 2:3 ratio. These results implicate the ANS in the spontaneous numerical discriminations of non-human primates.

The ability to represent approximate quantities appears to be phylogenetically widespread, but the selective pressures and proximate mechanisms favouring this ability remain unknown. We analysed quantity discrimination data from 672 subjects across 33 bird and mammal species, using a novel Bayesian model that combined phylogenetic regression with a model of number psychophysics and random effect components. This allowed us to combine data from 49 studies and calculate the Weber fraction (a measure of quantity representation precision) for each species. We then examined which cognitive, socioecological and biological factors were related to variance in Weber fraction. We found contributions of phylogeny to quantity discrimination performance across taxa. Of the neural, socioecological and general cognitive factors we tested, cortical neuron density and domain-general cognition were the strongest predictors of Weber fraction, controlling for phylogeny. Our study is a new demonstration of evolutionary constraints on cognition, as well as of a relation between species-specific neuron density and a particular cognitive ability. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

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We investigated the precision of the approximate number system (ANS) in three lemur species (Lemur catta, Eulemur mongoz, and Eulemur macaco flavifrons), one Old World monkey species (Macaca mulatta) and humans (Homo sapiens). In Experiment 1, four individuals of each nonhuman primate species were trained to select the numerically larger of two visual arrays on a touchscreen. We estimated numerical acuity by modeling Weber fractions (w) and found quantitatively equivalent performance among all four nonhuman primate species. In Experiment 2, we tested adult humans in a similar procedure, and they outperformed the four nonhuman species but showed qualitatively similar performance. These results indicate that the ANS is conserved over the primate order.

Do monkeys anchor their numerical judgments based on the context in which their choices are presented? We addressed this question by varying the numerical range across sessions while macaque monkeys made ordinal judgments. Monkeys were trained to make a conditional discrimination whereby they were reinforced for ordering arrays of dots in ascending or descending numerical order, dependent on a color cue. Monkeys were tested using two ranges of numerosities that converged on a single pair. Similar to the findings of Cantlon & Brannon (2005), we found a semantic congruity effect whereby decision time was systematically influenced by the congruity between the cue (ascending or descending) and the relative numerical magnitude of the stimuli within each range. Furthermore, monkeys showed a context effect, such that decision time for a given pair was dependent on whether it was a relatively small or large set of values compared to the other values presented in that session. This finding suggests that similar to humans, the semantic congruity effect observed in monkeys is anchored by the context. Thus our data provide further evidence for the existence of a shared numerical comparison process in monkeys and humans.