Elizabeth M. Brannon

Functional imaging of numerical processing in adults and 4-y-old children.

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.

Beyond the number domain

In a world without numbers, we would be unable to build a skyscraper, hold a national election, plan a wedding or pay for a chicken at the market. The numerical symbols used in all these behaviors build on the approximate number system (ANS) which represents the number of discrete objects or events as a continuous mental magnitude. Here, we first discuss evidence that the ANS bears a set of behavioral and brain signatures that are universally displayed across animal species, human cultures and development. We then turn to the question of whether the ANS constitutes a specialized cognitive and neural domain - a question central to understanding how this system works, the nature of its evolutionary and developmental trajectory and its physical instantiation in the brain.

The development of ordinal numerical knowledge in infancy

A critical question in cognitive science concerns how numerical knowledge develops. One essential component of an adult concept of number is ordinality: the greater than and less than relationships between numbers. Here it is shown in two experiments that 11-month-old infants successfully discriminated, whereas 9-month-old infants failed to discriminate, sequences of numerosities that descended in numerical value from sequences that increased in numerical value. These results suggest that by 11 months of age infants possess the ability to appreciate the greater than and less than relations between numerical values but that this ability develops between 9 and 11 months of age. In an additional experiment 9-month-old infants succeeded at discriminating the ordinal direction of sequences that varied in the size of a single square rather than in number, suggesting that a capacity for non-numerical ordinal judgments may develop before a capacity for ordinal numerical judgments. These data raise many questions about how infants represent number and what happens between 9 and 11 months to support ordinal numerical judgments.

The Evolution of Self-Control

Significance Although scientists have identified surprising cognitive flexibility in animals and potentially unique features of human psychology, we know less about the selective forces that favor cognitive evolution, or the proximate biological mechanisms underlying this process. We tested 36 species in two problem-solving tasks measuring self-control and evaluated the leading hypotheses regarding how and why cognition evolves. Across species, differences in absolute (not relative) brain volume best predicted performance on these tasks. Within primates, dietary breadth also predicted cognitive performance, whereas social group size did not. These results suggest that increases in absolute brain size provided the biological foundation for evolutionary increases in self-control, and implicate species differences in feeding ecology as a potential selective pressure favoring these skills. Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

Monotonic Coding of Numerosity in Macaque Lateral Intraparietal Area

As any child knows, the first step in counting is summing up individual elements, yet the brain mechanisms responsible for this process remain obscure. Here we show, for the first time, that a population of neurons in the lateral intraparietal area of monkeys encodes the total number of elements within their classical receptive fields in a graded fashion, across a wide range of numerical values (2–32). Moreover, modulation of neuronal activity by visual quantity developed rapidly, within 100 ms of stimulus onset, and was independent of attention, reward expectations, or stimulus attributes such as size, density, or color. The responses of these neurons resemble the outputs of “accumulator neurons” postulated in computational models of number processing. Numerical accumulator neurons may provide inputs to neurons encoding specific cardinal values, such as “4,” that have been described in previous work. Our findings may explain the frequent association of visuospatial and numerical deficits following damage to parietal cortex in humans.

Training the Approximate Number System Improves Math Proficiency

Humans and nonhuman animals share an approximate number system (ANS) that permits estimation and rough calculation of quantities without symbols. Recent studies show a correlation between the acuity of the ANS and performance in symbolic math throughout development and into adulthood, which suggests that the ANS may serve as a cognitive foundation for the uniquely human capacity for symbolic math. Such a proposition leads to the untested prediction that training aimed at improving ANS performance will transfer to improvement in symbolic-math ability. In the two experiments reported here, we showed that ANS training on approximate addition and subtraction of arrays of dots selectively improved symbolic addition and subtraction. This finding strongly supports the hypothesis that complex math skills are fundamentally linked to rudimentary preverbal quantitative abilities and provides the first direct evidence that the ANS and symbolic math may be causally related. It also raises the possibility that interventions aimed at the ANS could benefit children and adults who struggle with math.

Numerical Subtraction in the Pigeon: Evidence for a Linear Subjective Number Scale

When humans and animals compare two numbers, responding is faster and more accurate with increasing numerical disparity and decreasing numerical size. Researchers explaining these distance and size effects often assume that the subjective number continuum is logarithmically compressed. An alternative hypothesis is that the subjective number continuum is linear, but positions farther along it are proportionately fuzzier, that is, less precisely located. These two hypotheses have been treated as functionally equivalent because of their similar empirical predictions. The current experiment sought to resolve this issue with a paradigm originally developed to address the subjective representation of time (time left). In our adaptation, pigeons were required to compare a constant number with the number remaining after a numerical subtraction. Our results indicate that subjective number is linearly, not logarithmically, related to objective number.

The representation of numerical magnitude.

The combined efforts of many fields are advancing our understanding of how number is represented. Researchers studying numerical reasoning in adult humans, developing humans and non-human animals are using a suite of behavioral and neurobiological methods to uncover similarities and differences in how each population enumerates and compares quantities to identify the neural substrates of numerical cognition. An important picture emerging from this research is that adult humans share with non-human animals a system for representing number as language-independent mental magnitudes and that this system emerges early in development.

Number sense in infancy predicts mathematical abilities in childhood

Significance The uniquely human mathematical mind sets us apart from all other animals. How does this powerful capacity emerge over development? It is uncontroversial that education and environment shape mathematical ability, yet an untested assumption is that number sense in infants is a conceptual precursor that seeds human mathematical development. Our results provide the first support for this hypothesis. We found that preverbal number sense in 6-month-old infants predicted standardized math scores in the same children 3 years later. This discovery shows that number sense in infancy is a building block for later mathematical ability and invites educational interventions to improve number sense even before children learn to count. Human infants in the first year of life possess an intuitive sense of number. This preverbal number sense may serve as a developmental building block for the uniquely human capacity for mathematics. In support of this idea, several studies have demonstrated that nonverbal number sense is correlated with mathematical abilities in children and adults. However, there has been no direct evidence that infant numerical abilities are related to mathematical abilities later in childhood. Here, we provide evidence that preverbal number sense in infancy predicts mathematical abilities in preschool-aged children. Numerical preference scores at 6 months of age correlated with both standardized math test scores and nonsymbolic number comparison scores at 3.5 years of age, suggesting that preverbal number sense facilitates the acquisition of numerical symbols and mathematical abilities. This relationship held even after controlling for general intelligence, indicating that preverbal number sense imparts a unique contribution to mathematical ability. These results validate the many prior studies purporting to show number sense in infancy and support the hypothesis that mathematics is built upon an intuitive sense of number that predates language.

How does cognition evolve? Phylogenetic comparative psychology

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.