We report here that monkeys can actively match the number of sounds they hear to the number of shapes they see and present the first evidence that monkeys sum over sounds and sights. In Experiment 1, two monkeys were trained to choose a simultaneous array of 1-9 squares that numerically matched a sample sequence of shapes or sounds. Monkeys numerically matched across (audio-visual) and within (visual-visual) modalities with equal accuracy and transferred to novel numerical values. In Experiment 2, monkeys presented with sample sequences of randomly ordered shapes or tones were able to choose an array of 2-9 squares that was the numerical sum of the shapes and sounds in the sample sequence. In both experiments, accuracy and reaction time depended on the ratio between the correct numerical match and incorrect choice. These findings suggest monkeys and humans share an abstract numerical code that can be divorced from the modality in which stimuli are first experienced. © 2008 Elsevier B.V. All rights reserved.
Behavioral studies have demonstrated that time perception in adults, children, and nonhuman animals is subject to Weber's Law. More specifically, as with discriminations of other features, it has been found that it is the ratio between two durations rather than their absolute difference that controls the ability of an animal to discriminate them. Here, we show that scalp-recorded event-related electrical brain potentials (ERPs) in both adults and 10-month-old human infants, in response to changes in interstimulus interval (ISI), appear to obey the scalar property found in time perception in adults, children, and nonhuman animals. Using a timing-interval oddball paradigm, we tested adults and infants in conditions where the ratio between the standard and deviant interval in a train of homogeneous auditory stimuli varied such that there was a 1:4 (only for the infants), 1:3, 1:2, and 2:3 ratio between the standard and deviant intervals. We found that the amplitude of the deviant-triggered mismatch negativity ERP component (deviant-ISI ERP minus standard-ISI ERP) varied as a function of the ratio of the standard to deviant interval. Moreover, when absolute values were varied and ratio was held constant, the mismatch negativity did not vary.
This study investigates the ability of 6-month-old infants to attend to the continuous properties of a set of discrete entities. Infants were habituated to dot arrays that were constant in cumulative surface area yet varied in number for small ( 3) sets. Results revealed that infants detected a 4-fold (but not 3-fold) change in area, regardless of set size. These results are in marked contrast to demonstrations that infants of the same age successfully discriminate a 2- or 3-fold change in number, providing strong counterevidence to the claim that infants use solely nonnumerical, continuous extent variables when discriminating sets. These findings also shed light on the processes involved in tracking continuous variables in infants.
Adult humans possess a sophisticated repertoire of mathematical faculties. Many of these capacities are rooted in symbolic language and are therefore unlikely to be shared with nonhuman animals. However, a subset of these skills is shared with other animals, and this set is considered a cognitive vestige of our common evolutionary history. Current evidence indicates that humans and nonhuman animals share a core set of abilities for representing and comparing approximate numerosities nonverbally; however, it remains unclear whether nonhuman animals can perform approximate mental arithmetic. Here we show that monkeys can mentally add the numerical values of two sets of objects and choose a visual array that roughly corresponds to the arithmetic sum of these two sets. Furthermore, monkeys' performance during these calculations adheres to the same pattern as humans tested on the same nonverbal addition task. Our data demonstrate that nonverbal arithmetic is not unique to humans but is instead part of an evolutionarily primitive system for mathematical thinking shared by monkeys.
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.
Time perception is important for many aspects of human behavior, and a large literature documents that adults represent intervals and that their ability to discriminate temporal intervals is ratio dependent. Here we replicate a recent study by vanMarle and Wynn (2006) that used the visual habituation paradigm and demonstrated that temporal discrimination in 6-month-old infants is also ratio dependent. We further demonstrate that between 6 and 10 months of age temporal discrimination increases in precision such that by 10 months of age infants succeed at discriminating a 2:3 ratio, a ratio that 6-month-old infants were unable to discriminate. We discuss the potential implications of the fact that temporal discrimination follows the same developmental progression that has been previously observed for number discrimination in infancy (Lipton & Spelke, 2003).
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.
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.