Foundational Number Sense Training Gains Are Predicted by Hippocampal-Parietal Circuits.

The development of mathematical skills in early childhood relies on number sense, the foundational ability to discriminate among quantities. Number sense in early childhood is predictive of academic and professional success, and deficits in number sense are thought to underlie lifelong impairments in mathematical abilities. Despite its importance, the brain circuit mechanisms that support number sense learning remain poorly understood. Here, we designed a theoretically motivated training program to determine brain circuit mechanisms underlying foundational number sense learning in female and male elementary school-age children (7-10 years). Our 4 week integrative number sense training program gradually strengthened the understanding of the relations between symbolic (Arabic numerals) and nonsymbolic (sets of items) representations of quantity. We found that our number sense training program improved symbolic quantity discrimination ability in children across a wide range of math abilities including children with learning difficulties. Crucially, the strength of pretraining functional connectivity between the hippocampus and intraparietal sulcus, brain regions implicated in associative learning and quantity discrimination, respectively, predicted individual differences in number sense learning across typically developing children and children with learning difficulties. Reverse meta-analysis of interregional coactivations across 14,371 fMRI studies and 89 cognitive functions confirmed a reliable role for hippocampal-intraparietal sulcus circuits in learning. Our study identifies a canonical hippocampal-parietal circuit for learning that plays a foundational role in children's cognitive skill acquisition. Findings provide important insights into neurobiological circuit markers of individual differences in children's learning and delineate a robust target for effective cognitive interventions.SIGNIFICANCE STATEMENT Mathematical skill development relies on number sense, the ability to discriminate among quantities. Here, we develop a theoretically motivated training program and investigate brain circuits that predict number sense learning in children during a period important for acquisition of foundational cognitive skills. Our integrated number sense training program was effective in children across a wide a range of math abilities, including children with learning difficulties. We identify hippocampal-parietal circuits that predict individual differences in learning gains. Our study identifies a brain circuit critical for the acquisition of foundational cognitive skills, which will be useful for developing effective interventions to remediate learning disabilities.

Slowly walking down to the more food: relative quantity discrimination in African spurred tortoises (Centrochelys sulcata).

Quantity discrimination, is thought to be highly adaptive as it allows an organism to select greater amounts of food or larger social groups. In contrast to mammals, the processes underlying this ability are not as well understood in reptiles. This study examined the effects of ratio and number size on relative quantity discrimination in African spurred tortoises (Centrochelys sulcata). To assess these effects, tortoises were presented with trays containing favored food pieces in all possible number combinations between 1 and 7. The tortoises had to approach the tray they perceived as having the larger quantity. If correct, they received one piece of food as reinforcement. The results revealed that relative quantity discrimination was influenced by the ratio between the numbers of pieces, with performance improving as the ratio between the numbers increased. This finding suggests that the approximate number system or analogue magnitude estimation may control their behavior. However, as the number size increased, their performance declined, also suggesting that the approximate number system alone could not explain the present results.

Quantity discrimination by kittens of the domestic cat (Felis silvestris catus).

Quantitative abilities are well described in many species and in diverse life situations, including in the adult domestic cat. However, such abilities have been much less studied during ontogeny. In the present study we examined spontaneous quantity discrimination by pre-weaning age kittens in two-way food choice experiments. In Experiment 1, 26 kittens performed 12 trials with different ratios between the number of same-size food items. In Experiment 2, 24 other kittens performed eight trials with different ratios between the size of two food items. We found, in general, that the kittens discriminated between the different amounts of food and spontaneously chose the larger one, but that their choice was influenced by the ratio of difference. The kittens in Experiment 1 chose the larger number of same-size food items if the ratio was smaller than 0.4 and in Experiment 2 they chose the larger pieces of food if the ratio between the items was smaller than 0.5. Because the kittens' choice was not influenced by the absolute number of food items or the numerical difference between them in Experiment 1, it suggests that their cognitive performance relied on an analog magnitude system rather than on an object file system during the quantity discrimination tasks. We discuss our results considering the ecological and social background of cats and compare it with the performance of previously studied species.

Keep numbers in view: red-eared sliders (Trachemys scripta elegans) learn to discriminate relative quantities.

The ability to discriminate relative quantities, one of the numerical competences, is considered an adaptive trait in uncertain environments. Besides humans, previous studies have reported this capacity in several non-human primates and birds. Here, we test whether red-eared sliders (Trachemys scripta elegans) can discriminate different relative quantities. Subjects were first trained to distinguish different stimuli with food reward. Then, they were tested with novel stimulus pairs to demonstrate how they distinguished the stimuli. The results show that most subjects can complete the initial training and use relative quantity rather than absolute quantity to make choices during the testing phase. This study provides behavioural evidence of relative quantity discrimination in a reptile species and suggests that such capacity may be widespread among vertebrates.

Neurons in the Dorso-Central Division of Zebrafish Pallium Respond to Change in Visual Numerosity.

We found a region of the zebrafish pallium that shows selective activation upon change in the numerosity of visual stimuli. Zebrafish were habituated to sets of small dots that changed in individual size, position, and density, while maintaining their numerousness and overall surface. During dishabituation tests, zebrafish faced a change in number (with the same overall surface), in shape (with the same overall surface and number), or in size (with the same shape and number) of the dots, whereas, in a control group, zebrafish faced the same stimuli as during the habituation. Modulation of the expression of the immediate early genes c-fos and egr-1 and in situ hybridization revealed a selective activation of the caudal part of the dorso-central division of the zebrafish pallium upon change in numerosity. These findings support the existence of an evolutionarily conserved mechanism for approximate magnitude and provide an avenue for understanding its underlying molecular correlates.

Characterizing ontogeny of quantity discrimination in zebrafish.

A sense of non-symbolic numerical magnitudes is widespread in the animal kingdom and has been documented in adult zebrafish. Here, we investigated the ontogeny of this ability using a group size preference (GSP) task in juvenile zebrafish. Fish showed GSP from 21 days post-fertilization and reliably chose the larger group when presented with discriminations of between 1 versus 3, 2 versus 5 and 2 versus 3 conspecifics but not 2 versus 4 conspecifics. When the ratio between the number of conspecifics in each group was maintained at 1 : 2, fish could discriminate between 1 versus 2 individuals and 3 versus 6, but again, not when given a choice between 2 versus 4 individuals. These findings are in agreement with studies in other species, suggesting the systems involved in quantity representation do not operate separately from other cognitive mechanisms. Rather they suggest quantity processing in fishes may be the result of an interplay between attentional, cognitive and memory-related mechanisms as in humans and other animals. Our results emphasize the potential of the use of zebrafish to explore the genetic and neural processes underlying the ontogeny and function of number cognition.

Zebrafish excel in number discrimination under an operant conditioning paradigm.

Numerical discrimination is widespread in vertebrates, but this capacity varies enormously between the different species examined. The guppy (Poecilia reticulata), the only teleost examined following procedures that allow a comparison with the other vertebrates, outperforms amphibians, reptiles and many warm-blooded vertebrates, but it is unclear whether this is a feature shared with the other teleosts or represents a peculiarity of this species. We trained zebrafish (Danio rerio) to discriminate between numbers differing by one unit, varying task difficulty from 2 versus 3 to 5 versus 6 items. Non-numerical variables that covary with number, such as density or area, did not affect performance. Most fish reached learning criterion on all tasks up to 4 versus 5 discrimination with no sex difference in accuracy. Although no individual reached learning criterion in the 5 versus 6 task, performance was significant at the group level, suggesting that this may represent the discrimination threshold for zebrafish. Numerosity discrimination abilities of zebrafish compare to those of guppy, being higher than in some warm-blooded vertebrates, such as dogs, horses and domestic fowl, though lower than in parrots, corvids and primates. Learning rate was similar in a control group trained to discriminate between different-sized shapes, but zebrafish were slightly more accurate when discriminating areas than numbers and males were more accurate than females. At the end of the experiment, fish trained on numbers and controls trained on areas generalized to the reciprocal set of stimuli, indicating they had used a relational strategy to solve these tasks.

Quantity discrimination in a spontaneous task in a poison frog.

The use of quantitative information underlies a range of animal behaviors. There are thought to be two parallel systems for judging quantity: a precise representation of small numbers of objects, typically less than 4, that can be tracked visually (object tracking system) and an imprecise system for larger quantities (approximate number system) governed by Weber's law. Using a spontaneous discrimination task with live prey, we examined the ability of the poison frog Dendrobates auratus to discriminate quantities of low (1-4) or high (4-16) numerosity over a range of ratio contrasts (0.33, 0.5, 0.67, 0.75). Similar to a previous study in treefrogs, we found that the poison frogs chose the larger quantity of flies when choosing between 1 and 3 and between 1 and 2. However, their performance was near chance when choosing between 2 and 3 and below chance when choosing between 3 and 4. When the numerosity of flies was higher, they did not discriminate between the larger and smaller quantity. Our findings are consistent with the ability of poison frogs to discriminate small quantities of objects using an object tracking system, but could also reflect a singular vs. plural discrimination. We did not find evidence of an approximate number system governed by Weber's law, nor evidence of a speed-accuracy tradeoff. However, total set size was associated with lower accuracy and longer latencies to choose. Future studies should explore quantity discrimination in additional contexts to better understand the limits of these abilities in poison frogs.

Does quantity matter to a stingless bee?

Quantitative information is omnipresent in the world and a wide range of species has been shown to use quantities to optimize their decisions. While most studies have focused on vertebrates, a growing body of research demonstrates that also insects such as honeybees possess basic quantitative abilities that might aid them in finding profitable flower patches. However, it remains unclear if for insects, quantity is a salient feature relative to other stimulus dimensions, or if it is only used as a "last resort" strategy in case other stimulus dimensions are inconclusive. Here, we tested the stingless bee Trigona fuscipennis, a species representative of a vastly understudied group of tropical pollinators, in a quantity discrimination task. In four experiments, we trained wild, free-flying bees on stimuli that depicted either one or four elements. Subsequently, bees were confronted with a choice between stimuli that matched the training stimulus either in terms of quantity or another stimulus dimension. We found that bees were able to discriminate between the two quantities, but performance differed depending on which quantity was rewarded. Furthermore, quantity was more salient than was shape. However, quantity did not measurably influence the bees' decisions when contrasted with color or surface area. Our results demonstrate that just as honeybees, small-brained stingless bees also possess basic quantitative abilities. Moreover, invertebrate pollinators seem to utilize quantity not only as "last resort" but as a salient stimulus dimension. Our study contributes to the growing body of knowledge on quantitative cognition in invertebrate species and adds to our understanding of the evolution of numerical cognition.

Video playback versus live stimuli to assess quantity discrimination in angelfish (Pterophyllum scalare).

Video playback is a widely used technique for presentation of visual stimuli in animal behavior research. In the analysis of behavioral responses to social cues, presentation of video recordings of live conspecifics represents a consistently reproducible stimulus. However, video-recordings do not interact with the experimental subject, and thus this stimulus may be inferior in the social context. Here, we evaluated how angelfish (Pterophyllum scalare) respond to a video playback of conspecifics versus a live shoal of conspecifics. Using binary choice tests, subjects were presented different stimuli. Time spent close to one versus the other stimulus was considered an index of preference. We found angelfish to prefer a live shoal of conspecifics to an empty tank, and also the video playback of a shoal of conspecifics to a blank screen, although the level of preference in the latter was lower than in the former. These results indicate that video-playback of live conspecifics may be appropriate in angelfish, thus allowing manipulation of specific cues that angelfish may use in quantity discrimination. However, when we directly contrasted a live and a video recorded shoal, both having the same number of members, experimental fish preferred the live shoal. When the choice consisted of a live shoal of four conspecifics versus a video playback of a shoal of nine conspecifics no clear preference emerged. These results imply that video-playback has disadvantages in quantity discrimination studies with angelfish. Exploring procedural and/or technological parameters will verify the suitability of video-recording-based stimulus presentation for future use in angelfish.

Towards a standardization of non-symbolic numerical experiments: GeNEsIS, a flexible and user-friendly tool to generate controlled stimuli.

Several studies have suggested that vertebrate and invertebrate species may possess a number sense, i.e. an ability to process in a non-symbolic and non-verbal way the numerousness of a set of items. However, this hypothesis has been challenged by the presence of other non-numerical continuous physical variables, which vary along with numerosity (i.e., any change in the number of visual physical elements in a set naturally involves a related change in visual features such as area, density, contour length and convex hull of the stimulus). It is therefore necessary to control and manipulate the continuous physical information when investigating the ability of humans and other animals to perceive numerousness. During decades of research, different methods have been implemented in order to address this issue, which has implications for experiment replicability and inter-species comparisons, since no general standardized procedure is currently being used. Here we present the 'Generation of Numerical Elements Images Software' (GeNEsIS) for the creation of non-symbolic numerical arrays in a standardized and user-friendly environment. The main aim of this tool is to provide researchers in the field of numerical cognition a manageable and precise instrument to produce visual numerical arrays controlled for all the continuous variables. Additionally, we implemented the ability to actively guide stimuli presentation during habituation/dishabituation and dual-choice comparison tasks used in human and comparative research.

Giraffes go for more: a quantity discrimination study in giraffes (Giraffa camelopardalis).

Many species, including humans, rely on an ability to differentiate between quantities to make decisions about social relationships, territories, and food. This study is the first to investigate whether giraffes (Giraffa camelopardalis) are able to select the larger of two sets of quantities in different conditions, and how size and density affect these decisions. In Task 1, we presented five captive giraffes with two sets containing a different quantity of identical foods items. In Tasks 2 and 3, we also modified the size and density of the food reward distribution. The results showed that giraffes (i) can successfully make quantity judgments following Weber's law, (ii) can reliably rely on size to maximize their food income, and (iii) are more successful when comparing sparser than denser distributions. More studies on different taxa are needed to understand whether specific selective pressures have favored the evolution of these skills in certain taxa.

Neural representational similarity between symbolic and non-symbolic quantities predicts arithmetic skills in childhood but not adolescence.

Mathematical knowledge is constructed hierarchically from basic understanding of quantities and the symbols that denote them. Discrimination of numerical quantity in both symbolic and non-symbolic formats has been linked to mathematical problem-solving abilities. However, little is known of the extent to which overlap in quantity representations between symbolic and non-symbolic formats is related to individual differences in numerical problem solving and whether this relation changes with different stages of development and skill acquisition. Here we investigate the association between neural representational similarity (NRS) across symbolic and non-symbolic quantity discrimination and arithmetic problem-solving skills in early and late developmental stages: elementary school children (ages 7-10 years) and adolescents and young adults (AYA, ages 14-21 years). In children, cross-format NRS in distributed brain regions, including parietal and frontal cortices and the hippocampus, was positively correlated with arithmetic skills. In contrast, no brain region showed a significant association between cross-format NRS and arithmetic skills in the AYA group. Our findings suggest that the relationship between symbolic-non-symbolic NRS and arithmetic skills depends on developmental stage. Taken together, our study provides evidence for both mapping and estrangement hypotheses in the context of numerical problem solving, albeit over different cognitive developmental stages.

The olfactory capability of dogs to discriminate between different quantities of food.

A previous study failed to find evidence that dogs could use olfactory cues to discriminate between 1 and 5 hot dog slices presented on a single trial (Horowitz et al., Learning and Motivation, 44, 207-217, 2013). In the experiments reported here, multiple trials were used to test dogs' ability to use olfaction to choose one of two opaque containers under which a larger number of food items was placed. In Experiment 1, dogs chose between 1 and 5 hot dog slices. In Experiments 2 and 3, we examined dogs' ability to discriminate between numbers of hot dog slices that varied in the numerical distance and the ratio between the smaller and larger quantities. Experiment 4 explored olfactory discrimination between quantities of a different food, dog kibble. Experiments 1-3 all showed that dogs used olfactory stimuli to choose the larger number of hot dog slices, but Experiments 2 and 3 revealed no effects of distance or ratio between numerical quantities. In Experiment 4, dogs failed to discriminate between 1 and 5 pieces of dog kibble. Factors that allow dogs to use olfactory cues to discriminate between quantities are discussed.

Food density and preferred quantity: discrimination of small and large numbers in angelfish (Pterophyllum scalare).

Many animal species share the ability to discriminate between sets with different quantity of food items. In fish, this ability has rarely been investigated, although findings have been obtained do indicate a preference, as in other animals, for sets with large over small quantities. The role played by food item size has also been found to be important in the discrimination. However, another potentially important non-numerical variable, food density, has not been investigated. In this study, we examined the influence of density (inter-item distance) in the decision-making process of food discrimination in angelfish (Pterophyllum scalare). In a binary choice task, we kept the number and size of food items constant, but contrasted a set containing food items spaced further apart (sparse set) to another set with food items spaced more closely (dense set). We conducted this analysis with sets in the small (3 vs 3 food items) and in the large number range (5 vs 5 food items) and also varied the specific spatial arrangements of the food items in the sets. Contrary to expectations, angelfish showed a preference for the sparse sets over the dense sets in the five vs five contrasts irrespective of the specific spatial arrangement, but exhibited no preference in case of the three vs three contrasts. Subsequently, we slightly lengthened the inter-item distance in the dense sets, and found preference for the dense over the sparse sets. Last, we further examined the potential effect of spatial configuration of the items in the sets, but found no effect of this latter factor. Overall, these results indicate that higher density of the contrasted food item sets significantly influences choice in angelfish, which prefer denser sets if a clear discriminability of each individual item within the sets is provided.

Food quantity discrimination in puppies (Canis lupus familiaris).

There is considerable evidence that animals are able to discriminate between quantities. Despite the fact that quantitative skills have been extensively studied in adult individuals, research on their development in early life is restricted to a limited number of species. We, therefore, investigated whether 2-month-old puppies could spontaneously discriminate between different quantities of food items. We used a simultaneous two-choice task in which puppies were presented with three numerical combinations of pieces of food (1 vs. 8, 1 vs. 6 and 1 vs. 4), and they were allowed to select only one option. The subjects chose the larger of the two quantities in the 1 vs. 8 and the 1 vs. 6 combinations but not in the 1 vs. 4 combination. Furthermore, the last quantity the puppies looked at before making their choice and the time spent looking at the larger/smaller amounts of food were predictive of the choices they made. Since adult dogs are capable of discriminating between more difficult numerical contrasts when tested with similar tasks, our findings suggest that the capacity to discriminate between quantities is already present at an early age, but that it is limited to very easy discriminations.

Revisiting more or less: influence of numerosity and size on potential prey choice in the domestic cat.

Quantity discrimination is of adaptive relevance in a wide range of contexts and across a wide range of species. Trained domestic cats can discriminate between different numbers of dots, and we have shown that they also spontaneously choose between different numbers and sizes of food balls. In the present study we performed two experiments with 24 adult cats to investigate spontaneous quantity discrimination in the more naturalistic context of potential predation. In Experiment 1 we presented each cat with the simultaneous choice between a different number of live prey (1 white mouse vs. 3 white mice), and in Experiment 2 with the simultaneous choice between live prey of different size (1 white mouse vs. 1 white rat). We repeated each experiment six times across 6 weeks, testing half the cats first in Experiment 1 and then in Experiment 2, and the other half in the reverse order. In Experiment 1 the cats more often chose the larger number of small prey (3 mice), and in Experiment 2, more often the small size prey (a mouse). They also showed repeatable individual differences in the choices which they made and in the performance of associated predation-like behaviours. We conclude that domestic cats spontaneously discriminate between the number and size of potential prey in a way that can be interpreted as adaptive for a lone-hunting, obligate carnivore, and show complex levels of risk-reward analysis.

Surpassing the subitizing threshold: appetitive-aversive conditioning improves discrimination of numerosities in honeybees.

Animals including humans, fish and honeybees have demonstrated a quantity discrimination threshold at four objects, often known as subitizing elements. Discrimination between numerosities at or above the subitizing range is considered a complex capacity. In the current study, we trained and tested two groups of bees on their ability to differentiate between quantities (4 versus 5 through to 4 versus 8) when trained with different conditioning procedures. Bees trained with appetitive (reward) differential conditioning demonstrated no significant learning of this task, and limited discrimination above the subitizing range. In contrast, bees trained using appetitive-aversive (reward-aversion) differential conditioning demonstrated significant learning and subsequent discrimination of all tested comparisons from 4 versus 5 to 4 versus 8. Our results show conditioning procedure is vital to performance on numerically challenging tasks, and may inform future research on numerical abilities in other animals.

Effects of breed group and development on dogs' willingness to follow a human misleading advice.

The aim of this work was to investigate the effect of dog breed groups, i.e., primitive, hunting/herding and Mastiff like (Study 1) and development, i.e., 4-month-old puppies vs adults (Study 2) on a quantity discrimination task. The task consisted of three conditions: C1-dogs were asked to choose between a large and a small amount of food; C2-the same choice was presented and dogs could choose after having witnessed the experimenter favouring the small quantity. C3-similar to C2 but the plates had two equally small food quantities. Study 1 revealed that dogs in the hunting/herding group were significantly more likely than Mastiff-like group to choose the small quantity indicated by the person over the large one, although all dog groups chose the large quantity over the small when they had a free choice. These results are consistent with the hypothesis that hunting/herding breeds have been selected for working in cooperation with humans and thus may be more sensitive to human social communicative cues than other breeds. In Study 2, results showed that 4-month-old puppies performed at chance level in C1, whereas in C2 both adults and puppies conformed to the experimenter's choice. In C3, adults followed the experimenter significantly more than puppies, although puppies still followed the experimenter above chance. Overall, domestic dogs seem to rely heavily on social communicative cues from humans, even when the information contradicts their own perception. This tendency to respond to human social cues is present, although at a lesser extent already at 4 months.

Linear numerosity illusions in capuchin monkeys (Sapajus apella), rhesus macaques (Macaca mulatta), and humans (Homo sapiens).

Numerosity illusions emerge when the stimuli in one set are overestimated or underestimated relative to the number (or quantity) of stimuli in another set. In the case of multi-item arrays, individual items that form a better Gestalt are more readily grouped, leading to overestimation by human adults and children. As an example, the Solitaire illusion emerges when dots forming a central cluster (cross-pattern) are overestimated relative to the same number of dots on the periphery of the array. Although this illusion is robustly experienced by human adults, previous studies have produced weaker illusory results for young children, chimpanzees, rhesus macaques, capuchin monkeys, and guppies. In the current study, we presented nonhuman primates with other linear arrangements of stimuli from Frith and Frith's (Percept Psychoph 11:409-410, 1972) original paper with human participants that included the Solitaire illusion. Capuchin monkeys, rhesus macaques, and human adults learned to quantify black and white dots that were presented within intermingled arrays, responding on the basis of the more numerous dot colors. Humans perceived the various illusions similar to the original findings of Frith and Frith (1972), validating the current comparative design; however, there was no evidence of illusory susceptibility in either species of monkey. These results are considered in light of illusion susceptibility among primates as well as considering the role of numerical discrimination abilities and perceptual processing mode on illusion emergence.