The divisive normalization model of visual number sense: model predictions and experimental confirmation.

Our intuitive sense of number allows rapid estimation for the number of objects (numerosity) in a scene. How does the continuous nature of neural information processing create a discrete representation of number? A neurocomputational model with divisive normalization explains this process and existing data; however, a successful model should not only explain existing data but also generate novel predictions. Here, we experimentally test novel predictions of this model to evaluate its merit for explaining mechanisms of numerosity perception. We did so by consideration of the coherence illusion: the underestimation of number for arrays containing heterogeneous compared to homogeneous items. First, we established the existence of the coherence illusion for homogeneity manipulations of both area and orientation of items in an array. Second, despite the behavioral similarity, the divisive normalization model predicted that these two illusions should reflect activity in different stages of visual processing. Finally, visual evoked potentials from an electroencephalography experiment confirmed these predictions, showing that area and orientation coherence modulate brain responses at distinct latencies and topographies. These results demonstrate the utility of the divisive normalization model for explaining numerosity perception, according to which numerosity perception is a byproduct of canonical neurocomputations that exist throughout the visual pathway.

Number neurons in the nidopallium of young domestic chicks.

Numerical cognition is ubiquitous in the animal kingdom. Domestic chicks are a widely used developmental model for studying numerical cognition. Soon after hatching, chicks can perform sophisticated numerical tasks. Nevertheless, the neural basis of their numerical abilities has remained unknown. Here, we describe number neurons in the caudal nidopallium (functionally equivalent to the mammalian prefrontal cortex) of young domestic chicks. Number neurons that we found in young chicks showed remarkable similarities to those in the prefrontal cortex and caudal nidopallium of adult animals. Thus, our results suggest that numerosity perception based on number neurons might be an inborn feature of the vertebrate brain.

An insect brain organizes numbers on a left-to-right mental number line.

The "mental number line" (MNL) is a form of spatial numeric representation that associates small and large numbers with the left and right spaces, respectively. This spatio-numeric organization can be found in adult humans and has been related to cultural factors such as writing and reading habits. Yet, both human newborns and birds order numbers consistently with an MNL, thus raising the question of whether culture is a main explanation for MNL. Here, we explored the numeric sense of honey bees and show that after being trained to associate numbers with a sucrose reward, they order numbers not previously experienced from left to right according to their magnitude. Importantly, the location of a number on that scale varies with the reference number previously trained and does not depend on low-level cues present on numeric stimuli. We provide a series of neural explanations for this effect based on the extensive knowledge accumulated on the neural underpinnings of visual processing in honey bees and conclude that the MNL is a form of numeric representation that is evolutionarily conserved across nervous systems endowed with a sense of number, irrespective of their neural complexity.

Nonsymbolic Numerosity Maps at the Occipitotemporal Cortex Respond to Symbolic Numbers.

Numerosity, the set size of a group of items, helps guide human and animals' behavior and decisions. Numerosity perception is thought to be a precursor of symbolic numerical cognition. Previously, we uncovered neural populations selectively tuned to numerosities organized in a network of topographic maps in human association cortex. Here we investigate whether these numerosity maps are also involved in the processing of symbolic numbers, using 7T fMRI and a number-detection task. We recruited 7 participants (3 females) and found that the numerosity map at the temporal-occipital cortex (NTO) also responds to symbolic numbers. Furthermore, we found that numerosity-tuned neuronal populations at the NTO map in the left hemisphere are tuned to symbolic numbers. These results reveal different functions of the numerosity maps and support a link between numerosity representation and symbolic number processing in the ventral temporal-occipital cortex.SIGNIFICANCE STATEMENT Humans and other animals share an intuitive "number sense" to approximately represent numerosity. However, humans possess a unique ability to process number symbols (e.g., Arabic numbers). It has been argued that the human understanding of symbolic numbers is rooted in our ability to numerosity perception. Here we investigate whether numerosity-tuned neuronal populations organized at a network of topographic maps also respond to symbolic numbers. We find one of the maps at the temporal-occipital cortex is involved in symbolic numerical cognition and the neuronal populations are tuned to numbers. These results provide evidence for a link between nonsymbolic numerosity and symbolic number processing.

Cortical quantity representations of visual numerosity and timing overlap increasingly into superior cortices but remain distinct.

Many sensory brain areas are organized as topographic maps where neural response preferences change gradually across the cortical surface. Within association cortices, 7-Tesla fMRI and neural model-based analyses have also revealed many topographic maps for quantities like numerosity and event timing, often in similar locations. Numerical and temporal quantity estimations also show behavioral similarities and even interactions. For example, the duration of high-numerosity displays is perceived as longer than that of low-numerosity displays. Such interactions are often ascribed to a generalized magnitude system with shared neural responses across quantities. Anterior quantity responses are more closely linked to behavior. Here, we investigate whether common quantity representations hierarchically emerge by asking whether numerosity and timing maps become increasingly closely related in their overlap, response preferences, and topography. While the earliest quantity maps do not overlap, more superior maps overlap increasingly. In these overlapping areas, some intraparietal maps have consistently correlated numerosity and timing preferences, and some maps have consistent angles between the topographic progressions of numerosity and timing preferences. However, neither of these relationships increases hierarchically like the amount of overlap does. Therefore, responses to different quantities are initially derived separately, then progressively brought together, without generally becoming a common representation. Bringing together distinct responses to different quantities may underlie behavioral interactions and allow shared access to comparison and action planning systems.

Increased intra-individual variability among individuals with ADHD: first evidence from numerosity judgment and verbal and quantitative reasoning.

BACKGROUND: This article presents the results of two studies investigating increased intra-individual variability (IIV) in the performance of individuals with attention deficit hyperactivity disorder (ADHD), in two cognitive domains: numerosity judgments and quantitative and verbal reasoning. METHODS: Study 1, a pre-registered experiment, involved approximately 200 participants (42.66% female; mean age: 36.86; standard deviation of age: 10.70) making numerical judgments at two time-points. ADHD-symptom severity was assessed on a continuous scale. In Study 2, we collected the data of approximately 3000 examinees who had taken a high-stakes admissions test for higher education (assessing quantitative and verbal reasoning). The sample comprised only people formally diagnosed with ADHD. The control group consisted of approximately 200 000 examinees, none of whom presented with ADHD. RESULTS: The results of Study 1 revealed a positive correlation between IIV (distance between judgments at the two time-points) and ADHD symptom severity. The results of Study 2 demonstrated that IIV (distance between the scores on two test chapters assessing the same type of reasoning) was greater among examinees diagnosed with ADHD. In both studies, the findings persisted even after controlling for performance level. CONCLUSIONS: The results indicate that individuals with ADHD, v. those without, exhibit less consistent numerosity judgments and greater fluctuation in performance on verbal and quantitative reasoning. The measurement of the same psychological constructs appears to be less precise among individuals with ADHD compared to those without. We discuss the theoretical contributions and practical implications of our results for two fields: judgment and decision-making, and assessment.

Looks like home: numerosity, but not spatial frequency guides preference in zebrafish larvae (Danio rerio).

Despite their young age, zebrafish larvae have a well-developed visual system and can distinguish between different visual stimuli. First, we investigated if the first visual surroundings the larvae experience during the first days after hatching shape their habitat preference. Indeed, these animals seem to "imprint" on the first surroundings they see and select visual stimuli accordingly at 7 days post fertilization (dpf). In particular, if zebrafish larvae experience a bar background just after hatching, they later on prefer bars over white stimuli, and vice versa. We then used this acquired preference for bars to investigate innate numerical abilities. We wanted to specifically test if the zebrafish larvae show real numerical abilities or if they rely on a lower-level mechanism-i.e. spatial frequency-to discriminate between two different numerosities. When we matched the spatial frequency in stimuli with different numbers of bars, the larvae reliably selected the higher numerosity. A previous study has ruled out that 7 dpf zebrafish larvae use convex hull, cumulative surface area and density to choose between two numerosities. Therefore, our results indicate that zebrafish larvae rely on real numerical abilities rather than other cues, including spatial frequency, when spontaneously comparing two sets with different numbers of bars.

Behavior-related potentials from single-trial interindividual correlation between event related potentials and behavioral performance reveals right lateralized processing of numerosity.

Accumulated functional magnetic resonance imaging (fMRI) and electroencephalography evidence indicate that numerosity is first processed in the occipito-parietal cortex. fMRI evidence also indicates right-lateralized processing of numerosity, but there is no consistent evidence from event-related potential (ERP) studies. This study investigated the ERP of numerosity processing in the left, right, and bilateral visual fields. The single-trial ERP-behavioral correlation was applied to show how the ERP was associated with behavioral responses. The results showed a significant early behavioral-ERP correlation on the right N1 component when stimuli were presented in the left visual field rather than in the right visual field. The behavioral ERP correlation was termed BN1. There was bilateral BN1 based on the reaction time or error rate, but the right BN1 was larger than that the left BN1 when the stimulus was present in the bilateral visual field. Therefore, this study provided a new neural marker for individual differences in processing numerosity and suggested that processing numerosity was supported by the right occipito-parietal cortex.

Humans can sense large numbers of objects in a box by touch alone.

Everyday experiences suggest that a container, such as a box of cereal, can convey pertinent information about the nature and quantity of its content. This study investigated how well people can judge large quantities of objects in a container through haptic perception. Stimuli consisted of plastic drinking straws cut to "small" (1.5 cm) or "big" (4.5 cm) pieces contained in plastic food containers. Participants performed both a magnitude estimation of the number of objects and a direct estimation of the proportion of the container perceived to be filled with objects. Overall, participants demonstrated considerable accuracy for both tasks and irrespective of the size of the content. Post-experiment interviews revealed three potential strategies. Participants either focused on the container's contents, the excess space in the container, or the perceived weight of the container (content).

Silvia De Marchi (1929) on numerical estimation: A translation and commentary.

Vittorio Benussi (1878-1927) is known for numerous studies on optical illusions, visual and haptic perception, spatial and time perception. In Padova, he had a brilliant student who carefully worked on the topic of how people estimate numerosity, Silvia De Marchi (1897-1936). Her writings have never been translated into English before. Here we comment on her work and life, characterized also by the challenges faced by women in academia. The studies on perception of numerosity from her thesis were published as an article in 1929. We provide a translation from Italian, a redrawing of its 23 illustrations and of the graphs. It shows an original experimental approach and an anticipation of what later became known as magnitude estimation.

A color-digit Stroop task shows numerical influence on numerosity processing.

The numerical Stroop task involves presenting participants with two digits that differ in physical size and numerical value and asking them to report which digit had the larger size or value while ignoring the other dimension. Previous studies show that participants have difficulty ignoring the irrelevant dimension and thus have implications on the automaticity of numerical processing. The present study investigates the automatic influence of numerical value on numerosity processing in a novel Stroop-like task. In two experiments, participants were presented with digits made of colored stripes and asked to identify the number of different colors. In both experiments, interference and facilitation effects were found, supporting the automaticity of symbolic number processing and its influence on numerosity processing. These findings expand upon previous research on numerical as well as counting Stroop tasks, and have potential implications for studying interference and basic numerical processing in children and clinical populations.

Measuring temporal bias in sequential numerosity comparison.

While several methods have been proposed to assess the influence of continuous visual cues in parallel numerosity estimation, the impact of temporal magnitudes on sequential numerosity judgments has been largely ignored. To overcome this issue, we extend a recently proposed framework that makes it possible to separate the contribution of numerical and non-numerical information in numerosity comparison by introducing a novel stimulus space designed for sequential tasks. Our method systematically varies the temporal magnitudes embedded into event sequences through the orthogonal manipulation of numerosity and two latent factors, which we designate as "duration" and "temporal spacing". This allows us to measure the contribution of finer-grained temporal features on numerosity judgments in several sensory modalities. We validate the proposed method on two different experiments in both visual and auditory modalities: results show that adult participants discriminated sequences primarily by relying on numerosity, with similar acuity in the visual and auditory modality. However, participants were similarly influenced by non-numerical cues, such as the total duration of the stimuli, suggesting that temporal cues can significantly bias numerical processing. Our findings highlight the need to carefully consider the continuous properties of numerical stimuli in a sequential mode of presentation as well, with particular relevance in multimodal and cross-modal investigations. We provide the complete code for creating sequential stimuli and analyzing participants' responses.

Mental control of uncertainty.

Can you reduce uncertainty by thinking? Intuition suggests that this happens through the elusive process of attention: if we expend mental effort, we can increase the reliability of our sensory data. Models based on "rational inattention" formalize this idea in terms of a trade-off between the costs and benefits of attention. This paper surveys the origin of these models in economics, their connection to rate-distortion theory, and some of their recent applications to psychology and neuroscience. We also report new data from a numerosity judgment task in which we manipulate performance incentives. Consistent with rational inattention, people are able to improve performance on this task when incentivized, in part by increasing the reliability of their sensory data.

The more numerous the longer: how the integration between numerosity and time leads to a common neural response.

If you are stuck in a traffic jam, the more numerous the queuing cars are, the longer you expect to wait. Time and numerosity are stimulus dimensions often associated in the same percept and whose interaction can lead to misjudgements. At brain level it is unclear to which extent time and numerosity recruit same/different neural populations and how their perceptual integration leads to changes in these populations' responses. Here we used high-spatial-resolution functional magnetic resonance imaging with neural model-based analyses to investigate how the topographic representations of numerosity and time change when these dimensions are varied together on the same visual stimulus in a congruent (the more numerous the items, the longer the display time) or incongruent manner. Compared to baseline conditions, where only one dimension was changed at a time, the variation of both stimulus dimensions led to changes in neural population responses that became more sensitive either to the two features or to one of them. Magnitude integration led also to degradation of topographies and shifts in response preferences. These changes were more pronounced in the comparison between parietal and frontal maps. Our results while pointing to partially distinct representations of time and numerosity show a common neural response to magnitude integration.

The influence of visual illusion perception on numerosity estimation could be evolutionarily conserved: exploring the numerical Delboeuf illusion in humans (Homo sapiens) and fish (Poecilia reticulata).

Discriminating between different quantities is an essential ability in daily life that has been demonstrated in a variety of non-human vertebrates. Nonetheless, what drives the estimation of numerosity is not fully understood, as numerosity intrinsically covaries with several other physical characteristics. There is wide debate as to whether the numerical and spatial abilities of vertebrates are processed by a single magnitude system or two different cognitive systems. Adopting a novel approach, we aimed to investigate this issue by assessing the interaction between area size and numerosity, which has never been conceptualized with consideration for subjective experience in non-human animals. We examined whether the same perceptual biases underlying one of the best-known size illusions, the Delboeuf illusion, can be also identified in numerical estimation tasks. We instructed or trained human participants and guppies, small teleost fish, to select a target numerosity (larger or smaller) of squares between two sets that actually differed in their numerosity. Subjects were also presented with illusory trials in which the same numerosity was presented in two different contexts, against a large and a small background, resembling the Delboeuf illusion. In these trials, both humans and fish demonstrated numerical biases in agreement with the perception of the classical version of the Delboeuf illusion, with the array perceived as larger appearing more numerous. Thus, our results support the hypothesis of a single magnitude system, as perceptual biases that influence spatial decisions seem to affect numerosity judgements in the same way.

Mario Ponzo (1928) on perception of numerosity: A translation and commentary.

Ponzo is a familiar name in psychology because of the illusion that takes his name. He had a long and productive career in Italy, and some of his work was translated for international journals already in his lifetime. However, few of these papers are available in English. We provide a commentary that considers how his name came to be associated with an illusion he did not discover. We explain the content of several papers, some of which are often cited in a wrong context in the literature (i.e., papers on touch mentioned in relation to the Ponzo illusion). More importantly, we discuss his contribution to the study of perceived numerosity, and provide a full translation of his important 1928 paper, including a redrawing of its 28 illustrations.

Humans can sense small numbers of objects in a box by touch alone.

Everyday experiences suggest that a container, such as a box of chocolate sprinkles, can convey pertinent information about the nature of its content. Despite the familiarity of the experience, we do not know whether people can perceive the number of objects in the container from touch alone and how accurately they can do so. In three experiments, participants handled containers holding between one and five objects and verbally estimated their number. Containers were small cardboard jewelry boxes, and objects were round beads of varying diameter and weight. Any useful visual and auditory cues were precluded. Experiment 1 demonstrated very accurate performance, provided the objects were of sufficient weight. Experiment 2 demonstrated that withholding information about the possible number of objects inside the container does not affect accuracy at a group level but does produce occasional overestimations at an individual level. Experiment 3 demonstrated that removing the weight cue leads to systematic underestimations but does not eliminate people's ability to distinguish between different numbers of objects in the container. This study contributes to a growing picture that container haptics is surprisingly capable.

Does auditory numerosity and non-numerical magnitude affect visual non-symbolic numerical representation?

In the present study, we investigated the effects of auditory numerosity and magnitude (loudness) on visual numerosity processing. Participants compared numerosities of two sequential dot arrays. The second dot array was paired with a tone array that was independent of visual comparison. The numerosity (One-tone vs. Multiple-tone) and the non-numerical magnitude of tones (loudness) were manipulated in Experiments 1 and 2, respectively. In Experiment 1, participants' inverse efficiency score (IES), that is, the quotient between response time and accuracy, was significantly smaller in the One-tone and Multiple-tone conditions than that in the No-tone condition, and linear trend analyses showed that the IES decreased with the number of tones. In Experiment 2, the IES in the Loud-tone condition was significantly smaller than that in the No-tone condition, and the IES decreased as the loudness of the tones increased. In Experiment 3, both auditory numerosity and magnitude were manipulated. For soft tones, the IES was smaller in the Multiple-tone condition than in the One-tone condition, whereas no significant difference was found between two conditions in loud tones. In sum, these findings suggest that the visual numerical representation can be spontaneously affected by the numerosity and non-numerical magnitude of stimuli from another modality.

The neural signature of numerosity by separating numerical and continuous magnitude extraction in visual cortex with frequency-tagged EEG.

The ability to handle approximate quantities, or number sense, has been recurrently linked to mathematical skills, although the nature of the mechanism allowing to extract numerical information (i.e., numerosity) from environmental stimuli is still debated. A set of objects is indeed not only characterized by its numerosity but also by other features, such as the summed area occupied by the elements, which often covary with numerosity. These intrinsic relations between numerosity and nonnumerical magnitudes led some authors to argue that numerosity is not independently processed but extracted through a weighting of continuous magnitudes. This view cannot be properly tested through classic behavioral and neuroimaging approaches due to these intrinsic correlations. The current study used a frequency-tagging EEG approach to separately measure responses to numerosity as well as to continuous magnitudes. We recorded occipital responses to numerosity, total area, and convex hull changes but not to density and dot size. We additionally applied a model predicting primary visual cortex responses to the set of stimuli. The model output was closely aligned with our electrophysiological data, since it predicted discrimination only for numerosity, total area, and convex hull. Our findings thus demonstrate that numerosity can be independently processed at an early stage in the visual cortex, even when completely isolated from other magnitude changes. The similar implicit discrimination for numerosity as for some continuous magnitudes, which correspond to basic visual percepts, shows that both can be extracted independently, hence substantiating the nature of numerosity as a primary feature of the visual scene.

Increased Functional Connectivity of the Intraparietal Sulcus Underlies the Attenuation of Numerosity Estimations for Self-Generated Words.

Previous studies have shown that self-generated stimuli in auditory, visual, and somatosensory domains are attenuated, producing decreased behavioral and neural responses compared with the same stimuli that are externally generated. Yet, whether such attenuation also occurs for higher-level cognitive functions beyond sensorimotor processing remains unknown. In this study, we assessed whether cognitive functions such as numerosity estimations are subject to attenuation in 56 healthy participants (32 women). We designed a task allowing the controlled comparison of numerosity estimations for self-generated (active condition) and externally generated (passive condition) words. Our behavioral results showed a larger underestimation of self-generated compared with externally generated words, suggesting that numerosity estimations for self-generated words are attenuated. Moreover, the linear relationship between the reported and actual number of words was stronger for self-generated words, although the ability to track errors about numerosity estimations was similar across conditions. Neuroimaging results revealed that numerosity underestimation involved increased functional connectivity between the right intraparietal sulcus and an extended network (bilateral supplementary motor area, left inferior parietal lobule, and left superior temporal gyrus) when estimating the number of self-generated versus externally generated words. We interpret our results in light of two models of attenuation and discuss their perceptual versus cognitive origins.SIGNIFICANCE STATEMENT We perceive sensory events as less intense when they are self-generated compared with when they are externally generated. This phenomenon, called attenuation, enables us to distinguish sensory events from self and external origins. Here, we designed a novel fMRI paradigm to assess whether cognitive processes such as numerosity estimations are also subject to attenuation. When asking participants to estimate the number of words they had generated or passively heard, we found bigger underestimation in the former case, providing behavioral evidence of attenuation. Attenuation was associated with increased functional connectivity of the intraparietal sulcus, a region involved in numerosity processing. Together, our results indicate that the attenuation of self-generated stimuli is not limited to sensory consequences but is also impact cognitive processes such as numerosity estimations.