Resources Underlying Visuo-Spatial Working Memory Enable Veridical Large Numerosity Perception

Humans can quickly approximate how many objects are in a visual image, but no clear consensus has been achieved on the cognitive resources underlying this ability. Previous work has lent support to the notion that mechanisms which explicitly represent the locations of multiple objects in the visual scene within a mental map are critical for both visuo-spatial working memory and enumeration (at least for relatively small numbers of items). Regarding the cognitive underpinnings of large numerosity perception, an issue currently subject to much controversy is why numerosity estimates are often non-veridical (i.e., susceptible to biases from non-numerical quantities). Such biases have been found to be particularly pronounced in individuals with developmental dyscalculia (DD), a learning disability affecting the acquisition of arithmetic skills. Motivated by findings showing that DD individuals are also often impaired in visuo-spatial working memory, we hypothesized that resources supporting this type of working memory, which allow for the simultaneous identification of multiple objects, might also be critical for precise and unbiased perception of larger numerosities. We therefore tested whether loading working memory of healthy adult participants during discrimination of large numerosities would lead to increased interference from non-numerical quantities. Participants performed a numerosity discrimination task on multi-item arrays in which numerical and non-numerical stimulus dimensions varied congruently or incongruently relative to each other, either in isolation or in the context of a concurrent visuo-spatial or verbal working memory task. During performance of the visuo-spatial, but not verbal, working memory task, precision in numerosity discrimination decreased, participants’ choices became strongly biased by item size, and the strength of this bias correlated with measures of arithmetical skills. Moreover, the interference between numerosity and working memory tasks was bidirectional, with number discrimination impacting visuo-spatial (but not verbal) performance. Overall, these results suggest that representing visual numerosity in a way that is unbiased by non-numerical quantities relies on processes which explicitly segregate/identify the locations of multiple objects that are shared with visuo-spatial (but not verbal) working memory. This shared resource may potentially be impaired in DD, explaining the observed co-occurrence of working memory and numerosity discrimination deficits in this clinical population.

Hierarchical drift diffusion modeling uncovers multisensory benefit in numerosity discrimination tasks

Studies of accuracy and reaction time in decision making often observe a speed-accuracy tradeoff, where either accuracy or reaction time is sacrificed for the other. While this effect may mask certain multisensory benefits in performance when accuracy and reaction time are separately measured, drift diffusion models (DDMs) are able to consider both simultaneously. However, drift diffusion models are often limited by large sample size requirements for reliable parameter estimation. One solution to this restriction is the use of hierarchical Bayesian estimation for DDM parameters. Here, we utilize hierarchical drift diffusion models (HDDMs) to reveal a multisensory advantage in auditory-visual numerosity discrimination tasks. By fitting this model with a modestly sized dataset, we also demonstrate that large sample sizes are not necessary for reliable parameter estimation.

Evidence for an A-Modal Number Sense: Numerosity Adaptation Generalizes Across Visual, Auditory, and Tactile Stimuli

Humans and other species share a perceptual mechanism dedicated to the representation of approximate quantities that allows to rapidly and reliably estimate the numerosity of a set of objects: an Approximate Number System (ANS). Numerosity perception shows a characteristic shared by all primary visual features: it is susceptible to adaptation. As a consequence of prolonged exposure to a large/small quantity (“adaptor”), the apparent numerosity of a subsequent (“test”) stimulus is distorted yielding a robust under- or over-estimation, respectively. Even if numerosity adaptation has been reported across several sensory modalities (vision, audition, and touch), suggesting the idea of a central and a-modal numerosity processing system, evidence for cross-modal effects are limited to vision and audition, two modalities that are known to preferentially encode sensory stimuli in an external coordinate system. Here we test whether numerosity adaptation for visual and auditory stimuli also distorts the perceived numerosity of tactile stimuli (and vice-versa) despite touch being a modality primarily coded in an internal (body-centered) reference frame. We measured numerosity discrimination of stimuli presented sequentially after adaptation to series of either few (around 2 Hz; low adaptation) or numerous (around 8 Hz; high adaptation) impulses for all possible combinations of visual, auditory, or tactile adapting and test stimuli. In all cases, adapting to few impulses yielded a significant overestimation of the test numerosity with the opposite occurring as a consequence of adaptation to numerous stimuli. The overall magnitude of adaptation was robust (around 30%) and rather similar for all sensory modality combinations. Overall, these findings support the idea of a truly generalized and a-modal mechanism for numerosity representation aimed to process numerical information independently from the sensory modality of the incoming signals.

Perception of geometric sequences and numerosity both predict formal geometric competence in primary school children

While most animals have a sense of number, only humans have developed symbolic systems to describe and organize mathematical knowledge. Some studies suggest that human arithmetical knowledge may be rooted in an ancient mechanism dedicated to perceiving numerosity, but it is not known if formal geometry also relies on basic, non-symbolic mechanisms. Here we show that primary-school children who spontaneously detect and predict geometrical sequences (non-symbolic geometry) perform better in school-based geometry tests indexing formal geometric knowledge. Interestingly, numerosity discrimination thresholds also predicted and explained a specific portion of variance of formal geometrical scores. The relation between these two non-symbolic systems and formal geometry was not explained by age or verbal reasoning skills. Overall, the results are in line with the hypothesis that some human-specific, symbolic systems are rooted in non-symbolic mechanisms.

Automatic Processing of Numerosity in Human Neocortex Evidenced by Occipital and Parietal Neuromagnetic Responses

Humans and other animal species are endowed with the ability to sense, represent, and mentally manipulate the number of items in a set without needing to count them. One central hypothesis is that this ability relies on an automated functional system dedicated to numerosity, the perception of the discrete numerical magnitude of a set of items. This system has classically been associated with intraparietal regions, however accumulating evidence in favor of an early visual number sense calls into question the functional role of parietal regions in numerosity processing. Targeting specifically numerosity among other visual features in the earliest stages of processing requires high temporal and spatial resolution. We used frequency-tagged magnetoencephalography (MEG) to investigate the early automatic processing of numerical magnitudes and measured the steady-state brain responses specifically evoked by numerical and other visual changes in the visual scene. The neuromagnetic responses showed implicit discrimination of numerosity, total occupied area, and convex hull. The source reconstruction corresponding to the implicit discrimination responses showed common and separate sources along the ventral and dorsal visual pathways. Occipital sources attested the perceptual salience of numerosity similarly to both other implicitly discriminable visual features. Crucially, we found parietal responses uniquely associated with numerosity discrimination, showing automatic processing of numerosity in the parietal cortex, even when not relevant to the task. Taken together, these results provide further insights into the functional roles of parietal and occipital regions in numerosity encoding along the visual hierarchy.

Characterising ontogeny of numerosity discrimination in zebrafish reveals use of multiple, numerical and non- numerical mechanisms

Non-symbolic number cognition based on an approximate sense of magnitude has been documented in adult zebrafish. Here we investigated the ontogeny of this ability using a group size preference task in juvenile zebrafish. Fish showed group size preference from 26 days post fertilization (dpf) and from 27 dpf fish reliably chose the larger group when presented with discrimination ratios from 1:8 to 2:3. When the ratio between the number of conspecifics in each group was maintained at 1:2, fish could discriminate between 1 vs. 2 individuals and 3 vs. 6, but not when given a choice between 2 vs. 4 individuals. These findings suggest that the systems involved in numerosity representation in fish do not operate separately from other cognitive mechanisms. Rather they suggest numerosity processing is the result of an interplay between attentional, cognitive and memory-related mechanisms that orchestrate numerical competence both in humans and animals. Our results emphasise the potential of the use of zebrafish to explore the genetic and neural processes underlying the ontogeny of number cognition.

Poor numerical performance of guppies tested in a Skinner box

We tested the hypothesis that part of the gap in numerical competence between fish and warm-blooded vertebrates might be related to the more efficient procedures (e.g. automated conditioning chambers) used to investigate the former and could be filled by adopting an adapted version of the Skinner box in fish. We trained guppies in a visual numerosity discrimination task, featuring two difficulty levels (3 vs. 5 and 3 vs. 4) and three conditions of congruency between numerical and non-numerical cues. Unexpectedly, guppies trained with the automated device showed a much worse performance compared to previous investigations employing more “ecological” procedures. Statistical analysis indicated that the guppies overall chose the correct stimulus more often than chance; however, their average accuracy did not exceed 60% correct responses. Learning measured as performance improvement over training was significant only for the stimuli with larger numerical difference. Additionally, the target numerosity was selected more often than chance level only for the set of stimuli in which area and number were fully congruent. Re-analysis of prior studies indicate that the gap between training with the Skinner box and with a naturalistic setting was present only for numerical discriminations, but not for colour and shape discriminations. We suggest that applying automated conditioning chambers to fish might increase cognitive load and therefore interfere with achievement of numerosity discriminations.

Do estimates of numerosity really adhere to Weber’s law? A reexamination of two case studies

Both humans and nonhuman animals can exhibit sensitivity to the approximate number of items in a visual array or events in a sequence, and across various paradigms, uncertainty in numerosity judgments increases with the number estimated or produced. The pattern of increase is usually described as exhibiting approximate adherence to Weber’s law, such that uncertainty increases proportionally to the mean estimate, resulting in a constant coefficient of variation. Such a pattern has been proposed to be a signature characteristic of an innate “number sense.” We reexamine published behavioral data from two studies that have been cited as prototypical evidence of adherence to Weber’s law and observe that in both cases variability increases less than this account would predict, as indicated by a decreasing coefficient of variation with an increase in number. We also consider evidence from numerosity discrimination studies that show deviations from the constant coefficient of variation pattern. Though behavioral data can sometimes exhibit approximate adherence to Weber’s law, our findings suggest that such adherence is not a fixed characteristic of the mechanisms whereby humans and animals estimate numerosity. We suggest instead that the observed pattern of increase in variability with number depends on the circumstances of the task and stimuli, and reflects an adaptive ensemble of mechanisms composed to optimize performance under these circumstances.

Efficient sampling and noisy decisions

Human decisions are based on finite information, which makes them inherently imprecise. But what determines the degree of such imprecision? Here, we develop an efficient coding framework for higher-level cognitive processes in which information is represented by a finite number of discrete samples. We characterize the sampling process that maximizes perceptual accuracy or fitness under the often-adopted assumption that full adaptation to an environmental distribution is possible, and show how the optimal process differs when detailed information about the current contextual distribution is costly. We tested this theory on a numerosity discrimination task, and found that humans efficiently adapt to contextual distributions, but in the way predicted by the model in which people must economize on environmental information. Thus, understanding decision behavior requires that we account for biological restrictions on information coding, challenging the often-adopted assumption of precise prior knowledge in higher-level decision systems.