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.

Perceptual History Biases Are Predicted by Early Visual-Evoked Activity.

What we see in the present is affected by what we saw in the recent past. Serial dependence, a bias making a current stimulus appear more similar to a previous one, has been indeed shown to be ubiquitous in vision. At the neural level, serial dependence is accompanied by a signature of stimulus history (i.e., past stimulus information) emerging from early visual-evoked activity. However, whether this neural signature effectively reflects the behavioral bias is unclear. Here we address this question by assessing the neural (electrophysiological) and behavioral signature of stimulus history in human subjects (both male and female), in the context of numerosity, duration, and size perception. First, our results show that while the behavioral effect is task-dependent, its neural signature also reflects task-irrelevant dimensions of a past stimulus, suggesting a partial dissociation between the mechanisms mediating the encoding of stimulus history and the behavioral bias itself. Second, we show that performing a task is not a necessary condition to observe the neural signature of stimulus history, but that in the presence of an active task such a signature is significantly amplified. Finally, and more importantly, we show that the pattern of brain activity in a relatively early latency window (starting at ∼35-65 ms after stimulus onset) significantly predicts the behavioral effect. Overall, our results thus demonstrate that the encoding of past stimulus information in neural signals does indeed reflect serial dependence, and that serial dependence occurs at a relatively early level of visual processing.SIGNIFICANCE STATEMENT What we perceive is determined not only by the information reaching our sensory organs, but also by the context in which the information is embedded. What we saw in the recent past (perceptual history) can indeed modulate the perception of a current stimulus in an attractive way, a bias that is ubiquitous in vision. Here we show that this bias can be predicted by the pattern of brain activity reflecting the encoding of past stimulus information, very early after the onset of a stimulus. This in turn suggests that the integration of past and present sensory information mediating the attractive bias occurs early in the visual processing stream, and likely involves early visual cortices.

The nature of magnitude integration: Contextual interference versus active magnitude binding.

Magnitude dimensions such as duration and numerosity have been shown to systematically interact, biasing each other in a congruent fashion: the more numerous a set of items is, the longer it is perceived to last in time. This integration between dimensions plays an important role in defining how we perceive magnitude. So far, however, the nature of magnitude integration remains unclear. Is magnitude integration a contextual interference, occurring whenever different types of information are concurrently available in the visual field, or does it involve an active "binding" of the different dimensions of the same object? To address these possibilities, we measured the integration bias induced by numerosity on perceived duration, in two cases: with duration and numerosity conveyed by distinct stimuli, or by the same stimulus. We show that a congruent integration effect can be observed only when the two magnitudes belong to the same stimulus. Instead, when the two magnitudes are conveyed by distinct stimuli, we observed an opposite effect. These findings demonstrate for the first time that a congruent integration occurs only between the dimensions of the same stimulus, suggesting the involvement of an active mechanism integrating the different dimensions of the same object in a unified percept.

Deprivation of Auditory Experience Influences Numerosity Discrimination, but Not Numerosity Estimation.

Number sense is the ability to estimate the number of items, and it is common to many species. Despite the numerous studies dedicated to unveiling how numerosity is processed in the human brain, to date, it is not clear whether the representation of numerosity is supported by a single general mechanism or by multiple mechanisms. Since it is known that deafness entails a selective impairment in the processing of temporal information, we assessed the approximate numerical abilities of deaf individuals to disentangle these two hypotheses. We used a numerosity discrimination task (2AFC) and an estimation task, in both cases using sequential (temporal) or simultaneous (spatial) stimuli. The results showed a selective impairment of the deaf participants compared with the controls (hearing) in the temporal numerosity discrimination task, while no difference was found to discriminate spatial numerosity. Interestingly, the deaf and hearing participants did not differ in spatial or temporal numerosity estimation. Overall, our results suggest that the deficit in temporal processing induced by deafness also impacts perception in other domains such as numerosity, where sensory information is conveyed in a temporal format, which further suggests the existence of separate mechanisms subserving the processing of temporal and spatial numerosity.

The specious interaction of time and numerosity perception.

Magnitude information is essential to create a representation of the external environment and successfully interact with it. Duration and numerosity, for example, can shape our predictions and bias each other (i.e. the greater the number of people queuing, the longer we expect to wait). While these biases suggest the existence of a generalized magnitude system, asymmetric effects (i.e. numerosity affecting duration but not vice versa) challenged this idea. Here, we propose that such asymmetric integration depends on the stimuli used and the neural processing dynamics they entail. Across multiple behavioural experiments employing different stimulus presentation displays (static versus dynamic) and experimental manipulations known to bias numerosity and duration perceptions (i.e. connectedness and multisensory integration), we show that the integration between numerosity and time can be symmetrical if the stimuli entail a similar neural time-course and numerosity unfolds over time. Overall, these findings support the idea of a generalized magnitude system, but also highlight the role of early sensory processing in magnitude representation and integration.

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.

Serial dependence in time and numerosity perception is dimension-specific.

The perception of a visual event (e.g., a flock of birds) at the present moment can be biased by a previous perceptual experience (e.g., the perception of an earlier flock). Serial dependence is a perceptual bias whereby a current stimulus appears more similar to a previous one than it actually is. Whereas serial dependence emerges within several visual stimulus dimensions, whether it could simultaneously operate across different dimensions of the same stimulus (e.g., the numerosity and the duration of a visual pattern) remains unclear. Here we address this question by assessing the presence of serial dependence across duration and numerosity, two stimulus dimensions that are often associated and can bias each other. Participants performed either a duration or a numerosity discrimination task, in which they compared a constant reference with a variable test stimulus, varying along the task-relevant dimension (either duration or numerosity). Serial dependence was induced by a task-irrelevant inducer, that is, a stimulus presented before the reference and always varying in both duration and numerosity. The results show systematic serial dependencies only within the task-relevant stimulus dimension, that is, stimulus numerosity affects numerosity perception only, and duration affects duration perception only. Additionally, at least in the numerosity condition, the task-irrelevant dimension of the inducer (duration) had an opposite, repulsive effect. These findings thus show that attractive serial dependence operates in a highly specific fashion and does not transfer across different stimulus dimensions. Instead, the repulsive influence, possibly reflecting perceptual adaptation, can transfer from one dimension to another.

Tactile numerosity is coded in external space.

Humans, and several non-human species, possess the ability to make approximate but reliable estimates of the number of objects around them. Alike other perceptual features, numerosity perception is susceptible to adaptation: exposure to a high number of items causes underestimation of the numerosity of a subsequent set of items, and vice versa. Several studies have investigated adaptation in the auditory and visual modality, whereby stimuli are preferentially encoded in an external coordinate system. As tactile stimuli are primarily coded in an internal (body-centered) reference frame, here we ask whether tactile numerosity adaptation operates based on internal or external spatial coordinates as it occurs in vision or audition. Twenty participants performed an adaptation task with their right hand located either in the right (uncrossed) or left (crossed) hemispace, in order for the two hands to occupy either two completely different positions, or the same position in space, respectively. Tactile adaptor and test stimuli were passively delivered either to the same (adapted) or different (non-adapted) hands. Our results show a clear signature of tactile numerosity adaptation aftereffects with a pattern of over- and under-estimation according to the adaptation rate (low and high, respectively). In the uncrossed position, we observed stronger adaptation effects when adaptor and test stimuli were delivered to the "adapted" hand. However, when both hands were aligned in the same spatial position (crossed condition), the magnitude of adaptation was similar irrespective of which hand received adaptor and test stimuli. These results demonstrate that numerosity information is automatically coded in external coordinates even in the tactile modality, suggesting that such a spatial reference frame is an intrinsic property of numerosity processing irrespective of the sensory modality.

The shared numerical representation for action and perception develops independently from vision.

Humans share with other animals a number sense, a system allowing a rapid and approximate estimate of the number of items in a scene. Recently, it has been shown that numerosity is shared between action and perception as the number of repetitions of self-produced actions affects the perceived numerosity of subsequent visual stimuli presented around the area where actions occurred. Here we investigate whether this interplay between action and perception for numerosity depends on visual input and visual experience. We measured the effects of adaptation to motor routines (finger tapping) on numerical estimates of auditory sequences in sighted and congenitally blind people. In both groups, our results show a consistent adaptation effect with relative under- or over-estimation of perceived auditory numerosity following rapid or slow tapping adaptation, respectively. Moreover, adaptation occurred around the tapping area irrespective of the hand posture (crossed or uncrossed hands), indicating that motor adaptation was coded using external (not hand-centred) coordinates in both groups. Overall, these results support the existence of a generalized interaction between action and perception for numerosity that occurs in external space and manifests independently of visual input or even visual experience.

Distortions of visual time induced by motor adaptation.

As perception of time is fundamental for action planning and execution, we investigated how action distorts the perception of visual duration. Participants adapted to tapping in midair for a few seconds, either slowly or quickly, then judged the relative duration of 2 drifting gratings, 1 spatially coincident with the tapped region and the other in the opposite field. Fast tapping decreased apparent duration in the tapping region while slow tapping increased it. The effect was spatially specific in external (not body-centered) coordinates, occurring within a 10° region centered on the tapping hand. Within this space, motor adaptation similarly distorts visual numerosity, suggesting common mechanisms for number and time. However, motor adaptation did not affect the perception of speed, a lower level visual property, suggesting that the interactions were at a high level of processing. These results reinforce studies that suggest that visual time perception is coupled with action and suggest the existence of multiple local visuomotor clocks. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Motion-induced compression of perceived numerosity.

It has been recently proposed that space, time, and number might share a common representation in the brain. Evidence supporting this idea comes from adaptation studies demonstrating that prolonged exposure to a given stimulus feature distorts the perception of different characteristics. For example, visual motion adaptation affects both perceived position and duration of subsequent stimuli presented in the adapted location. Here, we tested whether motion adaptation also affects perceived numerosity, by testing the effect of adaptation to translating or rotating stimuli moving either at high (20 Hz) or low (5 Hz) speed. Adaptation to fast translational motion yielded a robust reduction in the apparent numerosity of the adapted stimulus (~25%) while adaptation to slow translational or circular motion (either 20 Hz or 5 Hz) yielded a weaker but still significant compression. Control experiments suggested that none of these results could be accounted for in terms of stimulus masking. Taken together, our results are consistent with the extant literature supporting the idea of a generalized magnitude system underlying the representation of numerosity, space and time via common metrics. However, as changes in perceived numerosity co-varied with both adapting motion profile and speed, our evidence also suggests complex and asymmetric interactions between different magnitude representations.

A shared numerical representation for action and perception.

Humans and other species have perceptual mechanisms dedicated to estimating approximate quantity: a sense of number. Here we show a clear interaction between self-produced actions and the perceived numerosity of subsequent visual stimuli. A short period of rapid finger-tapping (without sensory feedback) caused subjects to underestimate the number of visual stimuli presented near the tapping region; and a period of slow tapping caused overestimation. The distortions occurred both for stimuli presented sequentially (series of flashes) and simultaneously (clouds of dots); both for magnitude estimation and forced-choice comparison. The adaptation was spatially selective, primarily in external, real-world coordinates. Our results sit well with studies reporting links between perception and action, showing that vision and action share mechanisms that encode numbers: a generalized number sense, which estimates the number of self-generated as well as external events.

A generalized sense of number.

Much evidence has accumulated to suggest that many animals, including young human infants, possess an abstract sense of approximate quantity, a number sense. Most research has concentrated on apparent numerosity of spatial arrays of dots or other objects, but a truly abstract sense of number should be capable of encoding the numerosity of any set of discrete elements, however displayed and in whatever sensory modality. Here, we use the psychophysical technique of adaptation to study the sense of number for serially presented items. We show that numerosity of both auditory and visual sequences is greatly affected by prior adaptation to slow or rapid sequences of events. The adaptation to visual stimuli was spatially selective (in external, not retinal coordinates), pointing to a sensory rather than cognitive process. However, adaptation generalized across modalities, from auditory to visual and vice versa. Adaptation also generalized across formats: adapting to sequential streams of flashes affected the perceived numerosity of spatial arrays. All these results point to a perceptual system that transcends vision and audition to encode an abstract sense of number in space and in time.