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Numerosity processing in early visual cortex

&NA; While parietal cortex is thought to be critical for representing numerical magnitudes, we recently reported an event‐related potential (ERP) study demonstrating selective neural sensitivity to numerosity over midline occipital sites very early in the time course, suggesting the involvement of early visual cortex in numerosity processing. However, which specific brain area underlies such early activation is not known. Here, we tested whether numerosity‐sensitive neural signatures arise specifically from the initial stages of visual cortex, aiming to localize the generator of these signals by taking advantage of the distinctive folding pattern of early occipital cortices around the calcarine sulcus, which predicts an inversion of polarity of ERPs arising from these areas when stimuli are presented in the upper versus lower visual field. Dot arrays, including 8–32 dots constructed systematically across various numerical and non‐numerical visual attributes, were presented randomly in either the upper or lower visual hemifields. Our results show that neural responses at about 90 ms post‐stimulus were robustly sensitive to numerosity. Moreover, the peculiar pattern of polarity inversion of numerosity‐sensitive activity at this stage suggested its generation primarily in V2 and V3. In contrast, numerosity‐sensitive ERP activity at occipito‐parietal channels later in the time course (210–230 ms) did not show polarity inversion, indicating a subsequent processing stage in the dorsal stream. Overall, these results demonstrate that numerosity processing begins in one of the earliest stages of the cortical visual stream. HighlightsWe tested for early visual cortical involvement in magnitude processing.Subjects viewed dot arrays presented in upper or lower visual field.This manipulation resulted in ERP polarity inversion, occurring in V2/V3.The ERPs were selectively sensitive to numerosity and less to non‐numerical cues.This demonstrates that numerosity processing starts in very early visual areas.

Distinct Neural Signatures for Very Small and Very Large Numerosities

Behavioral studies of numerical cognition have shown that perceptual threshold for numerosity discrimination depends on the range of numerical values to be estimated. Discrimination threshold is constant when comparing very small numerosities via the mechanism called subitizing, while it increases as a function of numerosity for numbers beyond that range governed by subitizing. However, when numerosity gets so large that the individual elements start to form a cluttered ensemble, discrimination threshold increases as a function of the square root of numerosity. These behavioral patterns suggest that our sense of number is not based on a unitary mechanism and is rather based on multiple numerosity processing mechanisms depending on the absolute numerosity to be estimated. In this study, we demonstrate neurophysiological evidence for such multiple mechanisms. Participants’ electroencephalogram (EEG) was recorded while they viewed arrays containing either very small (1–4) or very large (100–400) number of dots with systematic variations in non-numerical cues. A linear model that tested the effects of numerical and non-numerical cues on the visual-evoked potentials (VEPs) revealed strong neural sensitivity to numerosity around 160–180 ms over right occipito-parietal sites irrespective of the numerical range presented. In contrast, earlier neural responses (~100 ms) showed markedly distinct patterns across the different numerical ranges tested. These results indicate that differences in behavioral response patterns in numerosity estimation across various numerical ranges may arise from the differences in the first stages of visual analysis. Collectively, the findings provide a firmer ground for the idea that there exists a brain system specifically dedicated for numerosity processing, yet they also suggest that multiple early visual cortical mechanisms converge to that numerosity processing stage later in the visual stream.

Attractive Serial Dependence in the Absence of an Explicit Task

Attractive serial dependence refers to an adaptive change in the representation of sensory information, whereby a current stimulus appears to be similar to a previous one. The nature of this phenomenon is controversial, however, as serial dependence could arise from biased perceptual representations or from biased traces of working memory representation at a decisional stage. Here, we demonstrated a neural signature of serial dependence in numerosity perception emerging early in the visual processing stream even in the absence of an explicit task. Furthermore, a psychophysical experiment revealed that numerosity perception is biased by a previously presented stimulus in an attractive way, not by repulsive adaptation. These results suggest that serial dependence is a perceptual phenomenon starting from early levels of visual processing and occurring independently from a decision process, which is consistent with the view that these biases smooth out noise from neural signals to establish perceptual continuity.

Spatiotemporal feature integration shapes approximate numerical processing

Numerosity perception involves a complex cascade of processing stages comprising an early sensory representation stage followed by a later stage providing a conceptual representation of numerical magnitude. While much recent work has focused on understanding how nonnumerical spatial features (e.g., density, area) influence numerosity perception in this processing cascade, little is known about how the spatiotemporal properties of the stimuli affect numerosity processing. Whether numerosity information is integrated over space and time in the processing cascade is an important question as it can provide insights into how the system dedicated for numerosity interacts with other perceptual systems. To address these issues, in four independent experiments, we asked participants to judge the numerosities of various different kinds of dynamically presented dot arrays, such as dots randomly changing in their locations, moving in smooth trajectories, or flickering on and off. The results revealed a systematic overestimation of dynamically presented dot arrays, which implicates the existence of spatiotemporal integration mechanisms, both at the early sensory representation stage and the later conceptual representation stage. The results also revealed the influence of motion and color processing areas on numerosity processing. The findings thus provide empirical evidence that numerosity perception arises from a complex interaction between multiple perceptual mechanisms in the visual stream, and that it is shaped by the integration of spatiotemporal properties of visual stimuli.

Modality-specific temporal constraints for state-dependent interval timing

The ability to discriminate temporal intervals in the milliseconds-to-seconds range has been accounted for by proposing that duration is encoded in the dynamic change of a neuronal network state. A critical limitation of such networks is that their activity cannot immediately return to the initial state, a restriction that could hinder the processing of intervals presented in rapid succession. Empirical evidence in the literature consistently shows impaired duration discrimination performance for 100 ms intervals demarked by short auditory stimuli immediately preceded by a similar interval. Here we tested whether a similar interference is present with longer intervals (300 ms) demarked either by auditory or by visual stimuli. Our results show that while temporal estimates of auditory stimuli in this range are not affected by the interval between them, duration discrimination with this duration is significantly impaired with visual intervals presented in rapid succession. The difference in performance between modalities is overall consistent with state-dependent temporal computations, as it suggests that the limits due to slow neuronal dynamics greatly depends on the sensory modality with which the intervals are demarked, in line with the idea of intrinsic, modality-specific neural mechanisms for interval timing.

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.

Serial dependence in numerosity perception

Our conscious experience of the external world is remarkably stable and seamless, despite the intrinsically discontinuous and noisy nature of sensory information. Serial dependencies in visual perception—reflecting attractive biases making a current stimulus to appear more similar to previous ones—have been recently hypothesized to be involved in perceptual continuity. However, while these effects have been observed across a variety of visual features and at the neural level, several aspects of serial dependence and how it generalizes across visual dimensions is still unknown. Here we explore the behavioral signature of serial dependence in numerosity perception by assessing how the perceived numerosity of dot-array stimuli is biased by a task-irrelevant “inducer” stimulus presented before task-relevant stimuli. First, although prior work suggests that numerosity perception starts in the subcortex, the current study rules out a possible involvement of subcortical processing in serial dependence, confirming that the effect likely starts in the visual cortex. Second, we show that the effect is coarsely spatially localized to the position of the inducer stimulus. Third, we demonstrate that the effect is present even with a stimulus presentation procedure minimizing the involvement of post-perceptual processes, but only when participants actively pay attention to the inducer stimulus. Overall, these results provide a comprehensive characterization of serial dependencies in numerosity perception, demonstrating that attractive biases occur by means of spatially localized attentional modulations of early sensory activity.

Trans-saccadic integration of orientation information

Does visual processing start anew after each eye movement, or is information integrated across saccades? Here we test a strong prediction of the integration hypothesis: that information acquired after a saccade interferes with the perception of images acquired before the saccade. We investigate perception of a basic visual feature, grating orientation, and we take advantage of a delayed interference phenomenon-in human participants, the reported orientation of a target grating, briefly presented at an eccentric location, is strongly biased toward the orientation of flanker gratings that are flashed shortly after the target. Crucially, we find that the effect is the same whether or not a saccade is made during the delay interval even though the eye movement produces a large retinotopic separation between target and flankers. However, the trans-saccadic effect nearly vanishes when flankers are displaced to a different screen location even when this location matches the retinotopic coordinates of the target. We conclude that information about grating orientation is integrated across saccades within a spatial region that is defined in external coordinates and thereby is stable in spite of the movement of the eyes.

Early Numerosity Encoding in Visual Cortex Is Not Sufficient for the Representation of Numerical Magnitude

Recent studies have demonstrated that the numerosity of visually presented dot arrays is represented in low-level visual cortex extremely early in latency. However, whether or not such an early neural signature reflects the perceptual representation of numerosity remains unknown. Alternatively, such a signature may indicate the raw sensory representation of the dot-array stimulus before becoming the perceived representation of numerosity. Here, we addressed this question by using the connectedness illusion, whereby arrays with pairwise connected dots are perceived to be less numerous compared with arrays containing isolated dots. Using EEG and fMRI in two independent experiments, we measured neural responses to dot-array stimuli comprising 16 or 32 dots, either isolated or pairwise connected. The effect of connectedness, which reflects the segmentation of the visual stimulus into perceptual units, was observed in the neural activity after 150 msec post stimulus onset in the EEG experiment and in area V3 in the fMRI experiment using a multivariate pattern analysis. In contrast, earlier neural activity before 100 msec and in area V2 was strictly modulated by numerosity regardless of connectedness, suggesting that this early activity reflects the sensory representation of a dot array before perceptual segmentation. Our findings thus demonstrate that the neural representation for numerosity in early visual cortex is not sufficient for visual number perception and suggest that the perceptual encoding of numerosity occurs at or after the segmentation process that takes place later in area V3.

Looking for more food or more people? Task context influences basic numerosity perception

Approximate numerical magnitude (or numerosity) is thought to represent one of the fundamental sensory properties driving perceptual choices. Recent studies indicate that numerosity judgment on a dot array is primarily driven by its numerical magnitude, largely independent from its other non-numerical visual dimensions. Nevertheless, these findings do not preclude the possibility that non-numerical cues such as size or spacing of a dot array influence numerosity judgment. Here, we test the hypothesis that numerosity judgment is influenced by non-numerical dimensions of a dot array depending on the context to which those non-numerical cues could be useful. Participants were asked to choose the more numerous of two dot arrays in two different contexts that differed only in one aspect. In one condition, the task was framed as choosing a set with more fruits to consume. In the other condition, the task was framed as choosing a group with more people to join. The results demonstrate that the influence of non-numerical cues - and particularly of the dimension of size - was significantly smaller when participants made quantitative choices about people than when they made choices about food, illustrating that the representation of discrete magnitude is more pronounced in the former case. These findings suggest that the information pooled to reach a decision about numerosity is flexibly determined according to the context and the goals of such judgment.