Automatic processing of numerosity in human neocortex evidenced by occipital and parietal neuromagnetic responses

Abstract

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. Significance StatementApproximating the number of items in a set has been identified as a building block of mathematical cognition but the processing of numerosity is not fully understood. The natural correlation between numerosity and other visual features makes it difficult to test whether the number of items is a perceptual primitive or whether it needs to be recombined at a higher level. We used frequency-tagged magnetoencephalography to localize the implicit discrimination of numerosity within the visual hierarchy. We found that numerosity yielded occipital responses, supporting that the human visual system can grasp it at a single glance. Crucially, numerosity also yielded specific parietal responses, showing that numerosity is a perceptual primitive with a unique automatic involvement of parietal cortex.