The neural representation of numerosity zero in the parieto-frontal magnitude network

Abstract

A general magnitude system is hosted in the fronto-parietal network. Neurons in this system represent the number of visual items in a collection, but it is unknown whether this system encodes null quantity (zero). We recorded from the ventral intraparietal area (VIP) and the prefrontal cortex (PFC) of monkeys performing a matching task including empty sets and countable numerosities as stimuli. Monkeys treated empty sets according to the null quantity they represent. This was revealed by a behavioral distance effect: monkeys wrongly matched empty sets with numerosity one more frequently than with numerosity two. However, reaction times were longer than expected in empty set trials. We first explored whether empty sets find a place in the visual sense of number. For that purpose, we analyzed neural activity during the sample epoch, when numerosity is visually available to the monkey. We found that VIP neurons encoded empty sets predominantly as a distinct category from countable numerosities. In contrast, PFC neurons represented empty sets more similarly to numerosity one than to larger numerosities, exhibiting a numerical distance effect. Crucially, only prefrontal neurons represented empty sets abstractly and irrespective of stimulus variations. Moreover, compared to VIP, the sample activity of numerosity neurons in PFC better correlated with behavioral tuning functions and predicted the outcome of empty-set trials. In the context of previous results, this data suggests a hierarchy in the processing from VIP to PFC, along which empty sets are detached from visual properties and gradually positioned in a numerical continuum. These findings elucidate how the brain transforms the absence of countable items, ‘nothing’, into an abstract quantitative category, ‘zero’. Second, we analyzed the temporal dynamics triggered by the different stimuli in VIP and PFC during the course of a trial. We found that, in comparison to other stimuli, empty sets elicit later neuronal responses and a distinct temporal response profile in the parieto-frontal magnitude system. Particularly, empty set trials are characterized by a late top-down effect from PFC to VIP. Approximately 200 ms after sample presentation, we identified the start of a dynamic shift in the population tuning towards a categorical representation of empty sets, which continues during the delay period. Consequently, in working memory, empty sets are over-represented in comparison to other stimuli. Correspondingly, a higher percent of neurons was classified as empty-set neurons in the delay period. Altogether, our results provide evidence that prefrontal cortex plays a central role in attaching a quantitative value to the absence of countable items. The dominant role of PFC in the processing of empty sets suggests that zero is treated differently with respect to other numerosities. In the visual sense of number, countable numerosities, as salient stimuli, elicit bottom-up signals from the parietal cortex. In contrast, to be treated as endowed with numerosity zero, empty sets seem to require a top-down signal originating in PFC. untranslated Ausgewählte entfernen