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A network of topographic numerosity maps in human association cortex

Abstract

Sensory and motor cortices each contain multiple topographic maps with the structure of sensory organs (such as the retina or cochlea) mapped onto the cortical surface. These sensory maps are hierarchically organized. For example, visual field maps contain neurons that represent increasingly large parts of visual space with increasingly complex responses1. Some visual neurons respond to stimuli with a particular numerosity — the number of objects in a set. We recently discovered a parietal topographic numerosity map in which neural numerosity preferences progress gradually across the cortical surface2, analogous to sensory maps. Following this analogy, we hypothesized that there may be multiple numerosity maps. Numerosity perception is implicated in many cognitive functions, including foraging3, multiple object tracking4, dividing attention5, decision-making6 and mathematics79. Here we use ultra-high-field (7 Tesla, 7T) functional magnetic resonance imaging (fMRI) and neural-model-based analyses to reveal numerosity-selective neural populations organized into six widely separated topographic maps in each hemisphere. Although we describe subtle differences between these maps, their properties are very similar, unlike in sensory map hierarchies. These maps are found in areas implicated in object recognition, motion perception, attention control, decision-making and mathematics. Multiple numerosity maps may allow interactions with these cognitive systems, suggesting a broad role for quantity processing in supporting many perceptual and cognitive functions.

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Figure 1: Similar responses to numerosity in several brain regions.
Figure 2: Numerosity map network.
Figure 3: Differences in numerosity range and surface area between numerosity maps and hemispheres.
Figure 4: Numerosity tuning widths.

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Acknowledgements

This work was supported by Netherlands Organization for Scientific Research grants no. 452.08.008 to S.O.D. and no. 433.09.223 to S.O.D. and F. W. Cornelissen, and by Portuguese Foundation for Science and Technology grant no. IF/01405/2014 to B.M.H. The Spinoza Centre is a joint initiative of the University of Amsterdam, Academic Medical Centre, VU University, VU Medical Centre, Netherlands Institute for Neuroscience and the Royal Netherlands Academy of Arts and Sciences. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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B.M.H. and S.O.D. designed the study; B.M.H. collected and analysed data; B.M.H. wrote the manuscript with input from S.O.D.

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Correspondence to Ben M. Harvey.

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Harvey, B., Dumoulin, S. A network of topographic numerosity maps in human association cortex. Nat Hum Behav 1, 0036 (2017). https://doi.org/10.1038/s41562-016-0036

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