Topographic Representation of Numerosity in the Human Parietal Cortex

Harvey, Ben M.; Klein, Barrie P.; Petridou, Natalia; Dumoulin, Serge O.

doi:10.1126/science.1239052

Cited by 446 publications

(618 citation statements)

References 65 publications

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“…Instead, the aIPS math sites were active only when subjects were required to interpret and manipulate numerals actively in the context of judging arithmetic statements. The aIPS math region we identify here is anatomically similar to the parietal regions in which previous studies have observed numerosity tuning in humans (24,71,72) and in macaques (4,73,74). However, although we are confident about the selective functional engagement of aIPS math sites during numerical processing, we are cognizant that future work is needed to disentangle further the functional roles of the aIPS math sites and nearby sites within different domains of numerical cognition.…”

Section: Numerical Processing In Discrete Neuronal Populations Withinmentioning

confidence: 67%

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

Daitch

Foster

Schrouff

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Brain areas within the lateral parietal cortex (LPC) and ventral temporal cortex (VTC) have been shown to code for abstract quantity representations and for symbolic numerical representations, respectively. To explore the fast dynamics of activity within each region and the interaction between them, we used electrocorticography recordings from 16 neurosurgical subjects implanted with grids of electrodes over these two regions and tracked the activity within and between the regions as subjects performed three different numerical tasks. Although our results reconfirm the presence of math-selective hubs within the VTC and LPC, we report here a remarkable heterogeneity of neural responses within each region at both millimeter and millisecond scales. Moreover, we show that the heterogeneity of response profiles within each hub mirrors the distinct patterns of functional coupling between them. Our results support the existence of multiple bidirectional functional loops operating between discrete populations of neurons within the VTC and LPC during the visual processing of numerals and the performance of arithmetic functions. These findings reveal information about the dynamics of numerical processing in the brain and also provide insight into the fine-grained functional architecture and connectivity within the human brain.A lthough the ability to approximate or compare rough quantities is present even in human infants (1) and in other species such as nonhuman primates (2-4) and birds (5), the association of exact quantities with symbols (e.g., the numeral "10") or verbal representations (e.g., the word "ten") is unique to humans exposed to such culturally learned entities (6-8). Moreover, dissociable number-and quantity-related behavioral deficits (i.e., deficits relating to symbolic or verbal numerical representations versus abstract quantity representations) are associated with different lesion locations within the brain (9-14). These observations in part motivated the Triple Code model positing that the human brain contains three different numerical representations: symbolic, verbal, and abstract quantity, each coded in a different brain region (15,16). The model also predicts that, depending on task demands (e.g., simple visual recognition of a numeral versus determining the larger of two numerals versus verbal naming of a numeral), all or a subset of these brain regions interact with each other (15, 16).Neuroimaging, electrophysiology, and lesion studies in both humans and nonhuman primates have long implicated the parietal lobe, particularly the anterior segment of the intraparietal sulcus (aIPS), in abstract quantity representations irrespective of the modality of presentation (e.g., "4" vs. "four" vs. "::"), with specific neurons or neuronal populations exhibiting tuning around a preferred numerosity (4, 17-25). Moreover, brain activity within this region and its functional and anatomical connectivity with other brain regions are correlated with mathematical performance in individual subjects (26)(27)(28)(29),...

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Section: Numerical Processing In Discrete Neuronal Populations Withinmentioning

confidence: 67%

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

Daitch

Foster

Schrouff

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…6), reflecting common topographical organization across stimulus configurations and repeated measures. However, numerosity preferences from the configuration with constant-perimeter stimuli were consistently less well correlated with preferences from other stimulus configurations 2,13 . The numerosity maps for the left and right hemispheres represented different numerosity ranges.…”

mentioning

confidence: 90%

“…We distinguished between responses to numerosity and co-varying stimulus features using several stimulus configurations 2,16 . We summarized the fMRI responses using numerosity-selective population receptive field (pRF) models with two parameters: preferred numerosity and tuning width.…”

mentioning

confidence: 99%

A network of topographic numerosity maps in human association cortex

2017

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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 responses 1 . Some visual neurons respond to stimuli with a particular numerositythe number of objects in a set. We recently discovered a parietal topographic numerosity map in which neural numerosity preferences progress gradually across the cortical surface . Here we use ultra-highfield (7 Tesla, 7T) functional magnetic resonance imaging (fMRI) and neural-model-based analyses to reveal numerosityselective 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.Topographic maps have an orderly organization of neurons with similar functions. The close proximity of neurons with similar functions minimizes local connection lengths to increase neural processing efficiency [10][11][12] . Furthermore, topographic maps allow simple one-to-one projections between maps. Finally, most neural processes are context-dependent. Topographic maps allow easy computations of context through comparisons between neighbouring neurons. Therefore, topographic organization has several benefits and gives a theoretical framework to explain why maps emerge in cognitive processing, as we recently demonstrated 2 and extend here. Together with this numerosity map, we also demonstrated that another quantity, object size, is processed in a distinct object size map that largely overlaps with this parietal numerosity map, showing correlated numerosity and object size preferences 13 . The parietal numerosity map that we have described encompasses part of a network implicated in numerosity processing, extending into occipital, parietal and frontal areas [14][15][16][17][18][19] . The fine-scale organization elsewhere in this numerosity network is unknown. We hypothesize that, like sensory maps, a hierarchy of several numerosity maps throughout human association cortices underlies this numerosity network. To investigate this hypothesis, we adapted our approach to reconstruct numerosity maps throughout the brain.We displayed visual stimuli of changing numerosity while collecting ultra-high-field (7T) fMRI data covering the occipital, parietal, posterior-superior frontal and temporal lobes. We distinguished between responses to numerosity and co-varying stimulus features using several stimulus configurations 2,16 . We summarized the fMRI...

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“…However, the response to ipsilateral stimulation is often found to be weaker due to large amount of feedforward input stemming from lowerlevel visual neurons that only respond to stimulation in the contralateral field (Ffytche, Howseman, Edwards, Sandeman, & Zeki, 2000;Huk, Dougherty, & Heeger, 2002). One example of the functional consequences of cortical separation is the fact that adaptation to numerosity -believed to originate in parietal areas of the brain (Harvey, Klein, Petridou, & Dumoulin, 2013) -has been shown to transfer across visual space, but not visual hemifield (Burr & Ross, 2008;Choo & Franconeri, 2010). While parietal areas have relatively large receptive fields -as well as areas that do not show any form of retinotopic mapping -crossing into the opposite hemifield reduces the magnitude of the numerosity after-effect.…”

Section: Methodsmentioning

confidence: 99%

An investigation of the spatial selectivity of the duration after-effect

et al. 2017

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a b s t r a c tAdaptation to the duration of a visual stimulus causes the perceived duration of a subsequently presented stimulus with a slightly different duration to be skewed away from the adapted duration. This pattern of repulsion following adaptation is similar to that observed for other visual properties, such as orientation, and is considered evidence for the involvement of duration-selective mechanisms in duration encoding. Here, we investigated whether the encoding of duration -by duration-selective mechanisms -occurs early on in the visual processing hierarchy. To this end, we investigated the spatial specificity of the duration after-effect in two experiments. We measured the duration after-effect at adapter-test distances ranging between 0 and 15°of visual angle and for within-and between-hemifield presentations. We replicated the duration after-effect: the test stimulus was perceived to have a longer duration following adaptation to a shorter duration, and a shorter duration following adaptation to a longer duration. Importantly, this duration after-effect occurred at all measured distances, with no evidence for a decrease in the magnitude of the after-effect at larger distances or across hemifields. This shows that adaptation to duration does not result from adaptation occurring early on in the visual processing hierarchy. Instead, it seems likely that duration information is a high-level stimulus property that is encoded later on in the visual processing hierarchy.

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Topographic Representation of Numerosity in the Human Parietal Cortex

Cited by 446 publications

References 65 publications

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

Mapping human temporal and parietal neuronal population activity and functional coupling during mathematical cognition

A network of topographic numerosity maps in human association cortex

An investigation of the spatial selectivity of the duration after-effect

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