Differential Impact of Behavioral Relevance on Quantity Coding in Primate Frontal and Parietal Neurons

Viswanathan, Pooja; Nieder, Andreas

doi:10.1016/j.cub.2015.03.025

Cited by 62 publications

(61 citation statements)

References 47 publications

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“…Second, neuronal discharges of selective neurons proved to be relevant for the crows' correct performance; if the neurons did not properly encode their preferred numerosity, the crow was prone to make mistakes. Similar results have been reported repeatedly for numerosity-selective neurons in monkeys (10)(11)(12)(13)(14)(15)(16)(17)(18). Third, both the neuronal and the behavioral tuning functions were best described on a logarithmic number line, arguing for a nonlinearly compressed coding of numerical information.…”

Section: Discussionsupporting

confidence: 83%

“…Our behavioral and neuronal data show an impressive correspondence of neuronal mechanisms found in the avian brain with those reported earlier in the nonhuman and human primate brain: First, NCL neurons were tuned to individual preferred numerosities characteristic of a "labeled-line code," enabling an unequivocal representation of numerosity by a neuronal population. Complementary findings have been made in the monkey prefrontal and posterior parietal cortex; both in the highly trained (10)(11)(12)(13)(14)(15)(16)(17)(18) and in the numerically naïve monkey (30), numerosity is encoded by a labeled-line code. Second, neuronal discharges of selective neurons proved to be relevant for the crows' correct performance; if the neurons did not properly encode their preferred numerosity, the crow was prone to make mistakes.…”

Section: Discussionmentioning

confidence: 67%

“…The neuronal correlates of numerosity representations have only been explored in humans (7)(8)(9) and primates (10)(11)(12)(13)(14)(15)(16)(17)(18), and they have been found to reside in the prefrontal and posterior parietal neocortices. In contrast to primates, birds lack a six-layered neocortex.…”

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confidence: 99%

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Neurons selective to the number of visual items in the corvid songbird endbrain

Ditz

Nieder

2015

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

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It is unknown whether anatomical specializations in the endbrains of different vertebrates determine the neuronal code to represent numerical quantity. Therefore, we recorded single-neuron activity from the endbrain of crows trained to judge the number of items in displays. Many neurons were tuned for numerosities irrespective of the physical appearance of the items, and their activity correlated with performance outcome. Comparison of both behavioral and neuronal representations of numerosity revealed that the data are best described by a logarithmically compressed scaling of numerical information, as postulated by the WeberFechner law. The behavioral and neuronal numerosity representations in the crow reflect surprisingly well those found in the primate association cortex. This finding suggests that distantly related vertebrates with independently developed endbrains adopted similar neuronal solutions to process quantity.single-cell recordings | crow | nidopallium caudolaterale | quantity B irds show elaborate quantification skills (1-3) that are of adaptive value in naturalistic situations like nest parasitism (4), food caching (5), or communication (6). The neuronal correlates of numerosity representations have only been explored in humans (7-9) and primates (10-18), and they have been found to reside in the prefrontal and posterior parietal neocortices. In contrast to primates, birds lack a six-layered neocortex. The birds' lineage diverged from mammals 300 Mya (19), at a time when the neocortex had not yet developed from the pallium of the endbrain. Instead, birds developed different pallial parts as dominant endbrain structures (20, 21) based on convergent evolution, with the nidopallium caudolaterale (NCL) as a highlevel association area (22-26). Where and how numerosity is encoded in vertebrates lacking a neocortex is unknown. Here, we show that neurons in the telencephalic NCL of corvid songbirds respond to numerosity and show a specific code for numerical information. ResultsCrows were trained in a delayed matching-to-sample task to match the number of (one to five) dots presented on touch-sensitive computer displays ( Fig. 1 A and B). Crows watched two displays (first sample, then test) separated by a 1-s delay. They were trained to peck at the displays on the screen if the test displays contained the same number of items as the sample. We varied the exact physical appearance of the displays by randomly placing dots in arbitrary locations, and by randomly choosing dot size.The crows performed the task proficiently (73.8 ± 0.4% and 77.5 ± 0.5% correct over all recording sessions for crow A and crow J, respectively; Fig. 1C). Average performance of both crows was significantly better than chance (50%) for all sample numerosities relative to the numerically most distant nonmatches (Binomial test, P < 0.01). Better performance for sample numerosities at the low (one) and high (five) numerosity range (Fig. 1D) are most likely due to "endeffects," because one and five items had to be discriminated only fro...

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Section: Discussionsupporting

confidence: 83%

Section: Discussionmentioning

confidence: 67%

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Neurons selective to the number of visual items in the corvid songbird endbrain

Ditz

Nieder

2015

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

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“…For instance, why crows seem to refrain from exploiting these capacities in specific situations [19] needs further investigation. Comparative behavioural and neuronal data from monkeys indicate that the same neuronal codes and brain areas are engaged in trained and in numerically naive (untrained) animals [60]; behavioural training results in mild, but not categorically different representational enhancements in some regions of the primate brain's number network [70]. It will be interesting to know whether this neuro-ethological observation also holds for corvids.…”

Section: (B) Precision and Speed Of Numerosity Discriminationsmentioning

confidence: 95%

Numerosity representations in crows obey the Weber–Fechner law

Ditz¹,

Nieder²

2016

Proc. R. Soc. B.

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105

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The ability to estimate number is widespread throughout the animal kingdom. Based on the relative close phylogenetic relationship (and thus equivalent brain structures), non-verbal numerical representations in human and nonhuman primates show almost identical behavioural signatures that obey the Weber-Fechner law. However, whether numerosity discriminations of vertebrates with a very different endbrain organization show the same behavioural signatures remains unknown. Therefore, we tested the numerical discrimination performance of two carrion crows (Corvus corone) to a broad range of numerosities from 1 to 30 in a delayed match-to-sample task similar to the one used previously with primates. The crows' discrimination was based on an analogue number system and showed the Weber-fraction signature (i.e. the 'just noticeable difference' between numerosity pairs increased in proportion to the numerical magnitudes). The detailed analysis of the performance indicates that numerosity representations in crows are scaled on a logarithmically compressed 'number line'. Because the same psychophysical characteristics are found in primates, these findings suggest fundamentally similar number representations between primates and birds. This study helps to resolve a classical debate in psychophysics: the mental number line seems to be logarithmic rather than linear, and not just in primates, but across vertebrates.

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“…Successive integration, if any, may therefore sharpen frontal numerosity representations. These are more closely linked to behavioural performance 40,41 , so finer tuning widths here may improve behavioural performance. Alternatively, multiple numerosity maps may instead aid interactions with multiple perceptual and cognitive systems without successive integrations Sensory and motor topographic maps are typically grouped in specific regions, allowing interactions over minimal distances.…”

Section: Lettersmentioning

confidence: 98%

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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Differential Impact of Behavioral Relevance on Quantity Coding in Primate Frontal and Parietal Neurons

Cited by 62 publications

References 47 publications

Neurons selective to the number of visual items in the corvid songbird endbrain

Neurons selective to the number of visual items in the corvid songbird endbrain

Numerosity representations in crows obey the Weber–Fechner law

A network of topographic numerosity maps in human association cortex

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