Tuning to non‐symbolic proportions in the human frontoparietal cortex

Jacob, Simon N.; Nieder, Andreas

doi:10.1111/j.1460-9568.2009.06932.x

Cited by 116 publications

(126 citation statements)

References 32 publications

(52 reference statements)

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“…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. Because logarithmic coding is postulated by the psychophysical WeberFechner Law and has been established for human brain signals (8,9) and primate neurons (28), this finding suggests that abstract numerical and sensory representations share the same fundamental mechanisms and neural coding schemes both in songbirds and primates.…”

Section: Discussionmentioning

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: Discussionmentioning

confidence: 99%

“…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%

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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155

187

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“…Such "number neurons" abstractly represent the number of items across space, time, and modalities (15,16,17). Number neurons have also been traced indirectly in the human brain using functional MRI (fMRI) (18,19).However, because neurons can be trained to represent behaviorally meaningful categories (20,21,22), it has been argued (23) that the presence of previously described number neurons in trained animals might be a product of intense learning, rather than a reflection of a spontaneous number sense. For the same reason, the coding scheme for numerosity has been debated (23): Is the spontaneous neuronal code for numerosity a summation code, as evidenced by monotonic discharges as a function of quantity (14,24), or a labeled-line code as witnessed by numerosity-selective neurons tuned to preferred numerosities analogous to those found in monkeys performing numerical tasks (25,26)?…”

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Neuronal correlates of a visual “sense of number” in primate parietal and prefrontal cortices

Viswanathan

Nieder

2013

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

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"Sense of number" refers to the classical idea that we perceive the number of items (numerosity) intuitively. However, whether the brain signals numerosity spontaneously, in the absence of learning, remains unknown; therefore, we recorded from neurons in the ventral intraparietal sulcus and the dorsolateral prefrontal cortex of numerically naive monkeys. Neurons in both brain areas responded maximally to a given number of items, showing tuning to a preferred numerosity. Numerosity was encoded earlier in area ventral intraparietal area, suggesting that numerical information is conveyed from the parietal to the frontal lobe. Visual numerosity is thus spontaneously represented as a perceptual category in a dedicated parietofrontal network. This network may form the biological foundation of a spontaneous number sense, allowing primates to intuitively estimate the number of visual items.association cortices | quantity | single-unit recording T he classical idea of a "sense of number" (1,2) suggests that we and animals are endowed with the faculty to perceive the number of items (i.e., numerosity) intuitively. Numerosity might be a perceptual category provided by hard-wired sensory brain processes, without the need to learn what numerosity refers to. Supporting this hypothesis, numerosity is represented by an approximate nonverbal system that allows wild animals (3,4), prelinguistic infants(5,6), and innumerate humans (7,8) to readily estimate set size. Evidence that the brain is set up to assess visual numerosity spontaneously was recently provided by psychophysical and computational experiments: numerosity-just like color or perceptual categories like faces-in humans is susceptible to adaptation (9,10), and is extracted en passant by computational network models (11).So far, the neuronal foundations of a perceptual number sense were never tested because all experiments done so far were performed in animals that learned to discriminate numerosity (12)(13)(14). Work with behaviorally trained nonhuman primates identified a cortical network with individual neurons in the prefrontal (PFC) and posterior parietal cortex (PPC) selectively responding to the number of items. Such "number neurons" abstractly represent the number of items across space, time, and modalities (15,16,17). Number neurons have also been traced indirectly in the human brain using functional MRI (fMRI) (18,19).However, because neurons can be trained to represent behaviorally meaningful categories (20,21,22), it has been argued (23) that the presence of previously described number neurons in trained animals might be a product of intense learning, rather than a reflection of a spontaneous number sense. For the same reason, the coding scheme for numerosity has been debated (23): Is the spontaneous neuronal code for numerosity a summation code, as evidenced by monotonic discharges as a function of quantity (14,24), or a labeled-line code as witnessed by numerosity-selective neurons tuned to preferred numerosities analogous to those found in monkeys perform...

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“…Differential ERPs to 5:1 deviants could, thus, be connected to the ratio between the two numerosities of the tones (for a cortical ratio correlate for visual objects, see, [35]) or the numerosities themselves. Obviously, they could also be linked to one of the two numerosities in a sequence at a time as the change in one numerosity might have been detectable differently from the other numerosity.…”

Section: Erps In the Ignore Conditionmentioning

confidence: 99%