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

Abstract

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...

Numerosity representations in crows obey the Weber–Fechner law

“…In addition, our findings indicate that the logarithmic scale (according to the Weber-Fechner law) described the data even better than power function scales ( postulated by Stevens's law) because the goodness-of-fit values of the crows' performance functions were the highest for the logarithmic scaling. These findings for large numerosities are fully consistent with a previous report on small numerosities in crows [44]. More importantly, the corvid data are in agreement with findings in rhesus monkeys for small [47] and large [46] numerosities, and also for non-verbal discriminations in adult humans [46] and an Amazonian indigenous group with reduced numerical lexicon [49].…”

“…The increased Weber fractions in the current report are most likely to result from much larger numerical distances of the non-match numerosities relative to the sample numerosity (i.e. the crows were not forced to discriminate as precisely as in the previous study [44] in which minimal numerical distances of one between all numerosities were applied). This indicates that the choice of the numerosities the animals have to compare has an impact on precision, and the Weber fractions we obtained for numerosities 1-5 are the more reliable and more comparable values.…”

“…Even more controls have been applied in a previous study [44], none of which distracted the crows from numerosity. Our data suggest that crows do not use number as a 'last resort' to discriminate quantity, as has been suggested several times (e.g.…”

“…Whether the mental number line for non-symbolic number is linear or rather logarithmically compressed is a classic debate in human psychophysics, but a comparative approach in different animal taxa is needed to arrive at cross-species, potentially evolutionary stable schemes of numerical representations. Suggestive evidence with small numbers indicated nonlinear compression of number representations in crows [44]. However, because discrimination for small numerosities is quite precise and only covers a very limited number range, absolute cardinality judgements to a broad range of numerosities addressing the ANS needs to be tested.…”

Konstruktywizm Jeana Piageta i koncepcja zmysłu liczby a edukacja matematyczna

“…Wyspecjalizowane neurony liczbowe wykryto także u krukowatych (Ditz i Nieder, 2015). Poszczególne neurony przejawiają szczytową aktywność jedynie w odpowiedzi na określoną wartość.…”