Neuronal Correlates of Visual Working Memory in the Corvid Endbrain

Veit, Lena; Hartmann, Konstantin; Nieder, Andreas

doi:10.1523/jneurosci.0612-14.2014

Cited by 89 publications

(79 citation statements)

References 32 publications

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“…Similar maximal accuracy levels have been reported for amphibians [6]. However, we know that crows can perform close to 100% correct [27,28,30]. Given that the tested numerical distances between match and non-match numerosities were much larger compared with previous monkey and human studies [45,46], an alternative explanation is that the crows did not exploit the full capacity of their ANS.…”

Section: (A) Analogue Number Representations In Crowssupporting

confidence: 76%

Numerosity representations in crows obey the Weber–Fechner law

Ditz¹,

Nieder²

2016

Proc. R. Soc. B.

104

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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Section: (A) Analogue Number Representations In Crowssupporting

confidence: 76%

Numerosity representations in crows obey the Weber–Fechner law

Ditz¹,

Nieder²

2016

Proc. R. Soc. B.

104

105

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“…NCL neurons carried an internal, stimulus-independent signal that was predictive of error and type of error. These results underscore the role of corvid NCL [4][5][6][7] in synthesizing external multisensory information and internal mnemonic data needed for executive control of behavior.…”

Section: Discussionmentioning

confidence: 62%

Cross-Modal Associative Mnemonic Signals in Crow Endbrain Neurons

Moll

Nieder

2015

Current Biology

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The ability to associate stimuli across time and sensory modalities endows animals and humans with many of the complex, learned behaviors. For successful performance, associations need to be retrieved from long-term memory and maintained active in working memory. We investigated how this is accomplished in the avian brain. We trained carrion crows (Corvus corone) to perform a bimodal delayed paired associate task in which the crows had to match auditory stimuli to delayed visual items. Single-unit recordings from the association area nidopallium caudolaterale (NCL) revealed sustained memory signals that selectively correlated with the learned audio-visual associations across time and modality, and sustained activity prospectively encoded the crows' choices. NCL neurons carried an internal, stimulus-independent signal that was predictive of error and type of error. These results underscore the role of corvid NCL in synthesizing external multisensory information and internal mnemonic data needed for executive control of behavior.

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“…The electrodes targeted the NCL. Tracing electrode tracks of an identically implanted crow used for a different study (25,26) confirmed that recording locations were within NCL. Cryostat sections were immunohistochemically stained for tyrosine-hydroxylase to identify dopaminergic cells, which characterize the NCL (25).…”

Section: Methodsmentioning

confidence: 68%

“…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)(23)(24)(25)(26). Where and how numerosity is encoded in vertebrates lacking a neocortex is unknown.…”

mentioning

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.

155

187

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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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Neuronal Correlates of Visual Working Memory in the Corvid Endbrain

Cited by 89 publications

References 32 publications

Numerosity representations in crows obey the Weber–Fechner law

Numerosity representations in crows obey the Weber–Fechner law

Cross-Modal Associative Mnemonic Signals in Crow Endbrain Neurons

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

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