Abstract rule neurons in the endbrain support intelligent behaviour in corvid songbirds

Veit, Lena; Nieder, Andreas

doi:10.1038/ncomms3878

Cited by 134 publications

(130 citation statements)

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“…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). Both crows used in this study are still alive and are participating in related experiments.…”

Section: Methodsmentioning

confidence: 94%

“…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.…”

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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: Methodsmentioning

confidence: 94%

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.

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155

187

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“…Birds can also be trained in the laboratory to distinguish stimuli based on the number of items [8,22,23]. Corvid songbirds are renowned for their flexible behaviour [24], making them ideal model organisms for the study of cognition [25,26] and high-level brain functions [27][28][29][30]. Ever since Koehler and his co-workers explored the numerical capabilities of birds [31], corvids have been known to show some level of quantity discrimination [32], and they use quantity rules to direct behaviour [33].…”

Section: Introductionmentioning

confidence: 99%

Numerosity representations in crows obey the Weber–Fechner law

Ditz¹,

Nieder²

2016

Proc. R. Soc. B.

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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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“…We have recently demonstrated that single NCL neurons encode abstract behavioral rules, irrespective of the arbitrary, learned cues used to instruct the rule (4). Furthermore, pigeons with lesions of the NCL show deficits in a reversal learning task, indicating that the NCL is a crucial structure to flexibly adapt behavior based on feedback during learning (5).…”

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confidence: 99%

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

Veit

Pidpruzhnykova

Nieder

2015

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

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The ability to form associations between behaviorally relevant sensory stimuli is fundamental for goal-directed behaviors. We investigated neuronal activity in the telencephalic area nidopallium caudolaterale (NCL) while two crows (Corvus corone) performed a delayed association task. Whereas some paired associates were familiar to the crows, novel associations had to be learned and mapped to the same target stimuli within a single session. We found neurons that prospectively encoded the chosen test item during the delay for both familiar and newly learned associations. These neurons increased their selectivity during learning in parallel with the crows' increased behavioral performance. Thus, sustained activity in the NCL actively processes information for the upcoming behavioral choice. These data provide new insights into memory representations of behaviorally meaningful stimuli in birds, and how such representations are formed during learning. The findings suggest that the NCL plays a role in learning arbitrary associations, a cornerstone of corvids' remarkable behavioral flexibility and adaptability.association learning | crow | single-cell recordings | nidopallium caudolaterale | memory T he ability to form arbitrary associations between sensory stimuli is fundamental for many flexible goal-directed behaviors. Corvids exploit learned associations intensively when adapting their behavior to a changing environment (1, 2). For example, scrub jays learn to associate different foods with different degradation speeds as a component of their episodic-like memory during food-caching behavior (3). The neuronal basis of corvids' ability to learn arbitrary associations has never been investigated.The avian cognitive integration area nidopallium caudolaterale (NCL) is a good candidate to investigate learning-related changes in the representation of initially unknown stimuli, as they acquire behavioral meaning during association learning. We have recently demonstrated that single NCL neurons encode abstract behavioral rules, irrespective of the arbitrary, learned cues used to instruct the rule (4). Furthermore, pigeons with lesions of the NCL show deficits in a reversal learning task, indicating that the NCL is a crucial structure to flexibly adapt behavior based on feedback during learning (5). The NCL is the main pallial target of dopaminergic projections from the midbrain (6), and dopamine signaling in striatal and cortical structures is involved in learning and memory processes in birds, as in mammals (7).Here we investigate changes in the neuronal representation while associative learning links arbitrary visual items in memory. We trained two carrion crows on a delayed paired-association learning (DPA) task and recorded NCL neurons during the course of learning. The task design allowed us to compare neuronal responses during the mapping of highly familiar images onto test items, as well as to follow the emergence of associative signals in the same neurons while the crows learned to map novel sample images onto the ...

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Abstract rule neurons in the endbrain support intelligent behaviour in corvid songbirds

Cited by 134 publications

References 54 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

Associative learning rapidly establishes neuronal representations of upcoming behavioral choices in crows

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