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The receptor architecture of the pigeons’ nidopallium caudolaterale: an avian analogue to the mammalian prefrontal cortex

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Abstract

The avian nidopallium caudolaterale is a multimodal area in the caudal telencephalon that is apparently not homologous to the mammalian prefrontal cortex but serves comparable functions. Here we analyzed binding-site densities of glutamatergic AMPA, NMDA and kainate receptors, GABAergic GABAA, muscarinic M1, M2 and nicotinic (nACh) receptors, noradrenergic α1 and α2, serotonergic 5-HT1A and dopaminergic D1-like receptors using quantitative in vitro receptor autoradiography. We compared the receptor architecture of the pigeons’ nidopallial structures, in particular the NCL, with cortical areas Fr2 and Cg1 in rats and prefrontal area BA10 in humans. Our results confirmed that the relative ratios of multiple receptor densities across different nidopallial structures (their “receptor fingerprints”) were very similar in shape; however, the absolute binding densities (the “size” of the fingerprints) differed significantly. This finding enables a delineation of the avian NCL from surrounding structures and a further parcellation into a medial and a lateral part as revealed by differences in densities of nACh, M2, kainate, and 5-HT1A receptors. Comparisons of the NCL with the rat and human frontal structures showed differences in the receptor distribution, particularly of the glutamate receptors, but also revealed highly conserved features like the identical densities of GABAA, M2, nACh and D1-like receptors. Assuming a convergent evolution of avian and mammalian prefrontal areas, our results support the hypothesis that specific neurochemical traits provide the molecular background for higher order processes such as executive functions. The differences in glutamate receptor distributions may reflect species-specific adaptations.

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Abbreviations

ACh:

Acetylcholine

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxalone propionic acid

Cg1:

Cingulate cortex 1

CDL:

Dorsolateral corticoid area

EPSCs:

Excitatory postsynaptic currents

FR2:

Frontal area 2

GABA:

γ-Aminobutyric acid

GLI:

Gray level index

gluR1:

Glutamate receptor subunit 1

HA:

Hyperpallium apicale

HVC:

Higher vocal center

IMM:

Intermediate and medial mesopallium ventrale

MNH:

Mediorostral nidopallium/hyperpallium

nACh:

Nicotinic acetylcholine

NCC:

Nidopallium caudocentrale

NCL:

Nidopallium caudolaterale

NCLl:

Nidopallium caudolaterale pars lateralis

NCLm:

Nidopallium caudolaterale pars medialis

NCM:

Nidopallium caudomediale

NFT:

Nidopallium fronto-trigeminale

NIM:

Nidopallium intermedium medialis

NMDA:

N-methyl-d-aspartate

PFC:

Prefrontal cortex

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Acknowledgments

Supported by a grant from the BMBF through the Bernstein Focus Group “Varying Tunes” to O.G.

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Herold, C., Palomero-Gallagher, N., Hellmann, B. et al. The receptor architecture of the pigeons’ nidopallium caudolaterale: an avian analogue to the mammalian prefrontal cortex. Brain Struct Funct 216, 239–254 (2011). https://doi.org/10.1007/s00429-011-0301-5

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