Cellular transcriptomics reveals evolutionary identities of songbird vocal circuits

doi:10.1126/science.abd9704

GSTDTAP > 气候变化

DOI	10.1126/science.abd9704
	Cellular transcriptomics reveals evolutionary identities of songbird vocal circuits
	Bradley M. Colquitt; Devin P. Merullo; Genevieve Konopka; Todd F. Roberts; Michael S. Brainard
	2021-02-12
发表期刊	Science
出版年	2021
英文摘要	Birds have complex motor and cognitive abilities that rival or exceed the performance of many mammals, but their brains are organized in a notably different way. Parts of the bird brain have been functionally compared to the mammalian neocortex. However, it is still controversial to what extent these regions are truly homologous with the neocortex or if instead they are examples of evolutionary convergence. Colquitt et al. used single-cell sequencing to identify and characterize the major classes of neurons that comprise the song-control system in birds (see the Perspective by Tosches). They found multiple previously unknown neural classes in the bird telencephalon and shed new light on the long-standing controversy regarding the nature of homology between avian and mammalian brains. Science , this issue p. [eabd9704][1]; see also p. [676][2] ### INTRODUCTION The mammalian neocortex, with its distinctive six-layered structure, is thought to enable advanced cognitive functions not seen in other animals. Yet birds, which have a remarkably different brain organization, display a range of complex motor and cognitive abilities, such as tool use and problem-solving, that are comparable to those of many mammals. Although portions of the avian brain are often compared to the neocortex, especially regions involved in the learning and production of vocalizations, it has remained unclear whether these regions are truly homologous with the neocortex (that is, whether they share a common evolutionary origin) or instead are examples of evolutionary convergence. ### RATIONALE The nature of the similarities and differences in brain organization between mammals and birds has implications for the evolutionary mechanisms that underlie the emergence of advanced behaviors. In mammals, the six-layered neocortex occupies most of the pallium (the outermost portion of the brain), whereas in birds, most of the pallium consists of a distinct unlayered structure called the dorsal ventricular ridge (DVR). The DVR contains multiple interconnected groups of neurons, often referred to as nuclei, that are necessary for complex avian behaviors, including vocal learning in songbirds. Two prevailing viewpoints offer opposing interpretations for how both the mammalian neocortex and avian DVR enable complex behaviors despite their structural differences. One view proposes that the DVR is homologous to the neocortex and that the nuclei in the DVR correspond to distinct layers of the neocortex and thus represent a rearrangement of a conserved ancestral circuit. A second hypothesis argues that the neocortex and DVR develop from distinct embryonic regions of the pallium (dorsal and ventral, respectively) and are therefore nonhomologous structures that separately evolved to serve similar functions. To test these models, we used single-cell transcriptomics to characterize the cell types and gene expression patterns of two regions in the songbird DVR that are necessary for learning and producing birdsong: HVC (proper name) and RA (robust nucleus of the arcopallium). For each type, we characterized the expression profiles of transcription factors, which reflect the cellular identities and regional origins of neurons, and effector genes, which specify neuronal cell properties and function. We compared these profiles with those of neurons previously described in mammals and reptiles to clarify how individual neuronal types are related across amniotes. ### RESULTS We identify a variety of excitatory cell classes that are different between HVC and RA, and inhibitory classes that are shared across regions, similar to organizational patterns of cell types in mammals and reptiles. We show that excitatory neurons in both HVC and RA have transcription factor profiles that bear strong similarity to the mammalian ventral pallium, which includes the olfactory bulb, piriform cortex, and pallial amygdala, but not to the neocortex, which develops from the dorsal pallium. However, when examining only effector genes, we find that excitatory neurons exhibit greater similarity to neocortical neurons from multiple layers and less similarity to the ventral pallium. We also find that songbird inhibitory neurons bear a considerable resemblance to neuron classes in both mammals and turtles, indicating that the major classes of inhibitory neurons are conserved and likely present in ancestral amniotes. We report that, consistent with the interpretation that song-control regions have ventral pallial origins, the most abundant inhibitory neuron type in the songbird DVR is similar to inhibitory neurons that are enriched in mammalian ventral pallial derivatives and absent from the neocortex. ### CONCLUSION Our findings indicate that the avian DVR and the neocortex derive from different neurodevelopmental regions employing distinct transcription factor expression patterns and therefore are not homologous structures. However, we find that excitatory neurons in the DVR have evolved similar properties to the neocortex by engaging overlapping patterns of effector genes. Such overlapping transcriptional profiles may account for the evolution of similar complex motor and cognitive abilities in mammals and birds, including vocal learning, and suggest that the DVR may perform neural computations in a way that is functionally analogous to the neocortex. By addressing a long-standing controversy regarding the relationship between avian and mammalian brains, these results provide insight into the evolution and diversification of neural cell types and structures that enable advanced behaviors. ![Figure][3] Cellular transcriptomics of a songbird vocal circuit. ( A ) Schematic of the song motor pathway (SMP). HVC, proper name; RA, robust nucleus of the arcopallium; DLM, medial portion of the dorsolateral thalamic nucleus; Av, mesopallial auditory nucleus Avalanche; LMAN, lateral magnocellular nucleus of the anterior nidopallium. ( B ) Transcriptional similarities between glutamatergic neurons in the SMP and the mouse neocortex. ( C ) Pallial biases of transcription factor (TF) versus effector gene (non-TF) expression profiles. DP/MP/LP/VP, dorsal/medial/lateral/ventral pallium. ( D ) Diversity and origins of γ-aminobutyric acid–releasing (GABAergic) neurons in the SMP. LGE/MGE/CGE, lateral/medial/caudal ganglionic eminence. Birds display advanced behaviors, including vocal learning and problem-solving, yet lack a layered neocortex, a structure associated with complex behavior in mammals. To determine whether these behavioral similarities result from shared or distinct neural circuits, we used single-cell RNA sequencing to characterize the neuronal repertoire of the songbird song motor pathway. Glutamatergic vocal neurons had considerable transcriptional similarity to neocortical projection neurons; however, they displayed regulatory gene expression patterns more closely related to neurons in the ventral pallium. Moreover, while γ-aminobutyric acid–releasing neurons in this pathway appeared homologous to those in mammals and other amniotes, the most abundant avian class is largely absent in the neocortex. These data suggest that songbird vocal circuits and the mammalian neocortex have distinct developmental origins yet contain transcriptionally similar neurons. [1]: /lookup/doi/10.1126/science.abd9704 [2]: /lookup/doi/10.1126/science.abf9551 [3]: pending:yes
领域	气候变化 ; 资源环境
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文献类型	期刊论文
条目标识符	http://119.78.100.173/C666/handle/2XK7JSWQ/314082
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Bradley M. Colquitt,Devin P. Merullo,Genevieve Konopka,et al. Cellular transcriptomics reveals evolutionary identities of songbird vocal circuits[J]. Science,2021.
APA	Bradley M. Colquitt,Devin P. Merullo,Genevieve Konopka,Todd F. Roberts,&Michael S. Brainard.(2021).Cellular transcriptomics reveals evolutionary identities of songbird vocal circuits.Science.
MLA	Bradley M. Colquitt,et al."Cellular transcriptomics reveals evolutionary identities of songbird vocal circuits".Science (2021).