Different origins for similar brain circuits

doi:10.1126/science.abf9551

GSTDTAP > 气候变化

DOI	10.1126/science.abf9551
	Different origins for similar brain circuits
	Maria Antonietta Tosches
	2021-02-12
发表期刊	Science
出版年	2021
英文摘要	More than 320 million years ago, a reptile-like amniote ancestor abandoned aquatic habitats and fully adapted to life on land. This transition was arguably the most impactful event in vertebrate history and catalyzed evolutionary innovations. Soon after, sauropsids (birds and reptiles) diverged from the ancestors of mammals. Racing to survive in their new environments, birds and mammals evolved cognitive abilities unmatched by other vertebrates, such as vocal learning in songbirds and spoken language in humans. The evolution of the brain areas supporting these behaviors has been a dilemma for neuroscientists. On page 695 of this issue, Colquitt et al. ([ 1 ][1]) disentangle molecular similarities and differences between the song nuclei of birds and the cerebral cortex of mammals and propose that these brain areas have distinct evolutionary origins. Vocal learning circuits are part of the pallium, the roof of the most anterior vesicle of the developing neural tube. In mammals, pallial neurons are generally arranged into layers; the neocortex, in the dorsal part of the pallium, has six layers. In birds, there is no layering: The pallium is a collection of nuclei, including a set of large nuclei protruding from the ventrolateral wall of the pallium, called the dorsal ventricular ridge (DVR). Reptiles, such as turtles and lizards, also have a DVR. In the brains of other vertebrates, the pallium is simpler and there is nothing clearly comparable to the neocortex or the DVR. Thus, when the ancestors of mammals and sauropsids parted ways, they each evolved their own brain specializations—the neocortex and DVR—from expansions of the dorsal and the ventral pallium, respectively. ![Figure][2] Vocal processing circuits in birds and mammals In birds, neural circuits in the dorsal ventricular ridge (DVR, simplified schematic) resemble circuits in the mammalian neocortex. However, songbird DVR circuits are genetically related to the mammalian ventral pallium and not to the neocortex (dorsal pallium), as indicated by transcription factor expression. Moreover, in songbirds, these circuits include γ-aminobutyric acid (GABA)–ergic interneurons from the lateral ganglionic eminence (LGE), which, in mammals, are restricted to parts of the ventral pallium. RA, robust nucleus of the arcopallium GRAPHIC: KELLIE HOLOSKI/ SCIENCE Despite their anatomical differences, the bird DVR and the mammalian neocortex harbor neural circuits with similar organization and function. The DVR and neocortex both have specialized visual, auditory, and somatosensory areas and are involved in high cognitive functions, such as vocal learning, planning, and abstraction. Notably, processing of sensory inputs in the avian DVR follows some of the same characteristic rules that define the “canonical” cortical microcircuit in mammals ([ 2 ][3]). These circuits have three major components: input neurons that receive sensory information relayed by the thalamus, intratelencephalic neurons that process this information locally, and output neurons that project to motor control centers ([ 3 ][4], [ 4 ][5]) (see the figure). Given these functional similarities, several neuroscientists refer to the DVR as the “bird's cortex,” even though its neurons are not arranged in layers. Yet, functional similarities are not sufficient to answer a key question: Do DVR and neocortical circuits trace back to the same neurons in the ancestor of birds, reptiles, and mammals? The equivalent circuit hypothesis claims so and proposes that DVR nuclei are homologous to layers of the mammalian neocortex ([ 3 ][4], [ 4 ][5]). But this hypothesis is at odds with the observation that the DVR develops from the ventral pallium and the neocortex develops from the dorsal pallium. These are two distinct parts of the pallium that exist in all vertebrates ([ 5 ][6]). To understand the evolutionary relationships of DVR and neocortical neuron types, Colquitt et al. collected single-cell transcriptomics data from two DVR nuclei that form part of the song circuits—HVC (proper name) and RA (robust nucleus of the arcopallium)—in zebra finches and Bengalese finches. Comparison with transcriptomes from the pallia of the red-eared slider turtle ([ 6 ][7]) and mouse ([ 7 ][8]) revealed that DVR nuclei and neocortical layers express similar genes related to neuronal function, as expected from the equivalent circuit hypothesis. However, the expression of these genes is regulated by different sets of transcription factors. DVR neurons express transcription factors enriched in the mouse ventral pallium but not in the neocortex [as also reported in reptiles ([ 6 ][7])]. Transcription factors specify and maintain cellular identities, and cells that express the same transcription factors have the same core genetic identity and are typically considered homologous ([ 4 ][5], [ 8 ][9]). For this reason, the results from Colquitt et al. strengthen the idea that the DVR and neocortex trace back to separate regions of the ancestral pallium ([ 5 ][6], [ 6 ][7]). This suggests that complex behaviors, such as vocal learning, require neuronal operations that can be implemented only if neurons are wired up in a certain way, explaining why similar circuits evolved independently in birds and mammals. In an unexpected twist, Colquitt et al. discover another key difference between the DVR and neocortex. By examining γ-aminobutyric acid (GABA)–ergic interneurons (inhibitory neurons that project locally), they find that the entire songbird pallium is populated by a type of interneuron that is largely absent in the neocortex. These interneurons, born in the lateral ganglionic eminence (LGE), migrate to ventral pallium areas in mammals, such as the amygdala and olfactory bulb. This implies that the cortex-like microcircuits described in the avian DVR may engage an entire class of interneurons that has no counterpart in the mammalian neocortex. The study by Colquitt et al. is a teaser for what is to come. Single-cell genomics, one of the most powerful tools to understand neuronal diversity, is revolutionizing the study of brain evolution. But in single-cell comparative studies, the power and accuracy of bioinformatic analyses depend on the breadth and depth of the data. Colquitt et al. sampled a small portion of the DVR in two closely related species of finches. On the mammalian side, ventral pallium single-cell data are scarce. More data—ideally whole-pallium cell-type transcriptomes from multiple species, including amphibians and fish—are needed to clarify in detail the relationships of ventral pallium cell types in vertebrates. An evolutionary view of the DVR that acknowledges its ventral pallium nature forces reexamination of the functional analogies with the neocortex. The independent expansions of the DVR and neocortex endowed birds and mammals with the capacity to process and integrate sensory inputs in complex ways, but perhaps for different uses. Unlike the neocortex in mammals, the DVR in birds is poorly connected with entorhinal-hippocampal circuits; instead, one of its main projection targets is the hypothalamus, resembling parts of the mammalian amygdala in the ventral pallium ([ 9 ][10]). Did early mammals benefit from an enhanced representation of space to tackle complex navigation tasks? Did the bird brain specialize in computing stimulus valence? 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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/314074
专题	气候变化资源环境科学
推荐引用方式 GB/T 7714	Maria Antonietta Tosches. Different origins for similar brain circuits[J]. Science,2021.
APA	Maria Antonietta Tosches.(2021).Different origins for similar brain circuits.Science.
MLA	Maria Antonietta Tosches."Different origins for similar brain circuits".Science (2021).