Human-specific increase of dopaminergic innervation in a striatal region associated with speech and language: A comparative analysis of the primate basal ganglia.

Human-specific increase of dopaminergic innervation in a striatal region associated with speech and language: A comparative analysis of the primate basal ganglia.
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DOI:
10.1002/cne.23937
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发表时间:
2016-07-01
期刊:
The Journal of comparative neurology
影响因子:
--
通讯作者:
Sherwood CC
Sherwood CC
中科院分区:
其他
文献类型:
--
作者:
Raghanti MA;Edler MK;Stephenson AR;Wilson LJ;Hopkins WD;Ely JJ;Erwin JM;Jacobs B;Hof PR;Sherwood CC

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纹状体的多巴胺能神经支配与学习过程以及人类言语和语言的发育有关。一些证据表明,纹状体多巴胺能传入的进化变化可能与人类独特的认知和行为能力有关,包括FOXP 2基因的人类特异性序列与小鼠背内侧纹状体多巴胺减少的关联。为了研究这种可能性,我们量化了酪氨酸羟化酶免疫反应(TH-IR)轴突的密度作为衡量多巴胺能神经支配在5个基底神经节区域在人类,大猩猩,和新的和旧世界的猴子。我们的研究结果表明,人类不同于非人灵长类动物物种有一个显着增加多巴胺能神经支配选择性地定位于内侧尾状核。纹状体的这个区域是高度互连的,接收来自多个新皮层区域的传入,并支持行为和认知灵活性。内侧尾状核在缺乏功能性FOXP 2等位基因的人类中也表现出活动过度,并且在人源化Foxp 2小鼠中表现出改变的多巴胺浓度。此外,黑猩猩使用社会习得的引起注意的声音与那些没有使用的黑猩猩相比,纹状体多巴胺能输入没有改变。这一证据表明,人类内侧尾状核多巴胺神经支配的增加是一种与经验依赖性可塑性无关的物种典型特征。这种增加的特异性可能与纹状体该区域内皮质区的会聚程度有关,也可能与人类言语和语言有关。在灵长类动物中,人类是独一无二的,其内侧尾状核的多巴胺能神经支配增加,该区域与新皮层高度互连,并与言语和语言产生有关。这些结果表明,纹状体多巴胺在人类大脑的进化中发挥了重要作用。
The dopaminergic innervation of the striatum has been implicated in learning processes and in the development of human speech and language. Several lines of evidence suggest that evolutionary changes in dopaminergic afferents of the striatum may be associated with uniquely human cognitive and behavioral abilities, including the association of the human-specific sequence of the FOXP2 gene with decreased dopamine in the dorsomedial striatum of mice. To examine this possibility, we quantified the density of tyrosine hydroxylase-immunoreactive (TH-ir) axons as a measure of dopaminergic innervation within five basal ganglia regions in humans, great apes, and New and Old World monkeys. Our results indicate that humans differ from nonhuman primate species in having a significant increase in dopaminergic innervation selectively localized to the medial caudate nucleus. This region of the striatum is highly interconnected, receiving afferents from multiple neocortical regions, and supports behavioral and cognitive flexibility. The medial caudate nucleus also shows hyperactivity in humans lacking a functional FOXP2 allele and exhibits altered dopamine concentrations in humanized Foxp2 mice. Additionally, striatal dopaminergic input was not altered in chimpanzees that used socially learned attention-getting sounds versus those that did not. This evidence indicates that the increase in dopamine innervation of the medial caudate nucleus in humans is a species-typical characteristic not associated with experience-dependent plasticity. The specificity of this increase may be related to the degree of convergence from cortical areas within this region of the striatum and may also be involved in human speech and language. Humans are unique among primates in having increased dopaminergic innervation of the medial caudate nucleus, a region that is highly interconnected with the neocortex and that has been implicated in speech and language production. These results indicate that striatal dopamine has played an important role in the evolution of the human brain.