Gale Samuel D, Perkel David J
Graduate Program in Neurobiology and Behavior, University of Washington, Box 356515, Seattle, WA 98195, USA.
J Neurophysiol. 2006 Nov;96(5):2295-306. doi: 10.1152/jn.01040.2005. Epub 2006 Jul 26.
The neurotransmitter dopamine plays important roles in motor control, learning, and motivation in mammals and probably other animals as well. The strong dopaminergic projection to striatal regions and more moderate dopaminergic projections to other regions of the telencephalon predominantly arise from midbrain dopaminergic neurons in the substantia nigra pars compacta (SNc) and ventral tegmental area (VTA). Homologous dopaminergic cell groups in songbirds project anatomically in a manner that may allow dopamine to influence song learning or song production. The electrophysiological properties of SNc and VTA neurons have not previously been studied in birds. Here we used whole cell recordings in brain slices in combination with tyrosine-hydroxylase immunolabeling as a marker of dopaminergic neurons to determine electrophysiological and pharmacological properties of dopaminergic and nondopaminergic neurons in the zebra finch SNc and VTA. Our results show that zebra finch dopaminergic neurons possess physiological properties very similar to those of mammalian dopaminergic neurons, including broad action potentials, calcium- and apamin-sensitive membrane-potential oscillations underlying pacemaker firing, powerful spike-frequency adaptation, and autoinhibition via D2 dopamine receptors. Moreover, the zebra finch SNc and VTA also contain nondopaminergic neurons with similarities (fast-firing, inhibition by the mu-opioid receptor agonist [d-Ala(2), N-Me-Phe(4), Gly-ol(5)]-enkephalin (DAMGO)) and differences (strong h-current that contributes to spontaneous firing) compared with GABAergic neurons in the mammalian SNc and VTA. Our results provide insight into the intrinsic membrane properties that regulate the activity of dopaminergic neurons in songbirds and add to strong evidence for anatomical, physiological, and functional similarities between the dopaminergic systems of mammals and birds.
神经递质多巴胺在哺乳动物以及可能在其他动物的运动控制、学习和动机方面发挥着重要作用。向纹状体区域的强大多巴胺能投射以及向端脑其他区域的适度多巴胺能投射主要源自黑质致密部(SNc)和腹侧被盖区(VTA)的中脑多巴胺能神经元。鸣禽中同源的多巴胺能细胞群在解剖学上的投射方式可能使多巴胺影响鸣叫学习或鸣叫产生。此前尚未在鸟类中研究过SNc和VTA神经元的电生理特性。在此,我们结合使用脑片全细胞记录以及酪氨酸羟化酶免疫标记作为多巴胺能神经元的标志物,来确定斑胸草雀SNc和VTA中多巴胺能和非多巴胺能神经元的电生理和药理学特性。我们的结果表明,斑胸草雀多巴胺能神经元具有与哺乳动物多巴胺能神经元非常相似的生理特性,包括宽动作电位、起搏器发放基础上的钙和蜂毒明肽敏感的膜电位振荡、强大的峰频率适应性以及通过D2多巴胺受体的自身抑制。此外,与哺乳动物SNc和VTA中的GABA能神经元相比,斑胸草雀的SNc和VTA还含有具有相似性(快速发放、被μ-阿片受体激动剂[D-Ala(2),N-Me-Phe(4),Gly-ol(5)]-脑啡肽(DAMGO)抑制)和差异(有助于自发放电的强大h电流)的非多巴胺能神经元。我们的结果为调节鸣禽多巴胺能神经元活动的内在膜特性提供了见解,并进一步有力证明了哺乳动物和鸟类多巴胺能系统在解剖学、生理学和功能上的相似性。