Luo Minmin, Perkel David J
Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104, USA.
J Neurophysiol. 2002 Oct;88(4):1903-14. doi: 10.1152/jn.2002.88.4.1903.
The anterior forebrain pathway (AFP) of the avian song system is a circuit essential for song learning but not for song production. This pathway consists of a loop serially connecting area X in the basal ganglia, the medial portion of the dorsolateral nucleus of thalamus (DLM), and the pallial lateral magnocellular nucleus of the anterior neostriatum (lMAN). The majority of DLM neurons in adult male zebra finches closely resemble mammalian thalamocortical neurons in both their intrinsic properties and the strong GABAergic inhibitory input they receive from the basal ganglia. These observations support the hypothesis that the AFP and the mammalian basal ganglia-thalamocortical pathway use similar information-processing mechanisms during sensorimotor learning. Our goal was to determine whether the cellular properties of DLM neurons are already established in juvenile birds in the sensorimotor phase of song learning when the AFP is essential. Current- and voltage-clamp recording in DLM of juvenile male zebra finches showed that juvenile DLM has two distinct cell types with intrinsic properties largely similar to those of their respective adult counterparts. Immunostaining for glutamic acid decarboxylase (GAD) in juvenile zebra finches revealed that, as in adults, most area X somata are large and strongly GAD+ and that their terminals in DLM form dense GAD+ baskets around somata. GAD immunoreactivity in DLM was depleted by lesions of area X, indicating that a strong GABAergic projection from area X to DLM is already established in juveniles. Some of the DLM neurons exhibited large, spontaneous GABAergic synaptic events. Stimulation of the afferent pathway evoked an inhibitory postsynaptic potential or current that was blocked by the GABA(A) receptor antagonist bicuculline methiodide. The decay of the GABA(A) receptor-mediated currents was slower in juvenile neurons than in adults. In addition, the reversal potential for these currents in juveniles was significantly more depolarized both than that in adults and than the Cl(-) equilibrium potential; yet the reversal potential was still well below the firing threshold and thus inhibitory in the slice preparation. Our findings suggest that the signal-processing role of DLM during sensorimotor learning is generally similar to that in adulthood but that quantitative changes in synaptic transmission accompany the development of stereotyped song.
鸟类鸣唱系统的前脑通路（AFP）是一条对鸣唱学习至关重要但对鸣唱产生并非必需的神经回路。该通路由一个环路组成，该环路依次连接基底神经节中的X区、丘脑背外侧核的内侧部分（DLM）以及新纹状体前部的皮质外侧大细胞核（lMAN）。成年雄性斑胸草雀中，大多数DLM神经元在其内在特性以及它们从基底神经节接收的强大GABA能抑制性输入方面，都与哺乳动物的丘脑皮质神经元非常相似。这些观察结果支持了这样一种假说，即AFP和哺乳动物的基底神经节 - 丘脑皮质通路在感觉运动学习过程中使用相似的信息处理机制。我们的目标是确定在鸣唱学习的感觉运动阶段，当AFP至关重要时，幼鸟DLM神经元的细胞特性是否已经确立。对幼年雄性斑胸草雀的DLM进行电流钳和电压钳记录显示，幼年DLM有两种不同的细胞类型，其内在特性与各自成年对应细胞的内在特性基本相似。对幼年斑胸草雀进行谷氨酸脱羧酶（GAD）免疫染色显示，与成年鸟一样，大多数X区的胞体较大且GAD强阳性，并且它们在DLM中的终末在胞体周围形成密集的GAD阳性篮状结构。X区损伤会使DLM中的GAD免疫反应性降低，这表明幼年时就已经建立了从X区到DLM的强大GABA能投射。一些DLM神经元表现出大的、自发的GABA能突触事件。刺激传入通路会诱发抑制性突触后电位或电流，该电位或电流会被GABA(A)受体拮抗剂甲基荷包牡丹碱阻断。GABA(A)受体介导的电流在幼年神经元中的衰减比成年神经元中慢。此外，幼年时这些电流的反转电位比成年时以及比Cl(-)平衡电位都显著更去极化；然而，反转电位仍远低于放电阈值，因此在脑片制备中仍具有抑制作用。我们的研究结果表明，在感觉运动学习过程中，DLM的信号处理作用通常与成年时相似，但突触传递的定量变化伴随着定型鸣唱的发展。
