A basal ganglia pathway drives selective auditory responses in songbird dopaminergic neurons via disinhibition.

A basal ganglia pathway drives selective auditory responses in songbird dopaminergic neurons via disinhibition.
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DOI:
10.1523/jneurosci.3585-09.2010
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发表时间:
2010-01-20
期刊:
The Journal of neuroscience : the official journal of the Society for Neuroscience
影响因子:
--
通讯作者:
Perkel DJ
Perkel DJ
中科院分区:
其他
文献类型:
--
作者:
Gale SD;Perkel DJ

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哺乳动物的多巴胺能神经元对奖励和奖励预测线索作出反应,并被认为在导致奖励的学习行为或感觉线索中发挥重要作用。驱动或调节这种反应的输入的解剖学来源尚不清楚;这些最终确定了多巴胺能神经元参与的行为范围。主要奖励并不是所有目标导向行为的直接目标。例如,语音学习的一个目标是模仿语音交流信号。在这里,我们证明了鸣鸟多巴胺能神经元的激活是由发声学习所需的基底神经节区域驱动的,X区。在麻醉的斑胸草雀中,多巴胺能神经元对鸟类自己的歌声(BOS)的反应比对其他声音的反应更强烈,而X区对这些反应至关重要。在没有听觉刺激的情况下,对X区输出的直接药理调节足以双向调节多巴胺能神经元的放电速率。唯一已知的从歌曲控制区到多巴胺能神经元的途径涉及从X区到腹侧苍白球(VP)的投射,后者又投射到多巴胺能区域。我们发现,VP神经元自发活跃,并优先被BOS抑制,这表明X区通过抑制VP来抑制多巴胺能神经元。支持这一模型的是,听觉反应潜伏期在X区比VP区短,在VP区比多巴胺能神经元短。因此,多巴胺能神经元可以通过基底神经节输入的复杂感觉刺激选择性地解除抑制。我们确定的功能途径可能允许多巴胺能神经元参与声乐学习。
Dopaminergic neurons in mammals respond to rewards and reward-predicting cues, and are thought to play an important role in learning actions or sensory cues that lead to reward. The anatomical sources of input that drive or modulate such responses are not well understood; these ultimately define the range of behavior to which dopaminergic neurons contribute. Primary rewards are not the immediate objective of all goal-directed behavior. For example, a goal of vocal learning is to imitate vocal-communication signals. Here, we demonstrate activation of dopaminergic neurons in songbirds driven by a basal ganglia region required for vocal learning, Area X. Dopaminergic neurons in anesthetized zebra finches respond more strongly to bird's own song (BOS) than to other sounds, and Area X is critical for these responses. Direct pharmacological modulation of Area X output, in the absence of auditory stimulation, is sufficient to bidirectionally modulate the firing rate of dopaminergic neurons. The only known pathway from song-control regions to dopaminergic neurons involves a projection from Area X to the ventral pallidum (VP), which in turn projects to dopaminergic regions. We show that VP neurons are spontaneously active and inhibited preferentially by BOS, suggesting that Area X disinihbits dopaminergic neurons by inhibiting VP. Supporting this model, auditory-response latencies are shorter in Area X than VP, and shorter in VP than dopaminergic neurons. Thus, dopaminergic neurons can be disinhibited selectively by complex sensory stimuli via input from the basal ganglia. The functional pathway we identify may allow dopaminergic neurons to contribute to vocal learning.