Millisecond timescale disinhibition mediates fast information transmission through an avian basal ganglia loop.

Millisecond timescale disinhibition mediates fast information transmission through an avian basal ganglia loop.
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DOI:
10.1523/jneurosci.3060-09.2009
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发表时间:
2009-12-09
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:
Leblois A;Bodor AL;Person AL;Perkel DJ

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鸟类的歌唱学习与人类的语言习得有着惊人的相似之处,需要基底节(BG)-丘脑-皮质回路。BG中的信息处理和传输速度被认为受到两个串联抑制性连接的突触结构的限制。由于在发声过程中对肌肉的精确控制,传播速度在鸟类的BG回路中可能是至关重要的。我们使用对BG的皮质输入的电刺激,以精细的时间分辨率来研究该网络内的功能连接。我们发现,丘脑和皮质核团中与刺激区域没有直接联系的神经元可以以极短的潜伏期对刺激做出反应。通过药物操作,我们将这一特性追溯到BG,并表明皮质刺激触发了丘脑神经元的快速去抑制。令人惊讶的是,纹状体抑制神经元对BG输出神经元的前馈抑制有时先于皮质传入的单突触兴奋性驱动。快速前馈抑制使BG输出神经元的单个棘波间期仅延长几毫秒。这一短暂的延迟足以驱动目标丘脑神经元的放电概率强劲而短暂的增加,从而引起短暂的潜伏期反应。通过在体内阻断谷氨酸受体,我们表明丘脑的反应似乎不依赖于兴奋性驱动,我们在一个理论模型中表明,它们可以通过抑制后反弹特性来调节。这种通过解除抑制和反弹发出的快速信号可能是学习快速和暂时精确的运动动作(如发声交流)的关键特化。
Avian song learning shares striking similarities with human speech acquisition and requires a basal ganglia (BG)-thalamo-cortical circuit. Information processing and transmission speed in the BG is thought to be limited by synaptic architecture of two serial inhibitory connections. Propagation speed may be critical in the avian BG circuit given the temporally precise control of musculature during vocalization. We used electrical stimulation of the cortical inputs to the BG to study, with fine time resolution, the functional connectivity within this network. We found that neurons in thalamic and cortical nuclei that are not directly connected with the stimulated area can respond to the stimulation with extremely short latencies. Through pharmacological manipulations, we trace this property back to the BG, and show that the cortical stimulation triggers fast disinhibition of the thalamic neurons. Surprisingly, feedforward inhibition mediated by striatal inhibitory neurons onto BG output neurons sometimes precedes the monosynaptic excitatory drive from cortical afferents. The fast feedforward inhibition lengthens a single inter-spike interval in BG output neurons by just a few milliseconds. This short delay is sufficient to drive a strong, brief increase in firing probability in the target thalamic neurons, evoking short latency responses. By blocking glutamate receptors in vivo, we show that thalamic responses do not appear to rely on excitatory drive, and we show in a theoretical model that they could be mediated by post-inhibitory rebound properties. Such fast signalling through disinhibition and rebound may be a crucial specialization for learning of rapid and temporally precise motor acts such as vocal communication.