Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context.

Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context.
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DOI:
10.1523/jneurosci.2250-08.2008
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发表时间:
2008-12-03
期刊:
The Journal of neuroscience : the official journal of the Society for Neuroscience
影响因子:
--
通讯作者:
Doupe AJ
Doupe AJ
中科院分区:
其他
文献类型:
--
作者:
Kao MH;Wright BD;Doupe AJ

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歌唱是一种后天习得的受社会互动影响的发声行为。先前的研究表明,前前脑通路(AFP)是一种特殊的白质-基底神经节回路,对声乐可塑性至关重要,它介导了社会信号对歌曲的影响。在这里,我们通过表征AFP输出核LMAN(前乳头外侧大细胞核)单个神经元的歌唱相关活动,研究AFP向歌唱运动区发送的信号及其对社会环境的依赖性。我们发现,与雌性的相互作用会导致LMAN神经元的放电特性发生显著的实时变化。当雄性向雌性唱歌时(“定向”),LMAN神经元表现出可靠的单尖峰放电,精确地锁定在歌曲上。相比之下,当雄性单独唱歌(“无定向”)时,相同的LMAN神经元表现出突出的突发放电和每次试验的可变性。在重复的无定向试验中,爆发结构和时间变化很大。尽管放电统计数据与上下文相关,但单个神经元的歌曲锁定放电的平均模式在不同的行为背景下是相似的,这表明有一个共同的潜在信号。然而,同一只鸟的不同LMAN神经元表现出不同的放电模式,这表明神经元子集共同编码鸣叫特征。总之,我们的研究结果表明,行为相互作用可逆地改变了LMAN神经元的信号模式。这种变化可能有助于在可变状态和精确状态之间快速切换运动活动。更一般地说,我们的研究结果表明,白质-基底神经节回路通过多种机制促进运动学习和产生:模式信号可以指导运动输出的变化,而状态依赖的可变性可以支持运动探索。
Song is a learned vocal behavior influenced by social interactions. Prior work has suggested that the anterior forebrain pathway (AFP), a specialized pallial–basal ganglia circuit critical for vocal plasticity, mediates the influence of social signals on song. Here, we investigate the signals the AFP sends to song motor areas and their dependence on social context by characterizing singing-related activity of single neurons in the AFP output nucleus LMAN (lateral magnocellular nucleus of the anterior nidopallium). We show that interaction with females causes marked, real-time changes in firing properties of individual LMAN neurons. When males sing to females (`directed'), LMAN neurons exhibit reliable firing of single spikes precisely locked to song. In contrast, when males sing alone (`undirected'), the same LMAN neurons exhibit prominent burst firing and trial-by-trial variability. Burst structure and timing vary substantially across repeated undirected trials. Despite context-dependent differences in firing statistics, the average pattern of song-locked firing for an individual neuron is similar across behavioral contexts, suggesting a common underlying signal. Different LMAN neurons in the same bird, however, exhibit distinct firing patterns, suggesting that subsets of neurons jointly encode song features. Together, our findings demonstrate that behavioral interactions reversibly transform the signaling mode of LMAN neurons. Such changes may contribute to rapid switching of motor activity between variable and precise states. More generally, our results suggest that pallial–basal ganglia circuits contribute to motor learning and production through multiple mechanisms: patterned signals could guide changes in motor output while state-dependent variability could subserve motor exploration.