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Fast-Spiking Interneurons of the Premotor Cortex Contribute to Initiation and Execution of Spontaneous Actions
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2023-06-07 , DOI: 10.1523/jneurosci.0750-22.2023
Nadia Giordano 1, 2 , Claudia Alia 3 , Lorenzo Fruzzetti 1, 4, 5 , Maria Pasquini 4, 5 , Giulia Palla 1, 2 , Alberto Mazzoni 4, 5 , Silvestro Micera 4, 5, 6 , Leonardo Fogassi 7 , Luca Bonini 7 , Matteo Caleo 1, 8
Affiliation  

Planning and execution of voluntary movement depend on the contribution of distinct classes of neurons in primary motor and premotor areas. However, timing and pattern of activation of GABAergic cells during specific motor behaviors remain only partly understood. Here, we directly compared the response properties of putative pyramidal neurons (PNs) and GABAergic fast-spiking neurons (FSNs) during spontaneous licking and forelimb movements in male mice. Recordings centered on the face/mouth motor field of the anterolateral motor cortex (ALM) revealed that FSNs fire longer than PNs and earlier for licking, but not for forelimb movements. Computational analysis revealed that FSNs carry vastly more information than PNs about the onset of movement. While PNs differently modulate their discharge during distinct motor acts, most FSNs respond with a stereotyped increase in firing rate. Accordingly, the informational redundancy was greater among FSNs than PNs. Finally, optogenetic silencing of a subset of FSNs reduced spontaneous licking movement. These data suggest that a global rise of inhibition contributes to the initiation and execution of spontaneous motor actions.

SIGNIFICANCE STATEMENT Our study contributes to clarifying the causal role of fast-spiking neurons (FSNs) in driving initiation and execution of specific, spontaneous movements. Within the face/mouth motor field of mice premotor cortex, FSNs fire before pyramidal neurons (PNs) with a specific activation pattern: they reach their peak of activity earlier than PNs during the initiation of licking, but not of forelimb, movements; duration of FSNs activity is also greater and exhibits less selectivity for the movement type, as compared with that of PNs. Accordingly, FSNs appear to carry more redundant information than PNs. Optogenetic silencing of FSNs reduced spontaneous licking movement, suggesting that FSNs contribute to the initiation and execution of specific spontaneous movements, possibly by sculpting response selectivity of nearby PNs.



中文翻译:

前运动皮层的快速尖峰中间神经元有助于自发动作的启动和执行

随意运动的规划和执行取决于初级运动区和运动前区不同类别神经元的贡献。然而,GABA 能细胞在特定运动行为期间激活的时间和模式仍然只有部分了解。在这里,我们直接比较了雄性小鼠自发舔舐和前肢运动期间假定的锥体神经元 (PN) 和 GABA 能快速尖峰神经元 (FSN) 的反应特性。以前外侧运动皮层 (ALM) 的面部/嘴运动场为中心的记录显示,FSN 的放电时间比 PN 更长,并且在舔舐时放电更早,但在前肢运动时则不然。计算分析表明,FSN 比 PN 携带更多有关运动开始的信息。虽然 PN 在不同的运动动作期间以不同的方式调节其放电,大多数 FSN 的反应都是提高发射率。因此,FSN 之间的信息冗余比 PN 更大。最后,FSN 子集的光遗传学沉默减少了自发的舔舐运动。这些数据表明,抑制的整体上升有助于自发运动动作的启动和执行。

意义声明我们的研究有助于阐明快速尖峰神经元(FSN)在驱动特定自发运动的启动和执行中的因果作用。在小鼠前运动皮层的面部/嘴运动场中,FSNs 在锥体神经元 (PNs) 之前以特定的激活模式放电:在舔舐运动开始时,FSNs 比 PNs 更早达到活动峰值,但在前肢运动开始时,FSNs 则不然;与 PN 相比,FSN 活动的持续时间也更长,并且对运动类型的选择性更低。因此,FSN 似乎比 PN 携带更多冗余信息。FSN 的光遗传学沉默减少了自发舔运动,这表明 FSN 有助于特定自发运动的启动和执行,可能是通过塑造附近 PN 的反应选择性。

更新日期:2023-06-08
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