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Neuronal Activity in the Premotor Cortex of Monkeys Reflects Both Cue Salience and Motivation for Action Generation and Inhibition
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2021-09-08 , DOI: 10.1523/jneurosci.0641-20.2021
Margherita Giamundo , Franco Giarrocco , Emiliano Brunamonti , Francesco Fabbrini , Pierpaolo Pani , Stefano Ferraina

Reward prospect weighs on motor decision processes, enhancing the selection of appropriate actions and the inhibition of others. While many studies have investigated the neuronal basis of reward representations and of cortical control of actions, the neuronal correlates of the influences of reward prospect on motor decisions are less clear. We recorded from the dorsal premotor cortex (PMd) of 2 male macaque monkeys performing a modified version of the Stop-signal (countermanding) task. This task challenges motor decisions by requiring responding to a frequent Go stimulus, but to suppress this response when a rare Stop signal is presented during the reaction time. We unbalanced the motivation to respond or to suppress the response by presenting a cue informing on three different rewards schedules: in one case, Go trials were rewarded more than Stop trials; in another case, Stop trials were rewarded more than Go trials; in the last case, both types of trials were rewarded equally. Monkeys adopted different strategies according to reward information provided by the cue: the higher the reward for Stop trials, the higher their ability to suppress the response and the slower their response to Go stimuli. PMd neuronal activity evolved in time and correlated with the behavior: PMd signaled first the cue salience, representing the chance to earn the highest reward at stake, then reflected the shaping of the motor choice by the motivation to move or to stop. These findings represent a neuronal correlate of the influence of reward information on motor decision.

SIGNIFICANCE STATEMENT The motivation to obtain rewards drives how animals act over their environment. To explore the involvement of motor cortices in motivated behaviors, we recorded high-resolution neuronal activity in the premotor cortex of monkeys performing a task that manipulated the motivation to generate/withhold a movement through different cued reward probabilities. Our results show the presence of neuronal signals dynamically reflecting the salience of the cue, in the time immediately following its presentation, and a motivation-related activity in performing (or cancelling) a motor program, while the behavioral response approached. The encoding of multiple reward-related signals in this region leads to consider an important role of premotor areas in the reward circuitry supporting action.



中文翻译:

猴子前运动皮层的神经元活动反映了提示显着性和动作产生和抑制的动机

奖励前景会影响运动决策过程,增强对适当行为的选择和对他人的抑制。虽然许多研究已经调查了奖励表征和皮层动作控制的神经元基础,但奖励前景对运动决策影响的神经元相关性尚不清楚。我们从 2 只雄性猕猴的背侧运动前皮层 (PMd) 进行记录,它们执行了停止信号(反命令)任务的修改版本。这项任务需要对频繁的 Go 刺激做出响应,从而挑战运动决策,但在反应时间内出现罕见的停止信号时要抑制这种响应。我们通过在三种不同的奖励时间表上提供提示来平衡响应或抑制响应的动机:在一种情况下,Go 试验的奖励比 Stop 试验多;在另一种情况下,停止试验的奖励比围棋试验更多;在最后一种情况下,两种类型的审判都得到同等奖励。猴子根据提示提供的奖励信息采取不同的策略:停止试验的奖励越高,抑制反应的能力就越高,对围棋刺激的反应越慢。PMd 神经元活动随时间演变并与行为相关:PMd 首先发出提示显着性的信号,代表获得最高奖励的机会,然后通过移动或停止的动机反映运动选择的形成。这些发现代表了奖励信息对运动决策影响的神经元相关性。两种类型的试验都得到同等奖励。猴子根据提示提供的奖励信息采取不同的策略:停止试验的奖励越高,抑制反应的能力就越高,对围棋刺激的反应越慢。PMd 神经元活动随时间演变并与行为相关:PMd 首先发出提示显着性的信号,代表获得最高奖励的机会,然后通过移动或停止的动机反映运动选择的形成。这些发现代表了奖励信息对运动决策影响的神经元相关性。两种类型的试验都得到同等奖励。猴子根据提示提供的奖励信息采取不同的策略:停止试验的奖励越高,抑制反应的能力就越高,对围棋刺激的反应越慢。PMd 神经元活动随时间演变并与行为相关:PMd 首先发出提示显着性的信号,代表获得最高奖励的机会,然后通过移动或停止的动机反映运动选择的形成。这些发现代表了奖励信息对运动决策影响的神经元相关性。他们抑制反应的能力越高,对围棋刺激的反应就越慢。PMd 神经元活动随时间演变并与行为相关:PMd 首先发出提示显着性的信号,代表获得最高奖励的机会,然后通过移动或停止的动机反映运动选择的形成。这些发现代表了奖励信息对运动决策影响的神经元相关性。他们抑制反应的能力越高,对围棋刺激的反应就越慢。PMd 神经元活动随时间演变并与行为相关:PMd 首先发出提示显着性的信号,代表获得最高奖励的机会,然后通过移动或停止的动机反映运动选择的形成。这些发现代表了奖励信息对运动决策影响的神经元相关性。

重要性声明获得奖励的动机驱使动物如何对环境采取行动。为了探索运动皮层在动机行为中的参与,我们记录了猴子前运动皮层中的高分辨率神经元活动,该活动执行一项任务,通过不同的提示奖励概率来操纵产生/抑制运动的动机。我们的研究结果表明,神经元信号的存在动态地反映了线索的显着性,在其出现后的时间内,以及在执行(或取消)运动程序时与动机相关的活动,而行为反应接近。该区域中多个奖励相关信号的编码导致考虑前运动区域在奖励回路支持动作中的重要作用。

更新日期:2021-09-09
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