Dominguez-Vargas Adan-Ulises, Schneider Lukas, Wilke Melanie, Kagan Igor
Decision and Awareness Group, Cognitive Neuroscience Laboratory, German Primate Center, Leibniz Institute for Primate Research, Goettingen 37077, Germany.
Department of Cognitive Neurology, University of Goettingen, Goettingen 37075, Germany.
J Neurosci. 2017 Feb 22;37(8):2234-2257. doi: 10.1523/JNEUROSCI.1984-16.2016. Epub 2017 Jan 24.
The pulvinar complex is interconnected extensively with brain regions involved in spatial processing and eye movement control. Recent inactivation studies have shown that the dorsal pulvinar (dPul) plays a role in saccade target selection; however, it remains unknown whether it exerts effects on visual processing or at planning/execution stages. We used electrical microstimulation of the dPul while monkeys performed saccade tasks toward instructed and freely chosen targets. Timing of stimulation was varied, starting before, at, or after onset of target(s). Stimulation affected saccade properties and target selection in a time-dependent manner. Stimulation starting before but overlapping with target onset shortened saccadic reaction times (RTs) for ipsiversive (to the stimulation site) target locations, whereas stimulation starting at and after target onset caused systematic delays for both ipsiversive and contraversive locations. Similarly, stimulation starting before the onset of bilateral targets increased ipsiversive target choices, whereas stimulation after target onset increased contraversive choices. Properties of dPul neurons and stimulation effects were consistent with an overall contraversive drive, with varying outcomes contingent upon behavioral demands. RT and choice effects were largely congruent in the visually-guided task, but stimulation during memory-guided saccades, while influencing RTs and errors, did not affect choice behavior. Together, these results show that the dPul plays a primary role in action planning as opposed to visual processing, that it exerts its strongest influence on spatial choices when decision and action are temporally close, and that this choice effect can be dissociated from motor effects on saccade initiation and execution. Despite a recent surge of interest, the core function of the pulvinar, the largest thalamic complex in primates, remains elusive. This understanding is crucial given the central role of the pulvinar in current theories of integrative brain functions supporting cognition and goal-directed behaviors, but electrophysiological and causal interference studies of dorsal pulvinar (dPul) are rare. Building on our previous studies that pharmacologically suppressed dPul activity for several hours, here we used transient electrical microstimulation at different periods while monkeys performed instructed and choice eye movement tasks, to determine time-specific contributions of pulvinar to saccade generation and decision making. We show that stimulation effects depend on timing and behavioral state and that effects on choices can be dissociated from motor effects.
丘脑枕复合体与参与空间处理和眼动控制的脑区广泛相连。最近的失活研究表明,背侧丘脑枕(dPul)在扫视目标选择中起作用;然而,它是否对视觉处理或在计划/执行阶段产生影响仍不清楚。我们在猴子执行向指示目标和自由选择目标的扫视任务时,对dPul进行电微刺激。刺激时间各不相同,在目标出现之前、之时或之后开始。刺激以时间依赖的方式影响扫视特性和目标选择。在目标出现之前但与目标出现重叠时开始的刺激缩短了向同侧(朝向刺激部位)目标位置的扫视反应时间(RTs),而在目标出现时及之后开始的刺激导致同侧和对侧位置都出现系统性延迟。同样,在双侧目标出现之前开始的刺激增加了同侧目标选择,而在目标出现之后的刺激增加了对侧选择。dPul神经元的特性和刺激效应与整体的对侧驱动一致,其结果因行为需求而异。在视觉引导任务中,RT和选择效应在很大程度上是一致的,但在记忆引导扫视期间的刺激,虽然影响RTs和错误,但不影响选择行为。总之,这些结果表明,dPul在动作计划而非视觉处理中起主要作用,当决策和动作在时间上接近时,它对空间选择产生最强的影响,并且这种选择效应可以与对扫视启动和执行的运动效应相分离。尽管最近人们对其兴趣激增,但灵长类动物中最大的丘脑复合体——丘脑枕的核心功能仍然难以捉摸。鉴于丘脑枕在当前支持认知和目标导向行为的整合脑功能理论中的核心作用,这种理解至关重要,但对背侧丘脑枕(dPul)的电生理和因果干扰研究很少。基于我们之前药理学抑制dPul活动数小时的研究,在此我们在猴子执行指示性和选择性眼动任务时,在不同时期使用短暂的电微刺激,以确定丘脑枕对扫视产生和决策的时间特异性贡献。我们表明,刺激效应取决于时间和行为状态,并且对选择的影响可以与运动效应相分离。