Department of Physiology, Hokkaido University School of Medicine, Sapporo 060-8638, Japan.
Department of Physiology, Hokkaido University School of Medicine, Sapporo 060-8638, Japan
J Neurosci. 2021 Mar 3;41(9):1917-1927. doi: 10.1523/JNEUROSCI.2151-20.2021. Epub 2021 Jan 15.
Prediction of periodic event timing is an important function for everyday activities, while the exact neural mechanism remains unclear. Previous studies in nonhuman primates have demonstrated that neurons in the cerebellar dentate nucleus and those in the caudate nucleus exhibit periodic firing modulation when the animals attempt to detect a single omission of isochronous repetitive audiovisual stimuli. To understand how these subcortical signals are sent and processed through the thalamocortical pathways, we examined single-neuron activities in the central thalamus of two macaque monkeys (one female and one male). We found that three types of neurons responded to each stimulus in the sequence in the absence of movements. Reactive-type neurons showed sensory adaptation and gradually waned the transient response to each stimulus. Predictive-type neurons steadily increased the magnitude of the suppressive response, similar to neurons previously reported in the cerebellum. Switch-type neurons initially showed a transient response, but after several cycles, the direction of firing modulation reversed and the activity decreased for each repetitive stimulus. The time course of Switch-type activity was well explained by the weighted sum of activities of the other types of neurons. Furthermore, for only Switch-type neurons the activity just before stimulus omission significantly correlated with behavioral latency, indicating that this type of neuron may carry a more advanced signal in the system detecting stimulus omission. These results suggest that the central thalamus may transmit integrated signals to the cerebral cortex for temporal information processing, which are necessary to accurately predict rhythmic event timing. Several cortical and subcortical regions are involved in temporal information processing, and the thalamus will play a role in functionally linking them. The present study aimed to clarify how the paralaminar part of the thalamus transmits and modifies signals for temporal prediction of rhythmic events. Three types of thalamic neurons exhibited periodic activity when monkeys attempted to detect a single omission of isochronous repetitive stimuli. The activity of one type of neuron correlated with the behavioral latency and appeared to be generated by integrating the signals carried by the other types of neurons. Our results revealed the neuronal signals in the thalamus for temporal prediction of sensory events, providing a clue to elucidate information processing in the thalamocortical pathways.
预测周期性事件的时间是日常活动的一项重要功能，但其确切的神经机制尚不清楚。先前在非人类灵长类动物中的研究表明，当动物试图检测到等时重复视听刺激的单次缺失时，小脑齿状核和尾状核中的神经元表现出周期性的放电调制。为了了解这些皮质下信号如何通过丘脑皮质通路发送和处理，我们检查了两只猕猴（一只雌性，一只雄性）中央丘脑的单个神经元活动。我们发现，在没有运动的情况下，三种类型的神经元对序列中的每个刺激都有反应。反应型神经元表现出感觉适应，并且对每个刺激的瞬态反应逐渐减弱。预测型神经元则稳定地增加抑制反应的幅度，类似于先前在小脑报告的神经元。转换型神经元最初表现出瞬态反应，但经过几个周期后，放电调制的方向反转，对每个重复刺激的活动减少。转换型活动的时间过程很好地解释了其他类型神经元活动的加权和。此外，只有转换型神经元在刺激缺失前的活动与行为潜伏期显著相关，这表明这种类型的神经元可能在检测刺激缺失的系统中携带更高级的信号。这些结果表明，中央丘脑可能会将整合后的信号传输到大脑皮层以进行时间信息处理，这对于准确预测节奏事件的时间至关重要。几个皮质和皮质下区域参与时间信息处理，而丘脑将在功能上发挥作用，将它们连接起来。本研究旨在阐明丘脑旁层部分如何传输和修改用于节奏事件时间预测的信号。当猴子试图检测到等时重复刺激的单次缺失时，三种类型的丘脑神经元表现出周期性活动。一种类型的神经元的活动与行为潜伏期相关，似乎是由其他类型的神经元携带的信号整合产生的。我们的结果揭示了丘脑在感觉事件时间预测中的神经元信号，为阐明丘脑皮质通路中的信息处理提供了线索。
