Department of Psychological & Brain Sciences, Indiana University 47405-7007, Bloomington, IN.
School of Informatics, Computing, and Engineering, Indiana University 47405-7007, Bloomington, IN.
Proc Natl Acad Sci U S A. 2023 Jan 10;120(2):e2207677120. doi: 10.1073/pnas.2207677120. Epub 2023 Jan 5.
One of the essential functions of biological neural networks is the processing of information. This includes everything from processing sensory information to perceive the environment, up to processing motor information to interact with the environment. Due to methodological limitations, it has been historically unclear how information processing changes during different cognitive or behavioral states and to what extent information is processed within or between the network of neurons in different brain areas. In this study, we leverage recent advances in the calculation of information dynamics to explore neural-level processing within and between the frontoparietal areas AIP, F5, and M1 during a delayed grasping task performed by three macaque monkeys. While information processing was high within all areas during all cognitive and behavioral states of the task, interareal processing varied widely: During visuomotor transformation, AIP and F5 formed a reciprocally connected processing unit, while no processing was present between areas during the memory period. Movement execution was processed globally across all areas with predominance of processing in the feedback direction. Furthermore, the fine-scale network structure reconfigured at the neuron level in response to different grasping conditions, despite no differences in the overall amount of information present. These results suggest that areas dynamically form higher-order processing units according to the cognitive or behavioral demand and that the information-processing network is hierarchically organized at the neuron level, with the coarse network structure determining the behavioral state and finer changes reflecting different conditions.
生物神经网络的基本功能之一是处理信息。这包括从处理感觉信息以感知环境,到处理运动信息以与环境交互的所有内容。由于方法学上的限制,历史上不清楚信息处理在不同的认知或行为状态下如何变化,以及在不同的大脑区域的神经元网络内或之间处理了多少信息。在这项研究中,我们利用信息动力学计算的最新进展,探索了三只猕猴在执行延迟抓握任务期间,顶额区 AIP、F5 和 M1 之间的神经水平处理。虽然在任务的所有认知和行为状态下,所有区域内的信息处理都很高,但区域间的处理却大不相同:在视觉运动转换期间,AIP 和 F5 形成了一个相互连接的处理单元,而在记忆期间,区域之间没有处理。运动执行在所有区域中进行整体处理,反馈方向的处理占主导地位。此外,尽管存在的信息量没有差异,但精细的网络结构在神经元水平上响应不同的抓握条件重新配置。这些结果表明,区域根据认知或行为需求动态形成更高阶的处理单元,并且信息处理网络在神经元水平上是分层组织的,粗网络结构决定行为状态,更精细的变化反映不同的条件。