Improved spatial memory in a modular network mimicking the prefrontal-thalamo-hippocampal triangular circuit

The hippocampus (HPC), prefrontal cortex (PFC), and thalamic nuclei, such as reuniens (Re), form a reciprocally connected circuit that plays a critical role in processing hippocampus-dependent memory. Accumulating evidence suggests that this triangular modular circuit is crucial for performing cognitive tasks that require context-dependent memory, which belong to a class of behavioral tasks difficult for animals to learn. Experiments are gradually revealing what behavioral information these brain regions represent, but how the triangular circuit gives rise to the observed divisions of labor remains unknown. It is also unclear whether the triangular modular circuit brings any advantage in solving such tasks. Here, we addressed these questions by constructing a prefrontal-thalamo-hippocampal circuit model comprising interconnected long-short-term memory (LSTM) units and training it on contextual memory-dependent spatial navigation tasks. Our model revealed the critical roles of the distinct brain modules. The HPC module encoded spatial information, whereas the PFC module represented the spatiotemporal task structure in a context-dependent manner. The Re module integrated task-relevant information to facilitate learning in the PFC and HPC modules, dynamically harmonizing these modules. The thalamic coordination of the other modules enhanced the systems robustness in learning to navigate complex environments. This division of labor between the HPC, PFC, and Re modules was not specified a priori but emerged through learning, showing an interesting coincidence with the task-related activities of the prefrontal-thalamo-hippocampal circuit. Our results demonstrate that the multi-modular network structure is crucial for robust processing of context-dependent memory.