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Robust routing of spatial information by subiculum neurons
Takuma Kitanishi1,2 (Kenji Mizuseki1)

Spatial navigation is fundamentally important for animal survival. Hippocampal neurons diversely represent a variety of spatial navigation parameters such as an animal’s current place, running speed, and trajectory. To support navigational behavior output, hippocampal information is likely distributed to extrahippocampal areas. However, little is known about how diverse hippocampal information is distributed to downstream areas. In this study, we revealed the outflow of spatial information from the hippocampus to four downstream regions through the subiculum, the major hippocampal output structure. We performed large-scale neuronal recordings from the rat hippocampus and subiculum while identifying the projection targets of individual subicular neurons with optogenetics. Subicular neurons robustly represented multiple types of navigation-associated information as accurately as or even more accurately than hippocampal neurons. Speed- and trajectory-dependent firings were most prominent in neurons projecting to the retrosplenial cortex (RSC) and nucleus accumbens (NAC), respectively. Place-related firing was uniformly observed in neurons targeting the retrosplenial cortex, nucleus accumbens, anteroventral thalamus (AV), and medial mammillary body (MMB). Theta oscillations and sharp-wave/ripples tightly controlled the firing of projection neurons in a target region–specific manner. These findings address how, which, and when information is emitted from the subiculum to downstream targets, providing a comprehensive view of spatial information flow from the hippocampal formation. The results potentially contribute to understanding the pathophysiology of hippocampus-associated dementia.

Kitanishi T*, Umaba R, Mizuseki K*. Robust information routing by dorsal subiculum neurons.
Science Advances, 7:eabf1913 (2021). *corresponding authors. https://doi.org/10.1126/sciadv.abf1913

<Figure Legends>
(A) We revealed the spatial information flow from the hippocampus to four downstream areas via the subiculum by combining large-scale neuronal recordings and optogenetics.
(B) Place representation in the hippocampus and subiculum. Subicular neurons were less specific to place but maintained a higher firing rate and thus were more resistant to network noises compared with hippocampal neurons.

1Department of Physiology, Osaka City University Graduate School of Medicine, Japan.
2PRESTO, Japan Science and Technology Agency (JST), Japan.