Neural Firing Patterns Are More Schematic and Less Sensitive to Changes in Background Visual Scenes in the Subiculum than in the Hippocampus

Literature suggests that the hippocampus is central to processing visual scenes to remember contextual information, but the roles of its downstream structure, subiculum, remain unknown. Here, single units were recorded simultaneously in the dorsal CA1 and subiculum while male rats made spatial choices using visual scenes as cues in a T-maze. The firing fields of subicular neurons were schematically organized following the task structure, largely divided into pre-choice and post-choice epochs, whereas those of CA1 cells were more punctate and bound to specific locations. When the rats were tested with highly familiar scenes, neurons in the CA1 and subiculum were indistinguishable in coding the task-related information (e.g., scene, choice) through rate remapping. However, when the familiar scenes were blurred parametrically, the neurons in the CA1 responded sensitively to the novelty in task demand and changed its representations parametrically following the physical changes of the stimuli, whereas these functional characteristics were absent in the subiculum. These results suggest that the unique function of the hippocampus is to acquire contextual representations in association with discrete positions in space, especially when facing new and ambiguous scenes, whereas the subiculum may translate the position-bound visual contextual information of the hippocampus into schematic codes once learning is established.

SIGNIFICANCE STATEMENT Although the potential functional significance has been recognized for decades for the subiculum, its exact roles in a goal-directed memory task still remain elusive. In the current study, we present experimental evidence that may indicate that the neural population in the subiculum could translate the location-bound spatial representations of the hippocampus into more schematic representations of task demands. Our findings also imply that the visual scene-based codes conveyed by the hippocampus and subiculum may be identical in a well learned task, whereas the hippocampus may be more specialized in representing altered visual scenes than the subiculum.