Significance of visual scene-based learning in the hippocampal systems across mammalian species.

The hippocampus and its associated cortical regions in the medial temporal lobe play essential roles when animals form a cognitive map and use it to achieve their goals. As the nature of map-making involves sampling different local views of the environment and putting them together in a spatially cohesive way, visual scenes are essential ingredients in the formative process of cognitive maps. Visual scenes also serve as important cues during information retrieval from the cognitive map. Research in humans has shown that there are regions in the brain that selectively process scenes and that the hippocampus is involved in scene-based memory tasks. The neurophysiological correlates of scene-based information processing in the hippocampus have been reported as "spatial view cells" in nonhuman primates. Like primates, it is widely accepted that rodents also use visual scenes in their background for spatial navigation and other kinds of problems. However, in rodents, it is not until recently that researchers examined the neural correlates of the hippocampus from the perspective of visual scene-based information processing. With the advent of virtual reality (VR) systems, it has been demonstrated that place cells in the hippocampus exhibit remarkably similar firing correlates in the VR environment compared with that of the real-world environment. Despite some limitations, the new trend of studying hippocampal functions in a visually controlled environment has the potential to allow investigation of the input-output relationships of network functions and experimental testing of traditional computational predictions more rigorously by providing well-defined visual stimuli. As scenes are essential for navigation and episodic memory in humans, further investigation of the rodents' hippocampal systems in scene-based tasks will provide a critical functional link across different mammalian species.

Subtle visual change in a virtual environment induces heterogeneous remapping systematically in CA1, but not CA3.

Environmental change may lead to new memories or modify old ones, but the underlying neural mechanisms are largely unclear. We recorded hippocampal place cells simultaneously from CA1 and CA3 in a virtual reality environment. Compared with CA1, place cells in CA3 are more tolerant of individual landmark changes but undergo orthogonal changes to code distinctively different environments. As visual noise (virtual fog) is introduced to a visually enriched environment, place cells in CA1 split into two subpopulations: in one, place cells maintain their field locations while changing their firing rates to reflect sensory changes; in the other, place cells exhibit global remapping in response to the contextual change. In contrast, place cells in CA3 exhibit mainly rate remapping under the same conditions. Our results suggest that CA1 may simultaneously represent heterogeneous maps of the same environment when subtle visual noise induces both sensory and contextual changes.

Goal-directed interaction of stimulus and task demand in the parahippocampal region.

The hippocampus and parahippocampal region are essential for representing episodic memories involving various spatial locations and objects, and for using those memories for future adaptive behavior. The "dual-stream model" was initially formulated based on anatomical characteristics of the medial temporal lobe, dividing the parahippocampal region into two streams that separately process and relay spatial and nonspatial information to the hippocampus. Despite its significance, the dual-stream model in its original form cannot explain recent experimental results, and many researchers have recognized the need for a modification of the model. Here, we argue that dividing the parahippocampal region into spatial and nonspatial streams a priori may be too simplistic, particularly in light of ambiguous situations in which a sensory cue alone (e.g., visual scene) may not allow such a definitive categorization. Upon reviewing evidence, including our own, that reveals the importance of goal-directed behavioral responses in determining the relative involvement of the parahippocampal processing streams, we propose the Goal-directed Interaction of Stimulus and Task-demand (GIST) model. In the GIST model, input stimuli such as visual scenes and objects are first processed by both the postrhinal and perirhinal cortices-the postrhinal cortex more heavily involved with visual scenes and perirhinal cortex with objects-with relatively little dependence on behavioral task demand. However, once perceptual ambiguities are resolved and the scenes and objects are identified and recognized, the information is then processed through the medial or lateral entorhinal cortex, depending on whether it is used to fulfill navigational or non-navigational goals, respectively. As complex sensory stimuli are utilized for both navigational and non-navigational purposes in an intermixed fashion in naturalistic settings, the hippocampus may be required to then put together these experiences into a coherent map to allow flexible cognitive operations for adaptive behavior to occur.