A Closer Look at the Hippocampus and Memory

Abstract

Current interpretations of hippocampal memory function are blind to the fact that viewing behaviors are pervasive and complicate the relationships among perception, behavior, memory, and brain activity. For example, hippocampal activity and associative memory demands increase with stimulus complexity. Stimulus complexity also strongly modulates viewing. Associative processing and viewing thus are often confounded, rendering interpretation of hippocampal activity ambiguous. Similar considerations challenge many accounts of hippocampal function. To explain relationships between memory and viewing, we propose that the hippocampus supports the online memory demands necessary to guide visual exploration. The hippocampus thus orchestrates memory-guided exploration that unfolds over time to build coherent memories. This new perspective on hippocampal function harmonizes with the fact that memory formation and exploratory viewing are tightly intertwined.

Keywords: episodic; exploration; eye-movement tracking; fMRI; long-term.

Figure 1. The complexity of visual exploration is a challenge for memory experiments

A. Viewing data from three representative subjects are shown for one scene stimulus from a memory experiment using typical study conditions [71]. Visual fixations are plotted as colored circles, with radius indicating fixation duration and center indicating fixation onset. The locations of these fixations within the scene are shown in several-second intervals. Viewing behavior was highly idiosyncratic in time and space, including for the first 3-s interval (the approximate duration of stimuli in many memory experiments). For the entire group (N=21), the average overlap between any two subjects in viewing the same locations of any scene (36 scenes total) was only 56%. B. Hippocampal subsequent memory effects measured with fMRI are more robust for stimuli of higher complexity [9]. The richness of viewing behavior also increases with stimulus complexity, as shown here by purple circles to indicate typical viewing fixations. C. As reviewed in the text, stimuli with greater amounts of visual exploration are likely to be better remembered, and this is especially true for stimuli of relatively higher complexity. Hippocampal subsequent-memory effects (later-remembered versus later-forgotten stimuli), which are only robust for complex stimuli, therefore could reflect activity related to visual exploration.

Figure 2. Key Figure. Two possibilities for the role of hippocampus in viewing behavior

When studying a complex visual stimulus such as a scene, the viewing history at any given moment will constrain the memory representation that is formed (top). Factors other than memory, such as the perceptual salience of stimuli, can determine further viewing (left-bottom panel). In this scenario, the current status of memory is ignored when determining what to explore next. Thus, the final memory representation that results will likely be fragmented and incomplete. Visual information would be independently sent to hippocampus for memory processing and to oculomotor control regions for determination of further viewing. In contrast, our active-memory hypothesis is that the status of memory at any moment is used to direct further viewing (right-bottom panel). Crucial information such as weak memory for a subset of items or their interrelationships could therefore be used to direct exploration to the information that is needed to build a coherent memory representation. In this scenario, the hippocampus would interact with cortical oculomotor control regions, such that online memory representations could be used to drive exploration. Note that for simplicity of illustration we define an “initial period” as distinct from “further viewing”, although we propose that memory-exploration interplay is a dynamic process occurring in a continuous fashion as each new visual fixation is made. [Cortical oculomotor control regions taken from [90]: parietal eye field (PEF), frontal eye field (FEF), supplementary eye field (SEF), and dorsolateral prefrontal cortex (dlPFC). Purple indicates visual input and cortical visual processing regions. Subcortical projections of cortical oculomotor regions are not shown for simplicity, and are illustrated via an arrow projecting to the eye. Anatomical substrates for functional interactions of hippocampus with these cortical oculomotor control regions include dense structural interconnections of hippocampus with FEF, SEF, and dlPFC [91].]

Box Figure I. Influence of viewing on perceptual and conceptual overlap between study and test

Purple circles indicate hypothetical viewing locations at study and test, demonstrating how the same stimulus can foster both conceptual and perceptual study-test overlap depending on viewing at both occasions.