Opinion
A Closer Look at the Hippocampus and Memory

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Memory experiments do not typically measure exploratory viewing behavior, and therefore the observed neural signals can reflect an unknown mixture of processing related to memory, perception, and visual exploration.

Experiments that quantify viewing behaviors during memory formation suggest that important memory–viewing interactions have been missed in previous research, warranting re-evaluation of conclusions about memory mechanisms supported by structures such as the hippocampus.

The hippocampus contributes to viewing during memory formation by providing online memory representations to guide effective exploration, which results in coherently organized memories.

This new theoretical perspective suggests that the hippocampus and viewing are tightly intertwined because hippocampal contributions to memory formation unfold over the timecourse of an episode in synchrony with the timecourse of viewing behavior.

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.

Section snippets

A New View of Memory Formation

Episodes of experience unfold over time and comprise various inter-related stimuli. Episodic memory (see Glossary) requires binding together these stimuli and their spatial, temporal, and conceptual relationships to form coherent memory representations 1, 2. Because perception has limited bandwidth, only a fraction of all the information comprising an episode will be effectively ‘sampled' by an individual. It is therefore straightforward to assume that the resulting episodic memories will

fMRI Confounds Hiding in Plain View

Visual exploration has astonishing speed and complexity, with an average of approximately four to five visual fixations to distinct and idiosyncratically selected portions of the environment made every second [3], including during memory experiments (Figure 1A). The stimulus durations typical of memory experiments (approximately 0.5–6 s) therefore permit substantial visual exploration. These characteristics of viewing behavior provide stiff challenges to experiments on memory.

Memory experiments

Evidence Linking the Hippocampus to Viewing Behavior

Neural recordings obtained directly from the hippocampus via depth electrodes in nonhuman primates and in humans have indicated that viewing behavior is strongly related to hippocampal activity (reviewed in [28]). For instance, visual fixations are associated with evoked activity of hippocampus and surrounding medial temporal cortical areas [29]. Hippocampal theta-band oscillatory activity has been strongly implicated in memory [30]. Visual fixations are generated at theta frequency [3], and

Hippocampal Contributions to Exploratory Viewing for Memory Formation

The aforementioned findings establish an association between hippocampal activity and viewing behavior during memory formation, but what is the nature of this association? In particular, does the hippocampus have any direct role in driving viewing behavior, or is its association with viewing merely a byproduct of its role in memory? If the role of the hippocampus in viewing behavior were only secondary, then its activity in relation to viewing would simply reflect the bottom-up flow of visual

Concluding Remarks

We first considered several possible ramifications of viewing behavior in memory experiments that do not either control or measure it, despite using stimuli that promote complex viewing patterns. Viewing determines the nature of visual input, and therefore has substantial face-validity as a key factor in almost any experimental design. Given that ‘nothing in neurobiology makes sense except in the light of behavior’ [63], it is imperative that rigorous measures of behavior, including viewing,

Acknowledgments

Support was provided by awards R21-MH108863 and R01-MH062500 from the National Institute of Mental Health. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Glossary

Episodic memory
memory for episodes of experience, including the storage and recall of sights, sounds, location, time, and other contextual information that define an event. The defining quality of episodic memory for the present purposes is that it requires binding together of these arbitrarily inter-related episodic fragments into an integrated relational memory representation.
Online memory representation
the ongoing maintenance of memory in an active state. Typically observed by measuring

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