Precision, binding, and the hippocampus: Precisely what are we talking about?
Section snippets
Spatiotemporal context: why is it important to episodic memory?
To successfully retrieve an item or other information that was encoded in episodic memory, one needs a cue specific to the encoding situation, which is often referred to as the context or source under which an item was encoded. For example, recovering the thoughts that we had when we encoded the word “cat” could provide sufficient information to cue recovery of the word “cat,” like the image of a tabby or other cats that got lost in Davis. In this way, context itself might not be unique, but
How does “precision” emerge from representation of context?
While we have considered the computational properties of temporal context to involve diffusion drift (Howard and Kahana, 2002; Long et al., 2015; Polyn et al., 2009), we have not defined the spatial aspects of spatiotemoral context. Past work considering spatial context has argued that such representations should be metric (e.g., Bellmund et al., 2018). Like a piece of graph paper, such a representation contains an underlying organization that follows Euclidean rules of geometry, for example,
Precision and context
Given the importance of unique contextual representations in allowing differentiation of memories, it seems reasonable to consider in more depth what one might mean with regard to “unique.” This is an instance in which we think considering the precision of contextual representations becomes particularly important. To differentiate an item on a list from all other occurrences of that item, there needs to be sufficient information embedded in the contextual representation to serve as an
Neural basis of contextual precision and binding within the hippocampus
Binding, or the process of associating a high-dimensional context with an item during encoding, depends primarily on the hippocampus, consistent with arguments from amnesia, neuroimaging, and other methodologies (Davachi et al., 2003; Davachi and Wagner, 2002; Diana et al., 2007; Eichenbaum et al., 2007; Hamann and Squire, 1997; Insausti et al., 2013; Lee et al., 2002; Lepage et al., 1998; Milner et al., 1968; Scoville and Milner, 1957; Sherman et al., 2011; Stark and Squire, 2000; Yonelinas et
Contextual precision and episodic memory outside of the hippocampus
The hippocampus is not the only brain area in which contextual processing and pattern completion/separation occur (e.g., Cowell, et al., 2019). Consistent with this idea, recent work has also highlighted the roles of areas outside of the hippocampus in episodic memory. In support of this idea, both imaging and lesion evidence in humans suggest that posterior parietal cortex, medial prefrontal cortex, precuneus/retrosplenial cortex, and other parts of the “core recollection network” are also
Precision, context, and hippocampal function
To better understand context, we also need to consider how such an entity might take shape in the first place. As we have discussed, many aspects of context are likely built on semantic knowledge, what could be termed a scaffold or a script (Bartlett, 1932; Schank and Abelson, 1977). One issue, however, as discussed above, is that the more static elements present in a contextual representation the less effective it will be at distinguishing different encoded items at retrieval. One way of
The neural basis of precision
Somewhat unlike the operation of binding of item and context, precision refers to the quality of a representation that would appear to be shared across many different brain networks and regions (Cowell et al., 2019). We can readily talk about the idea of precision, for example, in the sensory domain. When we perceive a scene, this necessitates some form of representation within primary visual cortex. If we hear a sound and remember it, this requires some form of representation within primary
Novel explanatory and predictive power
We hope that our proposal here regarding episodic memory and hippocampal involvement in memory and beyond will be helpful in generating new experiments. Theoretically, we think the somewhat ubiquitous role of the hippocampus in areas outside of memory has remained a bit of a puzzle, and classic theories of declarative memory do not have a clear explanation of how this could be so (Squire, 1992; Squire et al., 2004). Yet, the evidence that hippocampal lesions impact perception, working memory,
Conclusion
We have elucidated on the important concept of representational precision here to attempt to explain both the role of the hippocampus in item-context bindings and its contributions to representation more generally. The first area we explored, item-context binding, is widely recognized as important to episodic memory in particular and involves associating a unique context with an item representation. We suggest here that binding relies primarily on the hippocampus, with other brain regions
Acknowledgments
NIH grant NS093052 to ADE and APY. NIH grant NS076856 to ADE. NIH grant EY025999 to APY.
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2024, Psychiatry Research - NeuroimagingPersistent neuronal firing in the medial temporal lobe supports performance and workload of visual working memory in humans
2022, NeuroImageCitation Excerpt :Patients with MTL lesions failed in object-location maintenance, even at lower workload conditions, but not when maintenance of only spatial or color information is required (Finke et al., 2008; Olson et al., 2006; Owen et al., 1995), made more swapping errors, i.e. errors related to undetected reversed relative positions of item pairs (Pertzov et al., 2013; Watson et al., 2013), and made more errors when working memory required maintaining objects in high perceptual resolution (Aly et al., 2013; Koen et al., 2017). These operations might depend on the special role of the MTL in processing relational representations, including binding of items to a context during navigation (Ekstrom and Yonelinas, 2020; Jonides et al., 2008). That view is also supported by several functional magnetic resonance imaging studies (Libby et al., 2014; Piekema et al., 2006; von Allmen et al., 2013).
Independent features form integrated objects: Using a novel shape-color “conjunction task” to reconstruct memory resolution for multiple object features simultaneously
2022, CognitionCitation Excerpt :This perspective is supported by one previous neuroimaging study which found dependence between “gist” memory of object color and spatial context operationalized using a mixture model, which may be comparable to the results of our “yes” response bin (Cooper & Ritchey, 2019). Importantly, this previous study provides initial neural evidence that more integrated representations may be lower in resolution than less integrated representations (but see perspectives by Yonelinas, 2013; Ekstrom & Yonelinas, 2020). Although researchers have found dependence between lower-resolution object color representations bound to spatial context (Cooper & Ritchey, 2019), to our knowledge no neuroimaging studies have yet examined how the brain supports memory resolution for integrated and independent features for multiple features associated within the same object (e.g., shape and color).
Missing links: The functional unification of language and memory (L∪M)
2022, Neuroscience and Biobehavioral ReviewsCitation Excerpt :When actively engaged in verbal information processing, the IFG (pars opercularis in particular) could be an essential contributor to assembly operations (Merge; Zaccarella and Friederici, 2015). The hippocampus architecture is conducive to active links between multimodal information (Ekstrom and Yonelinas, 2020; Fig. 5 for details). Together and integrated into a vast network, these regions actively link different elements, leading to an increasingly rich representational content.