Medial Temporal Lobe Activity Predicts Successful Relational Memory Binding

Abstract

Previous neuropsychological findings have implicated medial temporal lobe (MTL) structures in retaining object-location relations over the course of short delays, but MTL effects have not always been reported in neuroimaging investigations with similar short-term memory requirements. Here, we used event-related functional magnetic resonance imaging to test the hypothesis that the hippocampus and related MTL structures support accurate retention of relational memory representations, even across short delays. On every trial, four objects were presented, each in one of nine possible locations of a three-dimensional grid. Participants were to mentally rotate the grid and then maintain the rotated representation in anticipation of a test stimulus: a rendering of the grid, rotated 90°from the original viewpoint. The test stimulus was either a "match" display, in which object-location relations were intact, or a "mismatch" display, in which one object occupied a new, previously unfilled location (mismatch position), or two objects had swapped locations (mismatch swap). Encoding phase activation in anterior and posterior regions of the left hippocampus, and in bilateral perirhinal cortex, predicted subsequent accuracy on the short-term memory decision, as did bilateral posterior hippocampal activity after the test stimulus. Notably, activation in these posterior hippocampal regions was also sensitive to the degree to which object-location bindings were preserved in the test stimulus; activation was greatest for match displays, followed by mismatch-position displays, and finally mismatch-swap displays. These results indicate that the hippocampus and related MTL structures contribute to successful encoding and retrieval of relational information in visual short-term memory.

Short-Term Memory and the Human Hippocampus

“…As such, the findings observed by Hannula and Ranganath (2008) resemble the well known phenomenon of "match enhancement" observed in monkey inferotemporal/perirhinal cortex in relation to the arrival of an anticipated target stimulus that matches the current stimulus being held in mind (Miller and Desimone, 1994) [Hannula and Ranganath (2008), their Fig. 3 (http://www.jneurosci.org/cgi/ content/full/28/1/116/F3)].…”

“…2 (http://www.jneurosci.org/cgi/ content/full/28/1/116/F2)[. Critically, a subsequent memory correlation was also observed in the hippocampus during the test phase [Hannula and Ranganath (2008), their Fig. 3 (http://www.…”

“…What is not clear from the neuropsychological data, however, is how the hippocampus supports this function. Hannula and Ranganath (2008) use functional magnetic resonance imaging (fMRI) to address this important issue by characterizing brain activity during each phase of a short-term associative memory task and by linking such neural activity to behavioral performance. Whereas a subsequent memory approach has been widely used to study long-term recognition memory, this has not been possible in previous short-term memory experiments because of the near-ceiling performance typically achieved by subjects.…”

“…During the sample phase of each trial, subjects viewed a novel scene consisting of four objects (out of a set of nine objects), each in one of nine possible locations in a 3 ϫ 3 grid [Hannula and Ranganath (2008) To encourage use of a hippocampally mediated allocentric (or world-centered) strategy, rather than an egocentric (or viewercentered) strategy thought to rely on parietal and prefrontal cortices, subjects were asked to form a mental image of the scene rotated 90°to the right of the original viewpoint. They were then required to maintain the rotated representation during the ensuing 11 s delay phase in anticipation of the test stimulus.…”

“…This revealed that hippocampal activity during the sample phase predicted successful recognition judgments in the test phase [Hannula and Ranganath (2008), their Fig. 2 (http://www.jneurosci.org/cgi/ content/full/28/1/116/F2)[.…”