Medial temporal lobe activity predicts successful relational memory binding - PubMed (original) (raw)

Medial temporal lobe activity predicts successful relational memory binding

Deborah E Hannula et al. J Neurosci. 2008.

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 degrees 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.

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Figures

Figure 1.

Figure 1.

A, Illustration of the events associated with a single short-term memory trial. B, Examples of the three types of test displays; test displays were always rotated 90° counter-clockwise relative to the sample. Object-location bindings were intact in match displays, one of the objects (drums) moved to a new, previously unoccupied, location in mismatch-position displays, and two of the objects (drums, birdbath) swapped positions in mismatch-swap displays.

Figure 2.

Figure 2.

Regions in the left anterior (MNI coordinates: x = −36, y = −12, z = −21; max t = 5.17) and posterior (MNI coordinates: x = −27, y = −33, z = −3; max t = 4.29) hippocampus where BOLD signal was higher for correct than for incorrect trials during presentation of the sample stimulus; contrasts are superimposed on an averaged T1-weighted image. Plots of parameter estimates (indexing response amplitude) and trial-averaged time courses illustrate that anterior hippocampal activity decreased relative to the ITI baseline after presentation of the sample stimulus; the decrease was of smaller magnitude for correct (blue) than incorrect (pink) trials. Posterior hippocampal activity increased relative to the ITI baseline after presentation of the sample stimulus; the increase was larger for correct than incorrect trials. Note that the time courses begin with 4 s of prestimulus baseline activity.

Figure 3.

Figure 3.

Regions in the left (MNI coordinates: x = −30, y = −30, z = −3; max t = 4.20) and right (MNI coordinates: x = 27, y = −27, z = −6; max t = 4.90) posterior hippocampus where BOLD signal was higher for correct than for incorrect trials are shown; results are superimposed on an averaged T1-weighted image. Plots of parameter estimates for correctly identified test displays (match, mismatch position, and mismatch swap, respectively) and for test displays that elicited incorrect responses are presented for each brain region along with trial-averaged time courses. These graphs illustrate that activity associated with presentation of the test stimulus was graded as a function of display type; activity was greatest for correctly identified match displays, followed by mismatch-position, mismatch-swap, and finally incorrect test trials.

Figure 4.

Figure 4.

Right perirhinal (MNI coordinates: x = 33, y = −6, z = −33; max t = 4.75) and left hippocampal (MNI coordinates: x = −30, y = −33, z = −6; max t = 3.96) regions where BOLD signal was higher for correctly identified match than mismatch displays. Parameter estimates and trial-averaged time courses associated with correctly identified match (dark blue) and mismatch (light blue) test displays are shown.

Figure 5.

Figure 5.

Plots of prefrontal and parietal activation associated with short-term memory accuracy. A, Regions in right ventrolateral prefrontal cortex [Brodmann area (BA) 45/47; MNI coordinates: x = 51, y = 24, z = 6; max t = 6.41], and inferior intraparietal sulcus (MNI coordinates: x = 21, y = −78, z = 33; max t = 4.84) where activation during the sample period was greater for correct than for incorrect trials. Plots of parameter estimates for correct (blue) and incorrect (pink) trials are shown for each brain region along with trial-averaged time courses. B, A region in right dorsolateral prefrontal cortex (BA 9; MNI coordinates: x = 18, y = 42, z = 39; max t = 4.96) where test period activation was increased on correct, relative to incorrect trials. Plots of parameter estimates and trial-averaged time courses associated with correctly identified test displays (match, mismatch position, and mismatch swap, respectively) and with test displays that elicited incorrect responses are shown.

Figure 6.

Figure 6.

Entorhinal cortex recruitment during the early delay predicts individual differences in behavioral performance. A scatterplot shows the relationship between behavioral performance on the test of short-term memory (i.e., percentage correct) and short-term memory accuracy effects (i.e., the difference in the early delay parameter estimates between correct and incorrect trials) in the left entorhinal cortex.

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