The inferior parietal lobule and recognition memory: expectancy violation or successful retrieval?

Abstract

Functional neuroimaging studies of episodic recognition demonstrate an increased lateral parietal response for studied versus new materials, often termed a retrieval success effect. Using a novel memory analog of attentional cueing, we manipulated the correspondence between anticipated and actual recognition evidence by presenting valid or invalid anticipatory cues (e.g., "likely old") before recognition judgments. Although a superior parietal region demonstrated the retrieval success pattern, a larger inferior parietal lobule (IPL) region tracked the validity of the memory cueing (invalid cueing > valid cueing) and no retrieval success-sensitive lateral parietal region was insensitive to cueing. The invalid cueing response occurred even for correctly identified new items unlikely to trigger substantive episodic retrieval. Within the IPL, although supramarginal and angular gyrus (SMG; AG) regions both demonstrated invalid cueing amplitude elevations, each region differentially coupled with distinct cortical networks when unexpectedly old items were encountered; a connectivity pattern also observed at rest in the same subjects. These findings jointly suggest that the lateral parietal response during recognition does not signify the recovery of episodic content, but is a marker of the violation of memory expectations. A second independent dataset confirmed this interpretation by demonstrating that SMG activation tracked the decision biases of observers, not their accuracy, with increased activation for nondominant recognition judgments. The expectancy violation interpretation of the lateral parietal recognition response is consistent with the literature on visual search and oddball paradigms and suggests that damage to these regions should impair memory-linked orienting behavior and not retrieval per se.

Figure 1.

Schematic diagram of the experimental paradigm. A, Test session order for all participants. B, Differences between low-run-validity sessions and high-run-validity sessions. C, The components of a single 6000 ms test trial.

Figure 2.

Task-evoked maps and amplitude responses. A, Regions demonstrating significant activation in the retrieval success contrast (hits vs correct rejections). B, Regions demonstrating significant activation in the invalid cueing contrast (invalid cueing vs valid cueing). Ci, The 256 voxel SMG (blue) cluster was defined by inclusively masking the left hemisphere temporoparietal cluster from the invalid cueing contrast map (thresholded at p < 0.001, 5 contiguous voxels) with the dorsomedial seed resting-state map, exclusive of voxels also lying in the anteromedial seed map (masks thresholded at p < 0.001) (for further explanation of resting-state seeds and maps, see Results, Resting and task-evoked connectivity, and Fig. 3A,B). The 314 voxel AG (red) cluster was defined in a similar way, by inclusively masking the parietal portion of the left hemisphere, invalid cueing, temporoparietal cluster with the anteromedial seed resting-state map exclusive of voxels in the dorsomedial seed map. Clusters are viewed from left and posterior aspects. Cii, Mean β parameter estimates from SMG (top panels) and AG clusters (bottom panels) in response to valid and invalid cueing. Error bars represent SEs. CRs, Correct rejections.

Figure 3.

Resting-state seeds and maps. A, ROIs used to seed resting-state analyses: dorsomedial PFC ROI (an 8-mm-diameter sphere with center [3, 24, 51]; blue); anteromedial PFC ROI (an 8-mm-diameter sphere with center [0, 63, 27]; red). ROIs are viewed from left and anterior aspects. B, Resting-state network of regions demonstrating significant activation associated with the activation of the dorsomedial seed (blue) and the activation of the anteromedial seed (red; overlap in purple; thresholded at p < 0.001, 5 contiguous voxels). C, Maps of the same seed regions (dorsomedial seed network, blue; anteromedial seed network, red) entered into one model and directly contrasted (thresholded at p < 0.001, 5 contiguous voxels). D, Conjunction map of regions demonstrating activation associated with the conjunction of the invalid cueing effect contrast (thresholded at p < 0.001, 5 contiguous voxels) and anteromedial seed resting-state network (thresholded at p < 0.001, 5 contiguous voxels; red) and dorsomedial seed resting-state network (thresholded at p < 0.001, 5 contiguous voxels; blue; overlap in purple).

Figure 4.

Schematic diagram and results of task-evoked connectivity analysis. These analyses demonstrating the degree to which AG and SMG seeds differ in their coupling with ROIs in the two independently defined resting connectivity networks. A, ROIs were 115 8-mm-diameter spheres centered on local maxima from the invalid cueing contrast (not shown in this figure; see Fig. 2B). ROIs were identified as target ROIs if their centers lay within either the dorsomedial seed (35) or anteromedial seed (29) resting-state maps (blue and red, respectively). ROIs with centers lying in both resting-state maps (9) or neither map (42) were excluded from this analysis. A small number of spheres representing possible target and nontarget ROIs are shown for illustrative purposes. SMG and AG clusters are shown in white (see Fig. 2Ci for details of how they were defined). B, Differential βs (invalid minus valid cueing βs) from all target ROIs were cross-correlated (across all 19 participants) with differential βs from the SMG and AG clusters (see Fig. 2A), producing two correlation coefficients per target ROI for each combination of run validity (high or low) and item status (hit or correct rejection). Correlations between differential βs from one target ROI and SMG/AG clusters, under one run-status combination (hits under high run validity), are shown. C, Correlation coefficients were entered into an ANOVA. Means are broken down in the four panels (i–iv) by run validity (rows) and item status (hits, correct rejections; columns) with each panel showing the mean correlation coefficients between βs (invalid minus valid cue trials) from SMG (blue) and AG clusters (red) and dorsomedial (left) and anteromedial target ROIs (right). Error bars represent SEs. CRs, Correct rejections.

Figure 5.

Response bias correlation maps. A, Regions demonstrating significant correlation with response bias. B, Multiplicative conjunction map of regions demonstrating activation associated with the conjunction of response bias correlation and invalid cueing effect maps (both thresholded at p < 0.005, 5 contiguous voxels). C, Scatter plots showing differential βs (hits minus correct rejections) from an independently defined ROI in lateral parietal cortex (an 8-mm-diameter sphere with center [−42, −54, 42]; shown in yellow on coronal section) plotted against the following: response bias (c) (i) and accuracy (d′) (ii).