Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain - PubMed (original) (raw)

. 2007 Sep 24;14(10):645-54.

doi: 10.1101/lm.575107. Print 2007 Oct.

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Spatial and temporal episodic memory retrieval recruit dissociable functional networks in the human brain

Arne D Ekstrom et al. Learn Mem. 2007.

Abstract

Imaging, electrophysiological studies, and lesion work have shown that the medial temporal lobe (MTL) is important for episodic memory; however, it is unclear whether different MTL regions support the spatial, temporal, and item elements of episodic memory. In this study we used fMRI to examine retrieval performance emphasizing different aspects of episodic memory in the context of a spatial navigation paradigm. Subjects played a taxi-driver game ("yellowcab"), in which they freely searched for passengers and delivered them to specific landmark stores. Subjects then underwent fMRI scanning as they retrieved landmarks, spatial, and temporal associations from their navigational experience in three separate runs. Consistent with previous findings on item memory, perirhinal cortex activated most strongly during landmark retrieval compared with spatial or temporal source information retrieval. Both hippocampus and parahippocampal cortex activated significantly during retrieval of landmarks, spatial associations, and temporal order. We found, however, a significant dissociation between hippocampal and parahippocampal cortex activations, with spatial retrieval leading to greater parahippocampal activation compared with hippocampus and temporal order retrieval leading to greater hippocampal activation compared with parahippocampal cortex. Our results, coupled with previous findings, demonstrate that the hippocampus and parahippocampal cortex are preferentially recruited during temporal order and spatial association retrieval--key components of episodic "source" memory.

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Figures

Figure 1.

Figure 1.

Behavioral methods and results. (A) Screen shot of a passenger waiting on sidewalk from a virtual city that subjects explored. (B) Overview layout of location of stores in virtual city; stores are labeled in black, buildings labeled in white. (C–E) Following navigation, subjects performed an episodic retrieval task in the scanner composed of three different conditions: (C) a landmark recognition condition, (D) a spatial association retrieval condition, and (E) a temporal order retrieval condition (see Materials and Methods). (F) Mean performance was above chance (50%; red-dotted line) in all conditions across subjects.

Figure 2.

Figure 2.

Activations in the hippocampus and parahippocampal cortex during retrieval of recently learned spatial information. (A) Group mean cluster activations in standard MNI space for 14 subjects during retrieval of landmarks, passenger–store associations (spatial association condition), and orderings of passengers (temporal order condition). We observed significant bilateral hippocampal, parahippocampal, and perirhinal cortex activations. Numbers next to slices indicate MNI values in millimeters of slice locations. Activations were thresholded at Z = 2.3. ROI analysis for these regions shown in B–G. (B) In left hippocampus, we observed greater activations during landmark recognition and spatial association conditions compared with the temporal order condition. (C) In right hippocampus, we did not find differences between conditions. However, all three conditions activated hippocampus bilaterally. (D) Left parahippocampal cortex showed greater activation during spatial association retrieval than the other two conditions; landmark recognition activated the left parahippocampal cortex to a greater extent than temporal order retrieval. (E) Right parahippocampal activation was also higher during spatial association retrieval than the other two conditions. (F) Left

perirhinal activation was higher during landmark retrieval than spatial and temporal retrieval. (G) Right perirhinal activity was higher during landmark retrieval compared with temporal order retrieval. (H) We observed a significant dissociation between hippocampal and parahippocampal activations during spatial and temporal order retrieval; spatial retrieval activated parahippocampus to a greater extent than hippocampus, and temporal order retrieval activated hippocampus to a greater extent than parahippocampus. (I) We also found a significant dissociation between parahippocampal cortex and perirhinal cortex; spatial retrieval led to greater activation in parahippocampal cortex compared with landmark retrieval, while the opposite trend (greater activation during landmark than spatial retrieval) was observed in perirhinal cortex.

Figure 3.

Figure 3.

Extra-hippocampal activations and retrosplenial region of interest analysis. (A) Outside of the hippocampus, significant activations in retrosplenial cortex, prefrontal cortex, and cingulate are readily identifiable in the mean across all three retrieval conditions. (B) ROI of retrosplenial cortex indicated overall significantly more activation during landmark retrieval and spatial association retrieval (combined) compared with temporal order; the contrast of spatial association vs. temporal order failed to reach significance. (C) In a group analysis, comparison of the spatial retrieval condition against temporal order retrieval, distinct clusters of activation were present in retrosplenial cortex. Activations were thresholded at Z = 2.3. Significant retrosplenial clusters of activation were also present when we contrasted landmark recognition against temporal order retrieval; no other contrasts showed significant retrosplenial activations.

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