Diffusion tensor studies dissociated two fronto-temporal pathways in the human memory system - PubMed (original) (raw)

Diffusion tensor studies dissociated two fronto-temporal pathways in the human memory system

Emi Takahashi et al. Neuroimage. 2007.

Abstract

Recent functional neuroimaging studies have shown that multiple cortical areas are involved in memory encoding and retrieval. However, the underlying anatomical connections among these memory-related areas in humans remain elusive due to methodological limitations. Diffusion tensor imaging (DTI) is a technique based on detecting the diffusion of water molecules from magnetic resonance images. DTI allows non-invasive mapping of anatomical connections and gives a comprehensive picture of connectivity throughout the entire brain. By combining functional magnetic resonance imaging (fMRI) and DTI, we show that memory-related areas in the left dorsolateral prefrontal cortex (DLPFC) and the left ventrolateral prefrontal cortex (VLPFC) each connect with memory-related areas in the left temporal cortex. This result suggests there are two pathways between prefrontal cortex and temporal cortex related to the human memory system.

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Figures

Figure 1

Figure 1

(A) Two possible models of connections between the prefrontal and temporal cortices. (i) Serial Pathway Model: DLPFC connects with VLPFC, but not with the temporal cortex, and VLPFC connects with the temporal cortex, (ii) Parallel Pathway Model: DLPFC and VLPFC both connect with the temporal cortex. (B) Experimental design for functional imaging in encoding (left) and retrieval (right). In encoding, there are four conditions: living/nonliving, detection, visuo-motor control, and fixation. In retrieval, there are retrieval trials and visuo-motor control trials (see text and Materials and Methods for further details).

Figure 2

Figure 2

(A-D) Activation and fiber tracking from the activated areas in the encoding phase in the comparison “deep encoding versus visuo-motor control”. (A) Activated clusters (20 subjects, random effect analysis, p<0.001, uncorrected; p<0.05 corrected for whole-brain multiple comparisons at cluster level, only cortical activation clusters are displayed) are superimposed on T1-weighted normalized brain slices. The left hemisphere of the brain corresponds to the left side of the image. A color bar for T values of activated areas is shown at the bottom of the left. Z coordinates of Talairach space are shown on the top of each slice. (a) Left DLPFC (BA9/46/45), (b) left VLPFC (BA45/47/insula), (c) medial frontal gyrus (BA6), (d) right VLPFC (BA45/46), (e) left superior frontal gyrus (BA6), (f) left intraparietal sulcus (BA7) and (g) left STS and FG (BA21/22/37). BA:Brodmann’s Area. (B) The mean percent signal changes (across subject ± standard error) for the three conditions in the encoding phase. The bars in the left side show activation levels from “Deep” condition, the bars in the middle from “Shallow” condition, and the bars in the right from “Visuo-motor Control” condition. (C) Activated clusters using the same threshold as (A) are shown as red superimposed on a saggital view (top) and an axial view (bottom) of a brain. (a)-(g) represent the same areas as shown in (A). (D) All the reconstructed fibers from the left DLPFC (left) and left VLPFC (right) in single subject are shown as green in a saggital view (top) and an axial view (bottom). The activated areas are shown as yellow.

Figure 3

Figure 3

The average results of 20 subjects’ terminal points of DTI fiber tracking. The left hemisphere of the brain corresponds to the left side of the image. The terminals of the tracked fibers are shown as yellow to green. The colors indicate the number of subjects whose fiber tracking from any seed points terminated in the voxel (see color bar). Terminal points of fibers from encoding activation in the left DLPFC (top row), left VLPFC (middle row) and the left STS (bottom row). The end points of fiber tracking converged in (a) left inferior frontal gyrus (BA47), (b) left anterior to posterior insula, (c) left hippocampus/parahippocampal formation, (d) bilateral brain stem, (e) left inferior occipital gyrus (BA18), (f) left STS and FG (BA21/22/37), (g) left inferior frontal gyrus (BA44/45), (h) left frontal operculum (BA47), (i) left striatum, (j) left thalamus, (k) right inferior frontal gyrus (BA46), (l) left superior to middle frontal gyri (BA9/10), (m) left occipital gyrus (BA19), (n) left medial frontal gyrus (BA9), (o) left supplementary motor area (BA8), (p) left precuneus (BA7), (q) left middle frontal gyrus (BA6), (r) left inferior parietal gyrus (BA40), (s) left supplementary motor area (BA6), (t) left superior frontal gyrus (BA6), and (u) left postcentral gyrus.

Figure 4

Figure 4

Fibers between two activation clusters in five different subjects. (A) Reconstructed fibers between the left DLPFC (BA9/8/46/45) and left STS to FG (BA21/22/37) in the encoding phase. (B) Reconstructed fibers between the left VLPFC and the left STS to FG (BA21/22/37) in the encoding phase. (A: Anterior, P: posterior, D: dorsal, V: ventral, L: left, R: right). Fibers were tracked in both directions. For summary, see Table 2 and S2. (For connections between other clusters, see Supplementary Figure S7.)

Figure 5

Figure 5

(A) A histogram of the probability of a connection to DLPFC for every voxel in STS/FG of one subject. All the seed points of more than 50% of probability (red bars) were found in a small specific region in the temporal cortex. (B) Boot-trac analysis with 1000 iterations from a voxel (-49, -41, 0) in a single subject. Estimated probabilities of a connection to DLPFC were plotted against number of iterations (blue line). The averages (red line) and errors (SD) of probabilities at each iteration were estimated by shuffling the orders of the 1000 boot-trac samples (see the main text). (C) The locations of the continuous thirty-three seed points that showed more than 50 % of probability (green in the temporal cortex activation). (A: anterior, P: posterior, D: dorsal, V: ventral). (D) All the fibers for 100 bootstraps from a single seed point at (-49, -41, 0). (E) A probabilitistic map of the connection from a single seed point (Talairach: x, y, z = -49, -41, 0). The voxels with more than 10 % probabilities were color-coded. (F) A probabilitistic map of the connection from the 33 seed points of high probabilities in the temporal cortex (green). Voxels that showed more than 50 % were color-coded.

Figure 6

Figure 6

(A) A histogram of the numbers of the fibers between the DLPFC cluster and each of the 100 random clusters for one subject. (B) Histograms of actual numbers of fibers from DLPFC to the temporal cortex (black bars) and median numbers of fibers from DLPFC to random clusters (white bars) for 18 subjects.

Figure 7

Figure 7

Summary of the fiber tracking results between the activation clusters. (A) Encoding, (B) Retrieval. The pathways found in more than 10 subjects both by streamline and tensor deflection algorithms are shown as solid arrows, while a dotted arrow indicates the pathways found in more than 10 subjects only by tensor deflection. (For a complete table of connections, see Table 2 and Supplementary Table S2). DLPFC: dorso-lateral prefrontal cortex, VLPFC: ventro-lateral prefrontal cortex, SFG: superior frontal gyrus, STS: superior temporal sulcus, FG: fusiform gyrus, AC: anterior cingulated cortex: SMA: supplementary motor area, OTC: occipito-temporal cortex.

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