Elsevier

NeuroImage

Volume 34, Issue 2, 15 January 2007, Pages 827-838
NeuroImage

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

https://doi.org/10.1016/j.neuroimage.2006.10.009Get rights and content

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.

Introduction

The human memory system is supported by multiple processes (Squire and Zola-Morgan, 1991, Cabeza and Nyberg, 2000, Tulving, 2002, Habib et al., 2003). Recent functional neuroimaging studies have shown that areas in the prefrontal, parietal and temporal cortices are involved in memory encoding and retrieval (Tulving et al., 1994, Demb et al., 1995, Buckner et al., 1998, Buckner et al., 1999, Buckner and Koutstaal, 1998, Wagner et al., 1998, Lepage et al., 2000).

Among these memory-related areas, prefrontal cortex (PFC) is thought to subserve cognitive control processes (Goldman-Rakic, 1987, Schacter, 1987, Shimamura, 1995, Fuster, 1997, Takahashi and Miyashita, 2002), and send top-down signals to posterior cortices (Incisa della Rocchetta and Milner, 1993, Gazzaniga, 1995, Tomita et al., 1999, Takahashi and Miyashita, 2002). Recently, a two-stage model of PFC has been proposed (Petrides, 1994a, Petrides, 1994b, Petrides, 1996, Owen et al., 1996). In this model, ventrolateral prefrontal cortex (VLPFC) interacts with posterior cortices such as temporal cortex for active (or controlled) encoding and retrieval of information, whereas dorsolateral prefrontal cortex (DLPFC) monitors and manipulates maintained information in VLPFC. Anatomical studies in nonhuman primates have shown direct corticocortical connections from VLPFC to temporal cortex (Petrides and Pandya, 2002), but direct connections from DLPFC to temporal cortex are still controversial (Seltzer and Pandya, 1989, Petrides and Pandya, 1994, Petrides and Pandya, 1999, Petrides, 2005).

Based on these studies we hypothesized two possibilities for the anatomical connections between PFC and temporal cortex in humans (Fig. 1A); (i) Serial Pathway Model: DLPFC connects with VLPFC, and VLPFC connects with temporal cortex, but DLPFC does not connect with temporal cortex, (ii) Parallel Pathway Model: DLPFC and VLPFC both connect with temporal cortex. In this study, we performed diffusion tensor imaging (DTI) fiber tracking from functionally defined memory areas to test these two connectivity models.

DTI is a new technique based on the diffusion properties of water molecules as detected from diffusion-weighted magnetic resonance images (Basser et al., 1994). A number of fiber tracking algorithms have been developed to visualize white matter fiber tracts from DTI images (Mori et al., 1999, Jones et al., 1999, Conturo et al., 1999). Although many studies have shown anatomical connections per se in the human brain (Conturo et al., 1999, Basser et al., 2000, Stieltjes et al., 2001, Xu et al., 2002, Behrens et al., 2003, Lehericy et al., 2004, Powell et al., 2004), no studies to date have related memory functions with anatomical connections in the same subject within one experiment (but see Dougherty et al., 2005, Kim et al., 2006 for connections among visual areas). Here, we show the feasibility and usefulness of such studies by combining functional magnetic resonance imaging (fMRI) and DTI in the same subject to show the anatomical network underlying memory functions in the human brain. The main goal of this study is to determine the pattern of anatomical connections between well-known memory-related activations observed in previous recognition memory studies (Buckner and Koutstaal, 1998, Buckner et al., 1998, Buckner et al., 1999, Wagner et al., 1998, Lepage et al., 2000, Habib et al., 2003). By studying anatomical connections, we hope to determine whether functional interactions between these areas are direct or indirect.

Section snippets

Subjects

Twenty healthy normally sighted subjects were tested (8 males and 12 females, aged 21–39, mean age 25). All subjects reported themselves to be native speakers of English, right handed, with no neurological or psychiatric histories. Written informed consent in accordance with the Declaration of Helsinki was obtained from each subject after the nature and possible consequences of the studies were explained. The procedures were approved by the Boston University School of Medicine.

Stimuli

Word stimuli

Results

The mean percent correct in the encoding phase was 96 ± 4% (mean ± SEM; n = 20) for the living/nonliving judgment task, and 97 ± 3% for the detection task. They were not significantly different (p > 0.05; two-tailed t-test). Reaction times were 1.17 ± 0.05 s for the living/nonliving judgments task, 1.07 ± 0.05 s for the detection task, and 0.80 ± 0.05 s for the visuo-motor control task (mean ± SEM). These reaction times were significantly different (F(2,54) = 13.8, p < 10 4, one-way ANOVA). In the post hoc Tukey's t

Discussion

By combining fMRI and DTI in vivo, we demonstrated that two fronto-temporal anatomical pathways between functionally defined memory-related areas. Many functional neuroimaging studies have suggested that the fronto-temporal pathway is involved in deep encoding processing and retrieval efforts with the top-down signaling (Buckner et al., 1998, Takahashi and Miyashita, 2002). Consistent with functional correlation studies that have suggested interaction between frontal and temporal cortices (

Acknowledgments

We thank Dorothe A. Poggel and Itamar Ronen for their helpful comments on this paper, and Jeff Thompson, Elizabeth Appleby and Kim Ono for their helpful editorial comments. This work was supported by NIH (NS44825), and the Human Frontiers Science Program. The first author (E.T.) was supported by the Uehara Memorial Foundation (Japan).

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