Elsevier

NeuroImage

Volume 22, Issue 2, June 2004, Pages 740-747
NeuroImage

Noninvasive in vivo demonstration of the connections of the human parahippocampal gyrus

https://doi.org/10.1016/j.neuroimage.2004.01.011Get rights and content

Abstract

MR tractography techniques provide a method for noninvasively studying white matter pathways in vivo. In this study we have used diffusion tensor imaging (DTI) and the fast marching tractography (FMT) algorithm to plot the structural connectivity of the human parahippocampal gyrus (PHG) in 10 healthy subjects, using seed points selected in the anterior parahippocampal gyrus. Our results demonstrate connectivity between the parahippocampal gyrus and the anterior temporal lobe, orbitofrontal areas, posterior temporal lobe and extrastriate occipital lobe via the lingual and fusiform gyri. We also demonstrate for the first time noninvasively direct connectivity between the parahippocampal gyrus and the hippocampus itself. These results agree with previous histological tract-tracing studies in animals. The connections demonstrated between neocortical areas and the hippocampus via the parahippocampal gyrus may provide the structural basis for theoretical models of memory and higher visual processing.

Introduction

Understanding the relationship between brain structure and function would be made easier by a detailed knowledge of the anatomical connections of the white matter fibres linking functional regions. In 1877 Meynert classified myelinated fibres into three major groups: association fibres, commissural fibres and projection fibres, and subsequent major contributions were made by the dissections of Dejerine (1895) and Klinger (1935) (Tamaraz and Comair, 2000). As yet, however, little is known about the anatomical connections of regions involved in behaviours such as memory, emotion and perception. Hippocampal and parahippocampal regions have been closely linked to these higher-order behaviours. The parahippocampal gyrus includes the entorhinal cortex anteriorly, an area known to have direct and extensive connections with the hippocampus and dentate gyrus. The parahippocampal gyrus is thought to be involved in the translation of temporary hippocampal information storage to a more permanent storage in cortical association areas (Rolls, 2000).

Neuroanatomical tracing methods have provided information on cortical input to the medial temporal lobe (MTL), demonstrating widespread connections from sensory-specific and multimodal association cortices converging on the parahippocampal gyrus (Pandya and Kuypers, 1969). These types of invasive tract-tracing procedures, such as the histological staining of postmortem tissue (Burgel et al., 1999) and the study of degenerating axons using silver staining (Di Virgilio et al., 1999), have significant limitations when used on the human brain (Rye, 1999). In addition none of these techniques have provided detailed information on any but the more major pathways.

Diffusion tensor imaging (DTI) is an MRI technique that evaluates brain structure through the three-dimensional measurement of water molecules' diffusion in tissue. Obstructions to this motion, such as cell membranes, cause restricted diffusion and this restriction is arranged in a highly directional manner in white matter fibres. DTI allows calculation of the magnitude of diffusional motion (diffusivity), the directionality of the motion (anisotropy) and the principal orientation of diffusion for each voxel Pierpaoli and Basser, 1996, Pierpaoli et al., 1996. This information can be used to evaluate connectivity between voxels, determine pathways of anatomical CNS connections in vivo and to provide information on the integrity of white matter tracts with alterations in tissue organisation resulting in altered diffusion and anisotropy Basser et al., 2000, Conturo et al., 1999, Jones et al., 1999, Mori et al., 1999, Parker et al., 2002a, Parker et al., 2002b, Poupon et al., 2000.

We used the fast marching tractography (FMT) technique to detect possible connection pathways from a seed point in the brain. This provides 3D connectivity maps representing an informal probability of connectivity between this seed point and each voxel in the brain.

Our aim was to use FMT to study the connectivity of the human anterior parahippocampal gyrus in vivo.

Section snippets

Subjects

Ten healthy volunteers (six males) without any history of neurological or psychiatric disorders were included in this study. The age range of the subjects was 30–54 years with a median of 35. Eight subjects were right handed, and two were left handed. The study was approved by the National Hospital for Neurology and Neurosurgery and the Institute of Neurology Joint Research Ethics Committee, and informed written consent was obtained from all subjects.

MR data acquisition

MRI studies were performed on a 1.5-T

Group maps

The unthresholded maps showed connections from the seed points selected in the anterior parahippocampal gyrus in all subjects on the left and right side. These were evaluated based on the colour-coded connectivity values of the tracts in the figures and different connections are described here based on these connectivity values. The connectivity values reported below are related to the confidence that we have that a fibre bundle exists between regions, and suggest a hierarchy in the

Discussion

This study demonstrates in vivo the connectivity between the parahippocampal gyrus and anterior temporal lobe, orbitofrontal areas and posterior temporal and extrastriate occipital areas via the lingual and fusiform gyri. We also demonstrated direct hippocampal–parahippocampal connectivity for the first time noninvasively. These multisynaptic connections between neocortical areas and the hippocampus via the parahippocampal gyrus may provide the structural basis for memory processing and

References (36)

  • N.I Bohnen et al.

    Cerebellar changes in partial seizures: clinical correlations of quantitative SPECT and MRI analysis

    Epilepsia

    (1998)
  • M Catani et al.

    Occipito-temporal connections in the human brain

    Brain

    (2003)
  • T.E Conturo et al.

    Tracking neuronal fiber pathways in the living human brain

    Proc. Natl. Acad. Sci. U. S. A.

    (1999)
  • G Di Virgilio et al.

    Cortical regions contributing to the anterior commissure in man

    Exp. Brain Res.

    (1999)
  • R Insausti et al.

    The entorhinal cortex of the monkey: II. Cortical afferents

    J. Comp. Neurol.

    (1987)
  • R Insausti et al.

    MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices

    Am. J. Neuroradiol.

    (1998)
  • R.J Ivnik et al.

    Effects of anterior temporal lobectomy on cognitive function

    J. Clin. Psychol.

    (1987)
  • D.K Jones et al.

    Non-invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI

    Magn. Reson. Med.

    (1999)
  • Cited by (0)

    View full text