Elsevier

NeuroImage

Volume 27, Issue 1, 1 August 2005, Pages 231-239
NeuroImage

Material-specific lateralization of memory encoding in the medial temporal lobe: Blocked versus event-related design

https://doi.org/10.1016/j.neuroimage.2005.04.033Get rights and content

Abstract

Lesion-deficit studies have provided evidence for a functional dissociation between the left medial temporal lobe (MTL) mediating verbal memory encoding and right MTL mediating non-verbal memory encoding. While a small number of functional MRI studies have demonstrated similar findings, none has looked specifically for material-specific lateralization using subsequent memory effects. In addition, in many fMRI studies, encoding activity has been located in posterior MTL structures, at odds with lesion-deficit and positron emission tomography (PET) evidence. In this study, we used an event-related fMRI memory encoding paradigm to demonstrate a material-specific lateralization of encoding in the medial temporal lobes of ten healthy control subjects. Activation was left-lateralized for word encoding, bilateral for picture encoding, and right-lateralized for face encoding. Secondly, we demonstrated the locations of activations revealed using an event-related analysis to be more anterior than those revealed using a blocked analysis of the same data. This suggests that anterior MTL structures underlie memory encoding as judged by subsequent memory effects, and that more posterior activity detected in other fMRI studies is related to deficiencies of blocked designs in the analysis of memory encoding.

Introduction

Evidence from studies of amnesic patients and targeted lesions in animals led to the hypothesis that the hippocampus and related medial temporal lobe (MTL) structures are critical for the encoding of information for subsequent long-term storage (Squire and Zola-Morgan, 1991). Such studies have provided evidence for a dissociation in function between the dominant (usually the left) MTL, mediating verbal memory (Frisk and Milner, 1990), and non-dominant (usually the right) MTL mediating non-verbal or visual memory (Smith and Milner, 1981). Further evidence for this material-specific lateralization in function comes from patients undergoing unilateral anterior temporal lobe resection for refractory temporal lobe epilepsy. Typically, these patients show a decline in verbal memory following surgery involving the language-dominant hemisphere (Ivnik et al., 1987) and deficits in topographical memory following non-dominant temporal lobe resection (Spiers et al., 2001).

Memory encoding involves a network of regions including prefrontal cortices in addition to the MTL. While a number of positron emission tomography (PET) and functional MRI (fMRI) studies have provided strong evidence for a functional dissociation in the prefrontal cortices (Demb et al., 1995, Fletcher and Henson, 2001, Iidaka et al., 2000, Kirchhoff et al., 2000, Shallice et al., 1994, Wagner et al., 1998), this has been less well documented in the MTL. Few studies have attempted to demonstrate functional dissociation of encoding of different stimulus types in the same subjects and in the same experimental session; however, it is only through such studies that functional dissociation can be demonstrated. One study by Kelley and colleagues used three different material types: words, line-drawings of objects, and unfamiliar faces, to demonstrate a clear lateralization of activation in both dorsal frontal cortex and MTL in five healthy control subjects. They concluded that encoding of words was left-lateralized, faces right-lateralized, and objects bilateral in both brain regions (Kelley et al., 1998). Similar findings from Golby et al. suggested that the lateralization of encoding processes is determined by the verbalizability of the stimuli being encoded (Golby et al., 2001).

Both these studies employed blocked experimental designs and therefore could not specifically look for successful encoding, as determined by subsequent memory effect. By using an event-related experimental design, it is possible to compare activation for those items subsequently remembered with those forgotten, allowing successful memory encoding to be directly studied. One recent study employed an event-related design to show encoding for words in the left hippocampus in normal subjects but did not examine non-verbal memory (Richardson et al., 2003) while other studies linking MTL activation with episodic encoding have not shown such clear lateralization of function (Fernandez et al., 1998, Stern et al., 1996).

A further area of debate concerns the localization of memory encoding within the MTL. The clinical description of patients with impaired memory encoding following anterior temporal lobe resections suggests that anterior MTL regions are critical for successful memory encoding. Functional imaging studies, however, have proved contradictory with many showing encoding-related activations located in posterior hippocampal and parahippocampal regions (Detre et al., 1998, Dupont et al., 2000, Gabrieli et al., 1997, Golby et al., 2001, Kelley et al., 1998, Kirchhoff et al., 2000, Stern et al., 1996). One possible explanation for this apparent conflict is that anterior temporal regions are subject to susceptibility artifacts and signal loss leading to reduced signal-to-noise ratio. Another possibility is that, as all the above studies employed blocked rather than event-related designs, the areas of activation seen were due to other cognitive processes, separate from memory encoding.

In this experiment, we employed an event-related fMRI study of verbal and non-verbal memory encoding to address these issues. We used an experimental design which permits data analysis either as a blocked design, or as an event-related design of successful encoding of each material type. We optimized fMRI acquisition parameters to maximize sensitivity to the anterior MTL. We test the hypothesis that the successful encoding of verbal and non-verbal material shows different lateralization in the MTL. We also test the hypothesis that a blocked design reveals activity in the posterior MTL regions, whereas an event-related design shows anterior (hippocampal) activity.

Section snippets

Subjects

We studied 10 right-handed native English-speaking healthy volunteers with no history of neurological or psychiatric disease. The age range was 23–37 years (median 30). 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 General Electric Signa Horizon scanner. Standard imaging gradients with a maximum strength

Results

Recognition accuracy for the stimuli seen during scanning was calculated for each stimulus type. A one-way ANOVA revealed significantly better (F = 39.44, P < 0.001) performance on memory for pictures (median 0.69, range 0.38–0.94) and words (median 0.64, range 0.3–0.9) compared to memory for faces (median 0.06, range 0.01–0.23). A subsequent memory effect was shown with recognition accuracy being significantly different from zero for all three material types (words t = 9.823, P < 0.001,

Discussion

Using an event-related fMRI paradigm, we have demonstrated material-specific lateralization of memory encoding in the anterior MTL in healthy control subjects. Activation was left-lateralized for word encoding, bilateral for picture encoding, and right-lateralized for face encoding. We examined an interaction between subsequent memory, material type, and laterality in order to establish material-specific lateralization. It is only by testing in this way that true functional segregation can be

Acknowledgments

This work was supported by the Wellcome Trust (Programme Grant No. 067176, RP, MRS), Action Medical Research (PAB), the National Society for Epilepsy (MJK, PT, JD), and the Medical Research Council (MPR). We have no financial conflict of interest to declare in relation to this publication.

References (50)

  • M.P. Richardson et al.

    Preserved verbal memory function in left medial temporal pathology involves reorganisation of function to right medial temporal lobe

    Neuroimage

    (2003)
  • S. Robinson et al.

    Optimized 3 T EPI of the amygdalae

    Neuroimage

    (2004)
  • M.L. Smith et al.

    The role of the right hippocampus in the recall of spatial location

    Neuropsychologia

    (1981)
  • J.P. Szaflarski et al.

    High-resolution functional MRI at 3 T in healthy and epilepsy subjects: hippocampal activation with picture encoding task

    Epilepsy Behav.

    (2004)
  • R.L. Buckner et al.

    Frontal cortex contributes to human memory formation

    Nat. Neurosci.

    (1999)
  • S. Corkin et al.

    H. M.'s medial temporal lobe lesion: findings from magnetic resonance imaging

    J. Neurosci.

    (1997)
  • A.R. Damasio et al.

    Prosopagnosia: anatomic basis and behavioral mechanisms

    Neurology

    (1982)
  • J.B. Demb et al.

    Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity

    J. Neurosci.

    (1995)
  • J.A. Detre et al.

    Functional MRI lateralization of memory in temporal lobe epilepsy

    Neurology

    (1998)
  • S. Dupont et al.

    Episodic memory in left temporal lobe epilepsy: a functional MRI study

    Brain

    (2000)
  • H.M. Duvernoy

    The Human Hippocampus

    (1998)
  • G. Fernandez et al.

    Successful verbal encoding into episodic memory engages the posterior hippocampus: a parametrically analyzed functional magnetic resonance imaging study

    J. Neurosci.

    (1998)
  • G. Fernandez et al.

    Real-time tracking of memory formation in the human rhinal cortex and hippocampus

    Science

    (1999)
  • P.C. Fletcher et al.

    Frontal lobes and human memory: insights from functional neuroimaging

    Brain

    (2001)
  • K.J. Friston et al.

    Statistical parametric maps in functional imaging: a general linear approach

    Hum. Brain Mapp.

    (1995)
  • Cited by (0)

    View full text