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Rhinal Cortex Asymmetries in Patients with Mesial Temporal Sclerosis

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Rhinal Cortex Asymmetries in Patients with Mesial Temporal Sclerosis View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Seizure (2008) 17, 234—246 www.elsevier.com/locate/yseiz Rhinal cortex asymmetries in patients with mesial temporal sclerosis Catherine E. Meade *, Stephen C. Bowden, Greg Whelan, Mark J. Cook St. Vincent’s Hospital Melbourne, Clinical Neurosciences, Victoria Pde, Fitzroy, Melbourne, Victoria 3065, Australia Received 13 April 2007; received in revised form 2 July 2007; accepted 10 July 2007 KEYWORDS Summary Rhinal cortex; Handedness; Purpose: The rhinal cortex, comprising the entorhinal (ErC) and perirhinal (PrC) Hippocampus; cortices, is one component of the limbic system that may be affected in patients with Memory; epilepsy and other temporal lobe pathologies. This study extended quantitative Volumetric imaging examination of the limbic system through development and validation of volumetric protocols to measure the ErC and PrC. Methods: Volumes were calculated from MRI studies using ANALYZE 7.5 and based on detailed anatomical definitions developed for the study. Subjects were 61 temporal lobe epilepsy patients with mesial temporal sclerosis (MTS: 33 left, 28 right) and 20 neurologically normal controls. Inter-rater reliabilities for the ErC and PrC volume protocols were found to be high (range 0.86—0.92). Results: Ipsilateral hippocampal volume was reduced in patients with MTS, while contralateral volume did not differ significantly from controls. In the patients, rhinal cortex volumes were reduced as a function of laterality of disease. The pattern of correlations between ErC and PrC differed between disease groups. Hippocampal and rhinal cortex volumes were not significantly correlated. A significant four-way inter- action was found between side of MTS, hemisphere, structure and handedness. Conclusions: This quantitative study demonstrates reliable in vivo evidence of morphometric changes in ErC and PrC in a substantial number of patients with unilateral MTS. The relationship observed between handedness, structure and disease status may suggest a role for cerebral dominance in modulating the expression of MTS. # 2007 Published by Elsevier Ltd on behalf of British Epilepsy Association. Introduction * Corresponding author. Tel.: +61 39288 3073; The entorhinal (ErC) and perirhinal (PrC) cortices are fax: +61 39288 3551. crucial components in the pathway through which E-mail address: [email protected] (C.E. Meade). highly processed information from the neocortex 1059-1311/$ — see front matter # 2007 Published by Elsevier Ltd on behalf of British Epilepsy Association. doi:10.1016/j.seizure.2007.07.010 Rhinal cortex asymmetries in patients with MTS 235 reaches the hippocampal formation and the amyg- human research.21,22 The PrC, with its close anato- dala.1 ErC, PrC as well as the parahippocampal gyrus mical and functional connections with the ErC, may (PHG) are heavily interconnected.2 The PrC receives also show morphometric changes in patients with input from the temporal, parietal, occipital, cingu- MTS. Bernasconi and colleagues found PrC abnorm- late and insular cortices and is one of the major inputs alities in two of six TLE patients examined. However, to the ErC, which then conveys this highly processed the distributional properties of the volume changes information to the hippocampus via the perforant were not discussed.23 pathway.3,4 So, while the ErC connects directly to the The present study extends quantitative examina- hippocampus, connections from the PrC and PHG to tion of the limbic system through the development the hippocampus are indirect, via relays in the ErC.5,6 and validation of detailed volumetric protocols to The hippocampus is thus the final stage of conver- measure the ErC and PrC. The volumetric protocols gence within the medial temporal lobe.7 will then be used to examine relationships in the Progress in the modelling of medial temporal lobe rhinal cortex in a substantial homogeneous group of (limbic system) function has been limited by the TLE patients, all with MTS. The fact that this dis- technological problems associated with character- order can result in pathological changes in different ising deep brain structures in vivo.8 The advent of mesial temporal structures also provides a unique volumetric magnetic resonance imaging (MRI) ana- opportunity to explore relationships between struc- lysis provides an opportunity to clarify issues of tures of interest, without the confounds of invasive human temporal lobe structure, by permitting a techniques. The proposed research has the poten- direct investigation of in vivo morphology. MRI volu- tial to improve our understanding of the patterns of metry is based on the principle that the response of limbic pathology in patients with MTS. neurons to disease is gliosis and cell loss.9 It follows that neural disease may be reflected in the mea- surement of discrete structures in vivo. Indeed, Materials and methods several studies have documented a close correlation between histopathologically determined cell loss Participants and atrophy as measured through hippocampal volume measurements.10—12 Several research Subjects were 61 consecutive patients with TLE groups now regard volumetric MRI as a surrogate admitted to the Comprehensive Epilepsy Program for histological examination of the hippocampus9,13 at St. Vincent’s Hospital, Melbourne. The Commis- and incorporate this technique routinely in their sion on Classification and Terminology of the Inter- pre-surgical analysis of temporal lobe epilepsy national League Against Epilepsy24 classifies TLE as a (TLE) patients with mesial temporal (hippocampal) symptomatic form of location-related (focal or par- sclerosis (MTS). tial) epilepsies and syndromes. Patients were iden- The exact limbic structures involved in MTS remain tified on the basis of clinical features, interictal uncertain.14 Histopathologically, MTS has been scalp/sphenoidal EEG, prolonged EEG-video moni- defined as cell loss and reactive gliosis in the hippo- toring and neuropsychological studies. Fifty-nine of campus, predominantly in field CA4, but often invol- the 61 patients have so far proceeded to anterior ving areas CA1 and CA3 and the subiculum.15 The temporal lobectomy, with histopathological confir- amygdala and dentate fascia are also often mation of MTS in all cases. Till date, two patients affected.16 Attempts to define the extent of damage have chosen not to proceed with surgery, but results in adjacent structures, namely the ErC and PrC, have of the above investigations are suggestive of typical been sparse.17 Recently, one group documented ErC MTS. Thirty-three patients had left MTS, 28 had right volume reductions ipsilateral to the epileptic focus in MTS. Of the patients with left MTS, 14 were male MTS patients with hippocampal volume reductions,18 and 19 were female, with a mean age of 37 years as well as those with normal hippocampal volume.19 (S.D. = 9.4). Nine of the left MTS group were left- In the latter study, nine of 22 patients had histo- handed, 24 were right-handed. Handedness was pathologically confirmed MTS, but ErC volumes were defined as laterality preference, as assessed by a examined in the group as a whole, making it difficult handedness questionnaire routinely administered to draw conclusions about the significance of ErC by the treating neurologist during initial consulta- changes. Salmenpera and colleagues documented tion. The questionnaire is available on request from ErC changes in a subpopulation of patients with the first author. For brevity, laterality of preference cryptogenic TLE, with mixed pathology, but did not will be referred to subsequently as handedness. Of examine MTS patients separately.20 The involvement the right MTS group, 15 were male and 13 were of ErC in the generation and propagation of temporal female, with a mean age of 36 years (S.D. = 11.9). lobe seizures has been documented in animal and Six of this group were left-handed, 22 were right- 236 C.E. Meade et al. handed. Twenty neurologically normal community The region of interest measurements were per- volunteers were examined as the control group, formed by an operator (CM), who was blind to the taken from a consecutive series of participants in side of MTS. Reliability of the protocol was then a wider research study being undertaken at St. examined by a second rater (MC), who measured ErC Vincent’s Hospital. The control subjects had no and PrC on the same 20 MRI studies, blinded to the history of head injury or significant medical or results of the first rater. The inter-rater reliabilities psychiatric illness. Ten control subjects were (Pearson product—moment correlations) for left and female, 10 were male. Mean age for all control right ErC were 0.86 and 0.90, respectively, and for subjects was 34 years (S.D. = 14.8). Handedness left and right PrC, inter-rater reliabilities were 0.92 data was available on 11 control subjects, 9 of whom and 0.91, respectively. Anatomical specifications for were right-handed, 2 were left-handed. There were the borders of ErC and PrC are defined at three no significant differences between control and levels moving through the structures from anterior patient groups on age (F(2,78) = 0.617, p = 0.542) to posterior. ErC and PrC volumes were traced or gender ratio (x2 = 0.790, d.f. = 2, p = 0.674). manually according to the defined protocol, using Data collection and imaging analysis of the a tracker-ball driven cursor. Area and volume were patients was conducted under approval of the automatically calculated by pixel counting. Hippo- Human Research Ethics Committee of St. Vincent’s campal volumes for patient and control subjects Hospital, Melbourne. were measured previously by MC using published protocols,10,26 as part of routine pre-surgical eva- MR acquisition luation in the MTS patients and the wider research study in the control group. The MRI images were acquired pre-surgically for the MTS patients, using a high-resolution 1.5-T scanner Histological and gross anatomical (Seimens and G.E.
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