Different structural correlates for verbal memory impairment in temporal lobe epilepsy with and without mesial temporal lobe sclerosis

Abstract

Objectives: Memory impairment is one of the most prominent cognitive deficits in temporal lobe epilepsy (TLE). The overall goal of this study was to explore the contribution of cortical and hippocampal (subfield) damage to impairment of auditory immediate recall (AIMrecall), auditory delayed recall (ADMrecall), and auditory delayed recognition (ADMrecog) of the Wechsler Memory Scale III (WMS-III) in TLE with (TLE-MTS) and without hippocampal sclerosis (TLE-no). It was hypothesized that volume loss in different subfields determines memory impairment in TLE-MTS and temporal neocortical thinning in TLE-no.

Methods: T1 whole brain and T2-weighted hippocampal magnetic resonance imaging and WMS-III were acquired in 22 controls, 18 TLE-MTS, and 25 TLE-no. Hippocampal subfields were determined on the T2 image. Free surfer was used to obtain cortical thickness averages of temporal, frontal, and parietal cortical regions of interest (ROI). MANOVA and stepwise regression analysis were used to identify hippocampal subfields and cortical ROI significantly contributing to AIMrecall, ADMrecall, and ADMrecog.

Results: In TLE-MTS, AIMrecall was associated with cornu ammonis 3 (CA3) and dentate (CA3&DG) and pars opercularis, ADMrecall with CA1 and pars triangularis, and ADMrecog with CA1. In TLE-no, AIMrecall was associated with CA3&DG and fusiform gyrus (FUSI), and ADMrecall and ADMrecog were associated with FUSI.

Conclusion: The study provided the evidence for different structural correlates of the verbal memory impairment in TLE-MTS and TLE-no. In TLE-MTS, the memory impairment was mainly associated by subfield-specific hippocampal and inferior frontal cortical damage. In TLE-no, the impairment was associated by mesial-temporal cortical and to a lesser degree hippocampal damage.

Figure 1

(a) Upper panel: hippocampal subfield parcellation scheme. Please see text for details of the parcellation protocol. Lower panel, section of the hippocampus from which subfield volumes are calculated from above (top) and below (bottom). The hippocampal head is oriented toward the bottom of the figure. Red, entorhinal cortex; green, subiculum; blue, CA1; yellow, CA1‐2 transition; maroon, CA3 and dentate gyrus. (b) Cortical regions commonly involved in episodic verbal memory processing: FUSI, fusiform gyrus; POB, pars orbitalis; POP, pars opercularis; PT, pars triangularis (PT); CMF, caudal middle frontal; RMF, rostral middle frontal; SFG, superior frontal gyrus; PRE, precuneus; SPL, lobulus parietalis superior; IPL; lobulus parietalis inferior; SM, supramarginal gyrus. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 2

Standardized auditory memory subscores from Wechsler Memory Scale III. AIMrecall, auditory immediate memory tested by recall; ADMrecall, auditory delayed memory tested by recall; ADMrecog, auditory delayed memory tested by recognition. (a) Memory scores in the three study groups. Yellow, controls; orange; TLE with normal MRI; red, TLE with hippocampal sclerosis. Asterisks indicate scores significantly different from the control group (P < 0.05). (b) Memory scores in TLE with right‐ and left‐sided focus. Dark blue, left TLE‐MTS; bright blue, right TLE‐MTS; orange, left TLE‐no; yellow, right TLE‐no. There were also no significant differences in the TLE subgroups (Mann–Whitney tests with Holm's test to correct for multiple comparisons). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 3

(a) Mean and standard deviation of hippocampal subfield volumes corrected for intracranial head size (please see text for correction formula). Yellow, controls; orange; TLE with normal MRI; red, TLE with hippocampal sclerosis. Asterisks indicate scores that are significantly different from the control group (P < 0.05). (b) Thickness of the cortical regions of interest (mean and standard deviation of the sum of both sides) in millimeters. PARA, parahippocampal gyrus; FUSI, fusiform gyrus; POB, pars orbitalis; POP, pars opercularis; PT, pars triangularis (PT); CMF, caudal middle frontal; RMF, rostral middle frontal; SFG, superior frontal gyrus; PRE, precuneus; SPL, lobulus parietalis superior; IPL; lobulus parietalis inferior; SM, supramarginal gyrus. Yellow, controls; orange; TLE with normal MRI; red, TLE with hippocampal sclerosis. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 4

Scatter plots of subfield volumes and cortical ROI thickness versus WMS‐III scores (without accounting for years of education). Blue squares, controls; red squares, TLE‐MTS; yellow squares, TLE‐no; recall AIMrecall, auditory immediate recall; ADMrecall, auditory delayed recall; ADMrecog, auditory delayed recognition; FUSI, fusiform gyrus; POP, pars opercularis; PT, pars triangularis; CA3&DG, CA3 and dentate gyrus. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]