Bilateral limbic diffusion abnormalities in unilateral temporal lobe epilepsy

Abstract

Diffusion tensor magnetic resonance imaging can acquire quantitative information on the microstructural integrity of white matter structures and depict brain connectivity in vivo based on the behavior of water diffusion. Diffusion tensor imaging-derived tractography has been used for virtual dissection of the fornix and cingulum in healthy subjects, but not in patients with temporal lobe epilepsy (TLE). Eight patients with medically intractable TLE and unilateral mesial temporal sclerosis and nine healthy control subjects were imaged using diffusion tensor imaging. Fiber tracking was performed to delineate the fornix and cingulum, which were quantitatively analyzed. Bilateral symmetrical reduction in fractional anisotropy was observed in the fornix of patients with TLE, together with an increase in water mobility perpendicular to the axis of the fibers. The findings in the cingulum are similar to those of the fornix with the exception of significantly increased bulk diffusivity in the latter. We observed strikingly symmetrical bilateral abnormalities of axonal integrity in the fornix and cingulum in a series of patients with unilateral mesial temporal sclerosis. Our findings suggest that TLE with unilateral mesial temporal sclerosis is associated with bilateral limbic system pathology.

In VivoDiffusion Tensor Imaging and Histopathology of the Fimbria-Fornix in Temporal Lobe Epilepsy

“…It must be noted, however, that the fimbriafornix is a bidirectional pathway, including afferents to the mesial temporal region from a variety of structures including the septum and that other sources of axonal degeneration are also possible. Our previous DTI tractography studies showed bilateral water diffusion abnormalities of the fimbria-fornix in TLEϩuMTS patients (Concha et al, 2005b(Concha et al, , 2009, in excellent agreement with a recent postmortem study confirming decreased axonal density of the fimbria-fornix bilaterally in four TLEϩuMTS patients (Ozdogmus et al, 2009) As ipsilateral but not contralateral fimbria-fornix abnormalities would be expected if the reduced fimbria-fornix integrity was solely secondary to degeneration of mesial temporal efferent fibers, the bilateral findings suggest that degeneration of efferent fibers may not be the only mechanism responsible for the observed changes. Ozdogmus et al reported that myelinated axons greatly outnumbered unmyelinated axons in the fimbriafornix of both TLE patients and normal controls (Ozdogmus et al, 2009), while we found a near complete absence of unmyelinated axons in TLEϩuMTS and TLEϪMTS patients.…”

“…in all voxels in the brain having a fractional anisotropy (FA) threshold Ͼ0.3, and was terminated if the propagating streamlines entered voxels of low anisotropy (FA Ͻ 0.3) or deviated by Ͼ70°. The fimbria-fornix was virtually dissected by the extraction of those tracts that intersected two manually placed regions of interest (Concha et al, 2005b). Fractional anisotropy was averaged for the voxels lying between the level of the mammillary bodies and the fusion of the crura of the fornices, exactly as we have performed in our previous DTI studies of TLE (Concha et al, 2005a(Concha et al, ,b, 2009).…”

“…While mesial temporal sclerosis (MTS) is the most commonly observed pathology in TLE, DTI studies have shown white matter abnormalities in several bundles not necessarily limited to the temporal lobe nor the hemisphere ipsilateral to seizure focus (Arfanakis et al, 2002;Gross et al, 2006;Rodrigo et al, 2007;Focke et al, 2008;McDonald et al, 2008;Nilsson et al, 2008;Yogarajah et al, 2008;Schoene-Bake et al, 2009). We have previously demonstrated that TLE patients with unilateral MTS (TLEϩuMTS) have DTI abnormalities of the fimbria-fornix (Concha et al, 2005b) that are not observed in TLE patients who do not have MTS (TLEϪMTS) (Concha et al, 2009). As medically intractable TLEϩuMTS and TLEϪMTS patients routinely undergo surgical resection of the temporal lobe (including a portion of the fimbria-fornix) in the management of their condition, this setting provides a unique opportunity to confirm the disruption of myelin/membrane integrity of the fimbria-fornix in patients with TLEϩuMTS (as predicted by DTI) and to perform the first correlative study of DTI acquired in vivo with subsequent histopathology of a major white matter structure in humans.…”

Interrupção das fibras brancas nos acessos cirúrgicos ao corno temporal do ventrículo lateral: estudo anatômico

“…Nas últimas décadas, o grande desenvolvimento tecnológico das técnicas de imagem (Basser et al, 1994;Cercignani et al, 2001;Concha et al;Jellison et al,2004;Ciccarelli et al, 2005;Voegts et al, 2006;Cho et al;Kubicki et al, 2007) e monitorização da função cerebral, in vivo, (Clarck et al,2003;Berman et al, 2004Berman et al, , 2007Kamada et al, 2005) evidenciou a necessidade de um substrato anatômico para corroborar seus achados. Tal fato, revitalizou o estudo das dissecções das fibras brancas cerebrais e resgatou a história da neuroanatomia (Ture et al, 1997(Ture et al, ,2000.…”

“…As informações das alterações quantitativa e qualitativa da difusão de moléculas de água tem influenciado a compreensão sobre a conectividade cerebral e permitido inferir sobre a fisiopatologia e possíveis intervenções terapêuticas em diversas patologias como epilepsia (Concha et al,2005), doenças cerebrovasculares (Voegts et al, 2006;Cho et al,2007), esclerose múltipla (Cercignani et al, 2001;Ciccarelli et al, 2005), esclerose lateral amiotrófica (Ciccarelli et al, 2006) e distúrbios neuropsiquiátricos (Kubicki et al, 2007). A aplicação da tractografia também tem influenciado a neurocirurgia, principalmente no que concerne o planejamento e estratégias de ressecções cirúrgicas em lesões intrinsicas cerebrais.…”