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. 2018 Jan:78:187-193.
doi: 10.1016/j.yebeh.2017.09.012. Epub 2017 Nov 8.

Decreased neurite density within frontostriatal networks is associated with executive dysfunction in temporal lobe epilepsy

Anny Reyes  1 , Vedang S Uttarwar  2 , Yu-Hsuan A Chang  2 , Akshara R Balachandra  2 , Chris J Pung  2 , Donald J Hagler Jr  2 , Briana M Paul  3 , Carrie R McDonald  4
Affiliations

Decreased neurite density within frontostriatal networks is associated with executive dysfunction in temporal lobe epilepsy

Anny Reyes et al. Epilepsy Behav. 2018 Jan.

Abstract

Objective: Executive dysfunction is observed in a sizable number of patients with refractory temporal lobe epilepsy (TLE). The frontostriatal network has been proposed to play a significant role in executive functioning, however, because of the complex architecture of these tracts, it is difficult to generate measures of fiber tract microstructure using standard diffusion tensor imaging. To examine the association between frontostriatal network compromise and executive dysfunction in TLE, we applied an advanced, multishell diffusion model, restriction spectrum imaging (RSI), that isolates measures of intraaxonal diffusion and may provide better estimates of fiber tract compromise in TLE.

Methods: Restriction spectrum imaging scans were obtained from 32 patients with TLE [16 right TLE (RTLE); 16 left TLE (LTLE)] and 24 healthy controls (HC). An RSI-derived measure of intraaxonal anisotropic diffusion (neurite density; ND) was calculated for the inferior frontostriatal tract (IFS) and superior frontostriatal tract (SFS) and compared between patients with TLE and HC. Spearman correlations were performed to evaluate the relationships between ND of each tract and verbal (i.e., D-KEFS Category Switching Accuracy and Color-Word Interference Inhibition/Switching) and visuomotor (Trail Making Test) set-shifting performances in patients with TLE.

Results: Patients with TLE demonstrated reductions in ND of the left and right IFS, but not SFS, compared with HC. Reduction in ND of left and right IFS was associated with poorer performance on verbal set-shifting in TLE. Increases in extracellular diffusion (isotropic hindered; IH) were not associated with executive dysfunction in the patient group.

Significance: Restriction spectrum imaging-derived ND revealed microstructural changes within the IFS in patients with TLE, which was associated with poorer executive functioning. This suggests that axonal/myelin loss to fiber networks connecting the striatum to the inferior frontal cortex is likely contributing to executive dysfunction in TLE.

Keywords: Advanced diffusion; Demyelination; Executive function; Inhibition; Set-shifting.

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Conflict of interest statement

Disclosure of Conflicts of Interest/Ethical Publication Statement

We confirm that we have read the Journal’s position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. None of the authors have any conflicts of interest to disclose.

Figures

Figure 1
Figure 1
A) Sagittal rendering of the IFS and SFS derived from a probabilistic diffusion tensor atlas (i.e., AtlasTrack) projected onto a T1-weighted image. IFS: inferior frontostriatal tract; SFS: superior frontostriatal tract. The corpus callosum is portrayed in gray in the background in order to provide additional spatial information.
Figure 2
Figure 2
Voxel-based group comparisons between patients with TLE and healthy controls using ANTS registration according to procedures described elsewhere [17]. Areas of red-yellow represent decreased ND within the vicinity of the frontostriatal networks in patients compared to controls. Sagittal, axial, and coronal views are represented respectively. All images are clustered and FDR-corrected at q <0.05.
Figure 3
Figure 3
Mean neurite density (ND) in patients with TLE and HCs for the right and left inferior frontostriatal (IFS) and superior frontostriatal (SFS) tracts. Asterisk indicates p < 0.025. Error bars represent standard error.
Figure 4
Figure 4
Relationship between neurite density (ND) of the right (A) and left (B) inferior frontostriatal tract (IFS) and Color Word Inhibition/Switching performance in patients with TLE.
See this image and copyright information in PMC

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