Disrupted White Matter Integrity and Structural Brain Networks in Temporal Lobe Epilepsy With and Without Interictal Psychosis

Abstract

Background: Despite the importance of psychosis as a comorbidity of temporal lobe epilepsy (TLE), the underlying neural mechanisms are still unclear. We aimed to investigate abnormalities specific to psychosis in TLE, using diffusion MRI parameters and graph-theoretical network analysis. Material and Methods: We recruited 49 patients with TLE (20 with and 29 without interictal schizophrenia-like psychosis) and 42 age-/gender-matched healthy controls. We performed 3-tesla MRI scans including 3D T1-weighted imaging and diffusion tensor imaging in all participants. Among the three groups, fractional anisotropy (FA), mean diffusivity (MD), and global network metrics were compared by analyses of covariance. Regional connectivity strength was compared by network-based statistics. Results: Compared to controls, TLE patients showed significant temporal and extra-temporal changes in FA, and MD, which were more severe and widespread in patients with than without psychosis. We observed distinct differences between TLE patients with and without psychosis in the anterior thalamic radiation (ATR), inferior fronto-occipital fasciculus (IFOF), and inferior longitudinal fasciculus (ILF). Similarly, for network metrics, global, and local efficiency and increased path length were significantly reduced in TLE patients compared to controls, but with more severe changes in TLE with psychosis than without psychosis. Network-based statistics detected significant differences between TLE with and without psychosis mainly involving the left limbic and prefrontal areas. Conclusion: TLE patients with interictal schizophrenia-like psychosis showed more widespread and severe white matter impairment, involving the ATR, IFOF and ILF, as well as disrupted network connectivity, particularly in the left limbic and prefrontal cortex, than patients without psychosis.

Upper cerebellar glucose hypermetabolism in patients with temporal lobe epilepsy and interictal psychosis

“…In addition to these functional studies, most structural neuroimaging studies reported cerebral abnormalities in patients with epilepsy of psychosis 8–12 ; we observed no significant difference in the cerebrum between the present TLE‐P and TLE‐N groups. This unexpected discrepancy might be caused by the small sample size in this study.…”

“…The clinical and imaging data were extracted from our previous study on brain structural networks in 20 patients with TLE with psychosis (TLE-P) and 29 patients with TLE without psychosis (TLE-N). 12 The inclusion and exclusion criteria were described in that paper, and in brief, the diagnosis of TLE was based on the presence of focal seizures consistent with TLE and focal epileptiform discharges in the temporal areas in scalp electroencephalography. Interictal schizophrenia-like psychosis was diagnosed based on the Diagnostic and Statistical Manual of Mental Disorders, fourth edition criteria.…”

“…8 More recently, bilateral hippocampal tail atrophy, 9 abnormal brain aging, 10 and structural network abnormalities were observed in studies of epilepsy. 11,12 In contrast to structural MRI studies, functional imaging studies on psychosis with epilepsy are still limited, although there are a few perfusion single-photon emission computed tomography (SPECT) studies. 13,14 18 F-fluorodeoxyglucose positron emission tomography ( 18 F-FDG PET) is a traditional and still useful imaging modality for epilepsy, as it allows measurements of the brain's regional glucose metabolisms with higher resolution than SPECT.…”

Neurobiological mechanisms of psychosis in epilepsy: Findings from neuroimaging studies

“…Both TLE-P and TLE-NonP showed significant volume reduction in the ipsilateral temporal and other brain areas, but there was no significant direct difference between them [Cited from Sone et al ( 25 )]. (B) Significant reduction in fractional anisotropy (FA) within the white matter tracts in TLE-P, derived from diffusion MRI [Cited from Sone et al ( 40 )]. (C) Disrupted brain white matter networks in TLE-P and TLE-NonP, derived from diffusion MRI [Cited from Sone et al ( 40 )].…”

Epilepsy and psychotic symptoms

“…Se observan diferencias claras en los pacientes con epilepsia del lóbulo temporal y psicosis a nivel de la radiación talámica anterior, el fascículo fronto-occipital inferior y el fascículo longitudinal inferior. Las estadísticas basadas en imágenes funcionales de las redes neuronales han detectado diferencias significativas a nivel de las áreas límbicas y prefrontales izquierdas en personas con epilepsia del lóbulo temporal que se complicaron con un cuadro psicótico y aquellas personas que no lo hicieron (13) .…”