The relationship between neuropsychological functioning and FDG-PET hypometabolism in intractable mesial temporal lobe epilepsy

We examined the relationship between baseline neuropsychological functioning and 18-fluorodeoxyglucose positron emission tomography (FDG-PET) in intractable mesial temporal lobe epilepsy (MTLE). We hypothesized relationships between dominant temporal lobe hypometabolism and verbal memory and between nondominant temporal lobe hypometabolism and nonverbal memory in line with the lateralized material-specific model of memory deficits in MTLE. We also hypothesized an association between performance on frontal lobe neuropsychological tests and prefrontal hypometabolism. Thirty-two patients who had undergone temporal lobectomy for treatment of MTLE and who completed both presurgical FDG-PET and comprehensive neuropsychological investigations with widely used standardized measures were included. Age-adjusted composite measures were calculated for verbal memory, nonverbal memory, relative material-specific memory, IQ, executive function, attention/working memory, and psychomotor speed. Fluorodeoxyglucose positron emission tomography was analyzed with statistical parametric mapping (SPM) to identify hypometabolism relative to healthy controls. Pearson's correlation was used to determine the relationship between regions of hypometabolism and neuropsychological functioning. Dominant temporal lobe hypometabolism was associated with relatively inferior verbal memory, while nondominant temporal lobe hypometabolism was associated with inferior nonverbal memory. No relationship was found between performance on any frontal lobe measures and prefrontal hypometabolism. Statistical parametric mapping-quantified lateralized temporal lobe hypometabolism correlates with material-specific episodic memory impairment in MTLE. In contrast, prefrontal hypometabolism is not associated with performance on frontal lobe measures. We suggest that this is because frontal lobe neuropsychology tests may not be good measures of isolated frontal lobe functioning.

[1]  J. Alvarez,et al.  Executive Function and the Frontal Lobes: A Meta-Analytic Review , 2006, Neuropsychology Review.

[2]  J. Mazziotta,et al.  Asymmetric interictal glucose hypometabolism and cognitive performance in epileptic patients. , 1994, Archives of neurology.

[3]  Chris Rorden,et al.  Lesion Mapping of Cognitive Abilities Linked to Intelligence , 2009, Neuron.

[4]  K. Laere,et al.  PET and SPECT in Presurgical Evaluation of Epilepsy , 2008 .

[5]  T. Tombaugh,et al.  Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. , 1999, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[6]  Jeffrey D. Riley,et al.  Caudate atrophy and impaired frontostriatal connections are linked to executive dysfunction in temporal lobe epilepsy , 2011, Epilepsy & Behavior.

[7]  O. Selnes A Compendium of Neuropsychological Tests , 1991, Neurology.

[8]  Jack J. Lin,et al.  The neurobiology of cognitive disorders in temporal lobe epilepsy , 2011, Nature Reviews Neurology.

[9]  O. Witte,et al.  Topography of interictal glucose hypometabolism in unilateral mesiotemporal epilepsy , 1996, Neurology.

[10]  T. Hanakawa,et al.  Prefrontal hypofunction in patients with intractable mesial temporal lobe epilepsy , 2006, Neurology.

[11]  G. E. Alexander,et al.  Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. , 1990, Progress in brain research.

[12]  T. Morioka,et al.  Thalamic hypometabolism on 18FDG-positron emission tomography in medial temporal lobe epilepsy , 2007, Neurological research.

[13]  B. Hermann,et al.  Extrahippocampal integrity in temporal lobe epilepsy and cognition: Thalamus and executive functioning , 2010, Epilepsy & Behavior.

[14]  Bruce Hermann,et al.  Neuroanatomical correlates of cognitive phenotypes in temporal lobe epilepsy , 2009, Epilepsy & Behavior.

[15]  Jerome Engel,et al.  Outcome with respect to epileptic seizures. , 1993 .

[16]  K. Byth,et al.  The topography and significance of extratemporal hypometabolism in refractory mesial temporal lobe epilepsy examined by FDG‐PET , 2010, Epilepsia.

[17]  Ron Dumont,et al.  Wechsler Memory Scale–Third Edition , 2008 .

[18]  A P Shimamura,et al.  Verbal and design fluency in patients with frontal lobe lesions , 2001, Journal of the International Neuropsychological Society.

[19]  B. Hermann Neuropsychological Assessment of Patients with Epilepsy , 1992 .

[20]  O W Witte,et al.  Prefrontal asymmetric interictal glucose hypometabolism and cognitive impairment in patients with temporal lobe epilepsy. , 1997, Brain : a journal of neurology.

[21]  G. Demakis,et al.  A meta-analytic review of the sensitivity of the Wisconsin Card Sorting Test to frontal and lateralized frontal brain damage. , 2003, Neuropsychology.

[22]  Massimo Avoli,et al.  Resting state networks in temporal lobe epilepsy , 2013, Epilepsia.

[23]  H. Fukuyama,et al.  Improved cerebral function in mesial temporal lobe epilepsy after subtemporal amygdalohippocampectomy. , 2009, Brain : a journal of neurology.

[24]  B. Milner,et al.  Interhemispheric differences in the localization of psychological processes in man. , 1971, British medical bulletin.

[25]  A. Connelly,et al.  The Relationship Between Quantitative MRI and Neuropsychological Functioning in Temporal Lobe Epilepsy , 1998, Epilepsia.

[26]  J R Moeller,et al.  Cerebral metabolic topography in unilateral temporal lobe epilepsy , 1995, Neurology.

[27]  R. Pyzalski,et al.  Memory relationships between MRI volumes and resting PET metabolism of medial temporal lobe structures , 2004, Epilepsy & Behavior.

[28]  W. Bell,et al.  Surgical treatment of the epilepsies—Second edition , 1994 .

[29]  C. Reynolds,et al.  Wechsler memory scale-revised , 1988 .

[30]  I. M. Harris,et al.  The effects of mesial temporal and cerebellar hypometabolism on learning and memory , 2001, Journal of the International Neuropsychological Society.

[31]  Mark S. Seidenberg,et al.  Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy. , 1997, Archives of neurology.

[32]  Neil Roberts,et al.  Quantitative MRI of the prefrontal cortex and executive function in patients with temporal lobe epilepsy , 2009, Epilepsy & Behavior.

[33]  Robert K. Heaton,et al.  Wisconsin Card Sorting Test Manual – Revised and Expanded , 1993 .

[34]  D. Tulsky,et al.  WAIS-III WMS-III Technical manual , 1977 .

[35]  T. Tombaugh Trail Making Test A and B: normative data stratified by age and education. , 2004, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[36]  M. Fulham,et al.  The cognitive profile of occipital lobe epilepsy and the selective association of left temporal lobe hypometabolism with verbal memory impairment , 2014, Epilepsia.

[37]  T. Morioka,et al.  emission tomography in medial temporal lobe epilepsy , 2007 .

[38]  David C Reutens,et al.  Verbal memory in left temporal lobe epilepsy: Evidence for task‐related localization , 2002, Annals of neurology.

[39]  T. Shallice,et al.  Multiple frontal systems controlling response speed , 2005, Neuropsychologia.

[40]  Fong Chan,et al.  Cognitive phenotypes in temporal lobe epilepsy , 2006, Journal of the International Neuropsychological Society.

[41]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[42]  Jian Chen,et al.  Structural and functional correlates of unilateral mesial temporal lobe spatial memory impairment. , 2008, Brain : a journal of neurology.