Temporal lobe surgery in childhood and neuroanatomical predictors of long-term declarative memory outcome.
The temporal lobes play a prominent role in declarative memory function, including episodic memory (memory for events) and semantic memory (memory for facts and concepts). Surgical resection for medication-resistant and well-localized temporal lobe epilepsy has good prognosis for seizure freedom, but is linked to memory difficulties in adults, especially when the removal is on the left side. Children may benefit most from surgery, because brain plasticity may facilitate post-surgical reorganization, and seizure cessation may promote cognitive development. However, the long-term impact of this intervention in children is not known. We examined memory function in 53 children (25 males, 28 females) who were evaluated for epilepsy surgery: 42 underwent unilateral temporal lobe resections (25 left, 17 right, mean age at surgery 13.8 years), 11 were treated only pharmacologically. Average follow-up was 9 years (range 5-15). Post-surgical change in visual and verbal episodic memory, and semantic memory at follow-up were examined. Pre- and post-surgical T1-weighted MRI brain scans were analysed to extract hippocampal and resection volumes, and evaluate post-surgical temporal lobe integrity. Language lateralization indices were derived from functional magnetic resonance imaging. There were no significant pre- to postoperative decrements in memory associated with surgery. In contrast, gains in verbal episodic memory were seen after right temporal lobe surgery, and visual episodic memory improved after left temporal lobe surgery, indicating a functional release in the unoperated temporal lobe after seizure reduction or cessation. Pre- to post-surgical change in memory function was not associated with any indices of brain structure derived from MRI. However, better verbal memory at follow-up was linked to greater post-surgical residual hippocampal volumes, most robustly in left surgical participants. Better semantic memory at follow-up was associated with smaller resection volumes and greater temporal pole integrity after left temporal surgery. Results were independent of post-surgical intellectual function and language lateralization. Our findings indicate post-surgical, hemisphere-dependent material-specific improvement in memory functions in the intact temporal lobe. However, outcome was linked to the anatomical integrity of the temporal lobe memory system, indicating that compensatory mechanisms are constrained by the amount of tissue which remains in the operated temporal lobe. Careful tailoring of resections for children undergoing epilepsy surgery may enhance long-term memory outcome.
1 Cognitive Neuroscience and Neuropsychiatry Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, 30 Guilford Street, London, WC1N 1EH, UK 2 Great Ormond Street Hospital NHS Trust, Great Ormond Street, WC1N 3JH, UK.
Caroline
C
Skirrow
2 Great Ormond Street Hospital NHS Trust, Great Ormond Street, WC1N 3JH, UK 3 Clinical Neurosciences Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, 30 Guilford Street, London, WC1N 1EH, UK.
J Helen
JH
Cross
1 Cognitive Neuroscience and Neuropsychiatry Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, 30 Guilford Street, London, WC1N 1EH, UK 2 Great Ormond Street Hospital NHS Trust, Great Ormond Street, WC1N 3JH, UK.
Sue
S
Harrison
4 Cognition and Brain Sciences Unit, 15 Chaucer Road, Cambridge, CB2 7EF, UK.
Francesca
F
Cormack
2 Great Ormond Street Hospital NHS Trust, Great Ormond Street, WC1N 3JH, UK.
William
W
Harkness
1 Cognitive Neuroscience and Neuropsychiatry Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, 30 Guilford Street, London, WC1N 1EH, UK 2 Great Ormond Street Hospital NHS Trust, Great Ormond Street, WC1N 3JH, UK.
Rosie
R
Coleman
1 Cognitive Neuroscience and Neuropsychiatry Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, 30 Guilford Street, London, WC1N 1EH, UK 5 Abteilung für Psychiatrie und Psychotherapie, Universitätsklinik Freiburg, Hugstetter Strasse 55, 29106 Freiburg, Germany.
Ellen
E
Meierotto
1 Cognitive Neuroscience and Neuropsychiatry Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, 30 Guilford Street, London, WC1N 1EH, UK.
Johanna
J
Gaiottino
1 Cognitive Neuroscience and Neuropsychiatry Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, 30 Guilford Street, London, WC1N 1EH, UK 2 Great Ormond Street Hospital NHS Trust, Great Ormond Street, WC1N 3JH, UK.
Faraneh
F
Vargha-Khadem
1 Cognitive Neuroscience and Neuropsychiatry Section, Developmental Neurosciences Programme, Institute of Child Health, University College London, 30 Guilford Street, London, WC1N 1EH, UK 2 Great Ormond Street Hospital NHS Trust, Great Ormond Street, WC1N 3JH, UK T.Baldeweg@ucl.ac.uk.
Torsten
T
Baldeweg
D000293:Adolescent; D038481:Anterior Temporal Lobectomy / Q000379:methods*; D004827:Epilepsy / Q000150:complications / Q000473:pathology* / Q000601:surgery*; D005260:Female; D007839:Functional Laterality; D006801:Humans; D008137:Longitudinal Studies; D008279:Magnetic Resonance Imaging; D008297:Male; D008569:Memory Disorders / Q000209:etiology / Q000601:surgery*; D061212:Memory, Episodic; D009483:Neuropsychological Tests; D010775:Photic Stimulation; D011237:Predictive Value of Tests; D012189:Retrospective Studies; D012660:Semantics; D013702:Temporal Lobe / Q000473:pathology*; D016896:Treatment Outcome; D014706:Verbal Learning; D055815:Young Adult
children; drug-resistant epilepsy; epilepsy surgery; hippocampus; memory