Verbal memory network mapping in individual patients predicts postoperative functional impairments

Hum Brain Mapp. 2024 May;45(7):e26691. doi: 10.1002/hbm.26691.

Abstract

Verbal memory decline is a significant concern following temporal lobe surgeries in patients with epilepsy, emphasizing the need for precision presurgical verbal memory mapping to optimize functional outcomes. However, the inter-individual variability in functional networks and brain function-structural dissociations pose challenges when relying solely on group-level atlases or anatomical landmarks for surgical guidance. Here, we aimed to develop and validate a personalized functional mapping technique for verbal memory using precision resting-state functional MRI (rs-fMRI) and neurosurgery. A total of 38 patients with refractory epilepsy scheduled for surgical interventions were enrolled and 28 patients were analyzed in the study. Baseline 30-min rs-fMRI scanning, verbal memory and language assessments were collected for each patient before surgery. Personalized verbal memory networks (PVMN) were delineated based on preoperative rs-fMRI data for each patient. The accuracy of PVMN was assessed by comparing post-operative functional impairments and the overlapping extent between PVMN and surgical lesions. A total of 14 out of 28 patients experienced clinically meaningful declines in verbal memory after surgery. The personalized network and the group-level atlas exhibited 100% and 75.0% accuracy in predicting postoperative verbal memory declines, respectively. Moreover, six patients with extra-temporal lesions that overlapped with PVMN showed selective impairments in verbal memory. Furthermore, the lesioned ratio of the personalized network rather than the group-level atlas was significantly correlated with postoperative declines in verbal memory (personalized networks: r = -0.39, p = .038; group-level atlas: r = -0.19, p = .332). In conclusion, our personalized functional mapping technique, using precision rs-fMRI, offers valuable insights into individual variability in the verbal memory network and holds promise in precision verbal memory network mapping in individuals.

Keywords: epilepsy; fMRI; individual difference; presurgical planning; verbal memory mapping.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Adult
  • Brain Mapping* / methods
  • Drug Resistant Epilepsy / diagnostic imaging
  • Drug Resistant Epilepsy / physiopathology
  • Drug Resistant Epilepsy / surgery
  • Epilepsy, Temporal Lobe / diagnostic imaging
  • Epilepsy, Temporal Lobe / physiopathology
  • Epilepsy, Temporal Lobe / surgery
  • Female
  • Humans
  • Magnetic Resonance Imaging*
  • Male
  • Memory Disorders / diagnostic imaging
  • Memory Disorders / etiology
  • Memory Disorders / physiopathology
  • Middle Aged
  • Nerve Net / diagnostic imaging
  • Nerve Net / physiopathology
  • Nerve Net / surgery
  • Neurosurgical Procedures
  • Postoperative Complications / diagnostic imaging
  • Verbal Learning / physiology
  • Young Adult