Neural basis of episodic memory in the intermediate term after medial temporal lobe resection

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OBJECTIVE

How the brain supports intermediate-term preservation of memory in patients who have undergone unilateral medial temporal lobe resection (MTLR) has not yet been demonstrated. To understand the neural basis of episodic memory in the intermediate term after surgery for temporal lobe epilepsy (TLE), the authors investigated the relationship between the activation of the hippocampus (HIP) during successful memory encoding and individual memory capacity in patients who had undergone MTLR. They also compared hippocampal activation with other parameters, including structural volumes of the HIP, duration of illness, and age at seizure onset.

METHODS

Thirty-five adult patients who had undergone unilateral MTLR at least 1 year before recruiting and who had a favorable seizure outcome were enrolled (17 left MTLR, 18 right MTLR; mean follow-up 6.31 ± 2.72 years). All patients underwent a standardized neuropsychological examination of memory function and functional MRI scanning with a memory-encoding paradigm of words and figures. Activations of the HIP during successful memory encoding were calculated and compared with standard neuropsychological memory scores, hippocampal volumes, and other clinical variables.

RESULTS

Greater activation in the HIP contralateral to the side of the resection was related to higher postoperative memory scores and greater postoperative memory improvement than the preoperative baseline in both patient groups. Specifically, postoperative verbal memory performance was positively correlated with contralateral right hippocampal activation during word encoding in the left-sided surgery group. In contrast, postoperative visual memory performance was positively correlated with contralateral left hippocampal activation during figure encoding in the right-sided surgery group. Activation of the ipsilateral remnant HIP was not correlated with any memory scores or volumes of the HIP; however, it had a negative correlation with the seizure-onset age and positive correlation with the duration of illness in both patient groups.

CONCLUSIONS

For the first time, a neural basis that supports effective intermediate-term episodic memory after unilateral MTLR has been characterized. The results provide evidence that engagement of the HIP contralateral rather than ipsilateral to the side of resection is responsible for effective memory function in the intermediate term (> 1 year) after surgery in patients who have undergone left MTLR and right MTLR. Engagement of the material-specific contralesional HIP, verbal memory in the left-sided surgery group, and visual memory in the right-sided surgery group were observed.

ABBREVIATIONS AFNI = Analysis of Functional NeuroImages; EPI = echo-planar imaging; fMRI = functional MRI; FSIQ = full-scale IQ; HIP = hippocampus; KAVLT = Korean version of the Rey Auditory Verbal Learning Test; KCFT = Korean version of the Rey Complex Figure Test; KWAIS = Korean Wechsler Adult Intelligence Scale; LMTLR = left MTLR; MNI = Montreal Neurological Institute; MQ = memory quotient; MTL = medial temporal lobe; MTLR = MTL resection; PIQ = performance IQ; RMTLR = right MTLR; ROI = region of interest; TLE = temporal lobe epilepsy; TR = repetition time; VIQ = verbal IQ.

Article Information

Correspondence Chun Kee Chung: Seoul National University Hospital, Seoul, South Korea. chungc@snu.ac.kr.

INCLUDE WHEN CITING Published online October 26, 2018; DOI: 10.3171/2018.5.JNS18199.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Examples of manually drawn hippocampal ROIs. L = left; R = right. Figure is available in color online only.

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    Examples of activated voxels in the hippocampal ROIs during memory encoding (correct > incorrect). A: Hippocampal activation during word encoding in two cases, one where the patient had undergone LMTLR (LMTLR#03) and the other where the patient had undergone RMTLR (RMTLR#06). B: Hippocampal activation during figure encoding in two cases, one where the patient had undergone LMTLR (LMTLR#12) and the other where the patient had undergone RMTLR (RMTLR#18). Survived voxels at p < 0.05 (uncorrected) are provided for display purposes only (blue box). Figure is available in color online only.

  • View in gallery

    Relationships of left (A) and right (B) hippocampal activations to clinical variables.

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