The significance of parahippocampal high gamma activity for memory preservation in surgical treatment of atypical temporal lobe epilepsy

Abstract

SUMMARYObjective: Resective surgery for mesial temporal lobe epilepsy (MTLE) with a correspondent lesion has been established as an effective and safe procedure. Surgery for temporal lobe epilepsies with bilateral hippocampal sclerosis or without correspondent lesions, however, carries a higher risk of devastating memory decline, underscoring the importance of establishing the memory-dominant side preoperatively and adopting the most appropriate procedure. In this study, we focused on high gamma activities (HGAs) in the parahippocampal gyri and investigated the relationship between memory-related HGAs and memory outcomes after hippocampal transection (HT), a hippocampal counterpart to neocortical multiple subpial transection. The transient nature of memory worsening after HT provided us with a rare opportunity to compare HGAs and clinical outcomes without risking permanent memory disorders. Methods: We recorded electrocorticography from parahippocampal gyri of 18 patients with temporal lobe epilepsy while they executed picture naming and recognition tasks. Memory-related HGA was quantified by calculating differences in power amplification of electrocorticography signals in a high gamma range (60-120 Hz) between the two tasks. We compared memory-related HGAs from correctly recognized and rejected trials (hit-HGA and reject-HGA). Using hit-HGA, we determined HGA-dominant sides and compared them with memory outcomes after HT performed on seven patients. Results: We observed memory-related HGA mainly between 500 and 600 msec poststimulus. Hit-HGA was significantly higher than reject-HGA. Three patients who had surgery on the HGA-dominant side experienced transient memory worsening postoperatively. The postoperative memory functions of the other four patients remained unchanged. Significance: Parahippocampal HGA was indicated to reflect different memory processes and be compatible with the outcomes of HT, suggesting that HGA could provide predictive information on whether the mesial temporal lobe can be resected without causing memory worsening. This preliminary study suggests a refined surgical strategy for atypical MTLE based on reliable memory lateralization.

Three- and four-dimensional mapping of speech and language in patients with epilepsy

“…This stream is not included in the dual stream model of speech processing (Hickok and Poeppel, 2007; Rauschecker and Scott, 2009). Yet, further discussion is worthwhile, particularly because verbal memory decline was induced by surgical damage of the left parahippocampal gyrus showing high-gamma augmentation during covert picture naming followed by successful recall (Kunii et al , 2014). Our ECoG observation of left-hemispheric dominance supports the hypothesis that high-gamma augmentation in this stream would reflect episodic memory encoding and/or memory retrieval in the verbal domain.…”

The human hippocampus contributes to both the recollection and familiarity components of recognition memory

“…In this case, the magnitude of the hippocampal HFA increase for successful recognition could be used to anticipate the risk of memory decline with resection (for support of such application within the parahippocampal gyrus, see ref. 50).…”

Long‐term outcome and neuroradiologic changes after multiple hippocampal transection combined with multiple subpial transection or lesionectomy for temporal lobe epilepsy

“…As a matter of course, residual epileptogenic activity in the MHT‐treated hippocampus/parahippocampal gyrus was also suggested in cases with hippocampal sclerosis, since the effect of MHT on a sclerotic hippocampus, that is, a hippocampus with an already disorganized structure, is unknown. This may explain the lower rate of class I outcomes at 3 years and later in the hippocampal sclerosis group than in the normal hippocampus group, and also indicates that, for patients with hippocampal sclerosis, resective surgery would be the choice in terms of seizure control unless memory preservation matters …”

“…Candidates were selected according to the above‐mentioned indication from patients who underwent our routine preoperative workup for their drug‐resistant epilepsy between September 2003 and June 2007 in the Department of Neurosurgery at the University of Tokyo Hospital. The workup consisted of video–electroencephalography (EEG) monitoring, MRI, ethyl cysteinate dimer–single‐photon emission computed tomography (SPECT), FDG‐PET, and neurocognitive examinations including the Wechsler Memory Scale‐Revised (WMS‐R), the Wechsler Adult Intelligence Scale‐III (WAIS‐III), and Miyake's Paired Word Recall (MPWR) . When information was needed for further lateralization or localization of the brain area to be treated, intracranial electrodes were implanted bilaterally .…”