Preeminence of extrahippocampal structures in the generation of mesial temporal seizures: Evidence from human depth electrode recordings

Purpose: To examine the intralimbic localization and morphology of mesial temporal seizure onsets and to correlate the findings with patterns of initial seizure spread and the presence or absence of clinical manifestations. Methods: Eighteen patients with temporal lobe epilepsy were investigated with intracranial depth electrodes implanted in the amygdala (AM), anterior hippocampus (HP), and parahippocampal gyrus (PH). Focal and regional ictal-onset morphologies were classified as rhythmic limbic spiking <2 Hz (RLS), spike-and-wave activity >2 Hz (S/W), rhythmic polyspike activity >13 Hz (RPS), and rhythmic sharp activity <13 Hz (RS). Results: Onset morphologies in 389 total seizures (260 regional + 129 focal) were 50% RPS, 35% RS, 11% RLS, and 4% S/W. Focal AM or HP onsets (30% and 58% of focal onsets, respectively) were more likely to show RLS, whereas RPS was more common in regional onsets. Most patients showed two or more different morphologies and focal onsets at more than one ipsilateral limbic site. Seizure propagation and clinical manifestations were significantly more common with AM or PH onsets (both 67% clinical seizures): only 23% of focal HP onsets resulted in clinical seizures. Conclusions: (a) There is substantial inter- and intrapatient variability in the morphology and localization of mesial temporal seizure onsets, which suggests that the epileptogenic temporolimbic system may be conceptualized as a dynamic network containing a multiplicity of potential ictal generators: (b) Seizures beginning in the AM or PH are more likely to propagate and dive rise to clinical manifestations than are focal-onset HP seizures, which suggests that inhibitory circuits within the HP may function to prevent seizure spread.