Abstract
Direct recordings from the human brain have historically involved epilepsy patients undergoing invasive electroencephalography (iEEG) for surgery. However, these measurements are temporally limited and affected by clinical variables. The RNS System (NeuroPace, Inc.) is a chronic, closed-loop electrographic seizure detection and stimulation system. When adapted by investigators for research, it facilitates cognitive testing in a controlled ambulatory setting, with measurements collected over months to years. We utilized an associative learning paradigm in 5 patients with traditional iEEG and 3 patients with chronic iEEG, and found increased hippocampal gamma (60–100 Hz) sustained at 1.3–1.5 seconds during encoding in successful versus failed trials in surgical patients, with similar results in our RNS System patients (1.4–1.6 seconds). Our findings replicate other studies demonstrating that sustained hippocampal gamma supports encoding. Importantly, we have validated the RNS System to make sensitive measurements of hippocampal dynamics during cognitive tasks in a chronic ambulatory research setting.
Highlights
The hippocampus is critical to forming novel associations between previously unrelated items[1,2,3], binding information across time and space[4]
During signal analysis, we found that we discarded less intracranial EEG (iEEG) data due to environmental noise or epileptiform activity in our RNS System patients compared to our surgical patients
During behavioral testing with our RNS System patients, we observed that our three RNS System patients were generally able to engage in memory testing for longer periods of time compared to our surgical patients
Summary
The hippocampus is critical to forming novel associations between previously unrelated items[1,2,3], binding information across time and space[4]. Traditional iEEG is limited to memory investigations studied across short timescales, as well as by subject-related limitations of pain, seizures, and distraction inherent to the clinical scenario. Some of the experimental constraints of traditional surgical iEEG research include: (1) Suboptimal patient participation due to clinical factors including seizures, pain, medications, fatigue, and disrupted sleep-wake cycles, (2) Lack of control over the hospital environment which may cause distraction during cognitive testing[9], (3) 60 Hz line noise generated from nearby equipment We aimed to replicate previous work on hippocampal physiology predictive of successful encoding using an associative memory paradigm in a traditional surgical iEEG group and extend these investigations to a chronic ambulatory iEEG (RNS System, NeuroPace, Inc.) population. We selected a face-profession association task, a memory task which has produced robust fMRI activation in bilateral hippocampi[13], and is similar to a face-name association task which has been demonstrated to be sensitive to memory decline in a clinical population[14] (Fig. 1A)
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