Hippocampal Theta-based Alarm Enhances Associative Memory: Human intracranial EEG Study

Poster No:

1060 

Submission Type:

Abstract Submission 

Authors:

Seong Jin Lee1, Chun Kee Chung2

Institutions:

1Seoul National University, Seoul, Korea, Republic of, 2Seoul National University Hospital, Seoul, Korea, Republic of

First Author:

Seong Jin Lee  
Seoul National University
Seoul, Korea, Republic of

Co-Author:

Chun Kee Chung  
Seoul National University Hospital
Seoul, Korea, Republic of

Introduction:

This study focuses on the role of hippocampal theta oscillation in memory formation, particularly in associative memory encoding. We use real-time monitoring of hippocampal activity through intracranial EEG (iEEG) in pharmaco-resistant epilepsy patients with hippocampal depth electrodes. Employing neurofeedback with audio signals, the study aims to investigate the impact of modulating hippocampal theta power in real-time on associative memory performance. The hypothesis is that a decrease in hippocampal theta power during encoding may lead to decreased memory performance, and preventing this decrease could enhance memory performance.

Methods:

This study involved 7 patients with pharmaco-resistant epilepsy who underwent intracranial electrode implantation to identify the seizure onset zone, with all patients having hippocampal depth electrodes inserted. The experimental session included Practice Encoding and Retrieval, Encoding, Distraction, and Retrieval blocks. In the Encoding block, participants faced No alarm, Random alarm, and Theta-based alarm conditions, tasked with encoding 20 word-pairs of Korean nouns in each. Real-time monitoring of the hippocampal target electrode's theta power determined alarm conditions. The Distraction block involved solving 12 math problems, and in the Retrieval block, participants responded to 80 word-pairs (including 60 from Encoding: 20 intact, 20 rearranged, 20 new). The experiment comprised two sessions, varying the order of conditions between sessions. No word-pair was presented more than once.

Results:

This study analyzed band power during a 3-second encoding period, finding significant differences in Theta, Alpha, and Gamma bands between successful and failed memory trials across all conditions (p < 0.05). Notably, significant differences were observed only in the No alarm condition, emphasizing the importance of hippocampal theta oscillations in successful encoding. When examining the impact of alarms on encoding, band power during the 1.8-second interval post-alarm revealed significant differences in mean theta power between successful and failed trials for all conditions. Alarms were triggered when average theta power during an 800ms interval fell below a threshold, demonstrating significant differences in Theta and Beta band power for all conditions. Using theta band power for alarm triggering significantly enhanced memory accuracy, particularly in the Theta-based alarm condition compared to No alarm and Random alarm conditions (p < 0.05). These findings robustly support the hypothesis that alarms based on hippocampal theta power lead to improved memory performance.

Conclusions:

This study introduces a groundbreaking use of intracranial electroencephalography (iEEG) to target the human hippocampus and enhance real-time hippocampal theta power for the purpose of improving memory performance. Unlike previous neurofeedback studies primarily relying on non-invasive methods like EEG, this study presents novel real-time neurofeedback specifically based on hippocampal theta power. We employed the Hjorth activity method to compute hippocampal theta power in real-time, delivering alarms in case of a decrease, with the goal of improving memory performance. The study confirmed the hypothesis by showing that hippocampal theta power was not decreased in response to theta-based alarms compared to no alarm or random alarm conditions. Simultaneously, associative memory has been shown to improve. This novel approach is expected to significantly contribute to our understanding and improvement of human memory mechanisms, offering potential strategies for preventing memory-related neurological and mental health disorders.

Learning and Memory:

Long-Term Memory (Episodic and Semantic)
Learning and Memory Other 1

Modeling and Analysis Methods:

Classification and Predictive Modeling

Novel Imaging Acquisition Methods:

Imaging Methods Other 2

Keywords:

Data analysis
ELECTROCORTICOGRAPHY
Limbic Systems
Memory

1|2Indicates the priority used for review

Provide references using author date format

1. Kota, S., M.D. Rugg, and B.C. Lega, Hippocampal theta oscillations support successful associative memory formation. Journal of Neuroscience, 2020. 40(49): p. 9507-9518.
2. Addante, R.J., et al., Prestimulus theta activity predicts correct source memory retrieval. Proceedings of the National Academy of Sciences, 2011. 108(26): p. 10702-10707.
3. Jun, S., J.S. Kim, and C.K. Chung, Direct stimulation of human hippocampus during verbal associative encoding enhances subsequent memory recollection. Frontiers in human neuroscience, 2019. 13: p. 23.
4. Lin, J.J., et al., Theta band power increases in the posterior hippocampus predict successful episodic memory encoding in humans. Hippocampus, 2017. 27(10): p. 1040-1053.
5. Wang, J.-R. and S. Hsieh, Neurofeedback training improves attention and working memory performance. Clinical Neurophysiology, 2013. 124(12): p. 2406-2420.
6. Nan, W., et al., Individual alpha neurofeedback training effect on short term memory. International journal of psychophysiology, 2012. 86(1): p. 83-87.
7. Hsueh, J.J., et al., Neurofeedback training of EEG alpha rhythm enhances episodic and working memory. Human brain mapping, 2016. 37(7): p. 2662-2675.
8. Escolano, C., M. Aguilar, and J. Minguez. EEG-based upper alpha neurofeedback training improves working memory performance. in 2011 annual international conference of the IEEE engineering in medicine and biology society. 2011. IEEE.
9. Friedman, D. and R. Johnson Jr, Event‐related potential (ERP) studies of memory encoding and retrieval: A selective review. Microscopy research and technique, 2000. 51(1): p. 6-28.
10. Koizumi, K., et al., Paving the Way for Memory Enhancement: Development and Examination of a Neurofeedback System Targeting the Medial Temporal Lobe. 2023.
11. Khader, P.H., et al., Theta and alpha oscillations during working-memory maintenance predict successful long-term memory encoding. Neuroscience letters, 2010. 468(3): p. 339-343.
12. Jun, S., J.S. Kim, and C.K. Chung, Prediction of successful memory encoding based on lateral temporal cortical gamma power. Frontiers in Neuroscience, 2021. 15: p. 517316.
13. Hjorth, B., EEG analysis based on time domain properties. Electroencephalography and clinical neurophysiology, 1970. 29(3): p. 306-310.
14. Oh, S.-H., Y.-R. Lee, and H.-N. Kim, A novel EEG feature extraction method using Hjorth parameter. International Journal of Electronics and Electrical Engineering, 2014. 2(2): p. 106-110