Theta band power increases in the posterior hippocampus predict successful episodic memory encoding in humans

• Published in: Hippocampus 2017-10, Vol.27 (10), p.1040-1053
• Main Authors: Lin, Jui‐Jui, Rugg, Michael D., Das, Sandhitsu, Stein, Joel, Rizzuto, Daniel S., Kahana, Michael J., Lega, Bradley C.
• Format: Article
• Language: English
• Subjects: Amygdala; anterior hippocampus; Drug Resistant Epilepsy - diagnostic imaging; Drug Resistant Epilepsy - physiopathology; Drug Resistant Epilepsy - surgery; EEG; Electrocorticography; episodic memory; Gamma Rhythm; Gene expression; Hippocampus; Hippocampus - diagnostic imaging; Hippocampus - physiology; Hippocampus - physiopathology; Humans; Magnetic Resonance Imaging; Memory, Episodic; Mental Recall - physiology; Neuropsychological Tests; posterior hippocampus; Rodents; Specialization; Stereotaxic Techniques; subsequent memory effect; theta; Theta Rhythm; Theta rhythms
• ISSN: 1050-9631; 1098-1063
• DOI: 10.1002/hipo.22751

Functional differences in the anterior and posterior hippocampus during episodic memory processing have not been examined in human electrophysiological data. This is in spite of strong evidence for such differences in rodent data, including greater place cell specificity in the dorsal hippocampus, greater sensitivity to the aversive or motivational content of memories in ventral regions, connectivity analyses identifying preferential ventral hippocampal connections with the amygdala, and gene expression analyses identifying a dorsal–ventral gradient. We asked if memory‐related oscillatory patterns observed in human hippocampal recordings, including the gamma band and slow‐theta (2.5–5 Hz) subsequent memory effects, would exhibit differences along the longitudinal axis and between hemispheres. We took advantage of a new dataset of stereo electroencephalography patients with simultaneous, robotically targeted anterior, and posterior hippocampal electrodes to directly compare oscillatory subsequent memory effects during item encoding. This same data set allowed us to examine left–right connectivity and hemispheric differences in hippocampal oscillatory patterns. Our data suggest that a power increase during successful item encoding in the 2.5–5 Hz slow‐theta frequency range preferentially occurs in the posterior hippocampus during the first 1,000 ms after item presentation, while a gamma band power increase is stronger in the dominant hemisphere. This dominant–nondominant pattern in the gamma range appears to reverse during item retrieval, however. Intrahippocampal phase coherence was found to be stronger during successful item encoding. Our phase coherence data are also consistent with existing reports of a traveling wave for theta oscillations propagating along the septotemporal (longitudinal) axis of the human hippocampus. We examine how our findings fit with theories of functional specialization along the hippocampal axis.