Oscillations support short latency co-firing of neurons during human episodic memory formation

Abstract

Theta and gamma oscillations in the medial temporal lobe are suggested to play a critical role for human memory formation via establishing synchrony in neural assemblies. Arguably, such synchrony facilitates efficient information transfer between neurons and enhances synaptic plasticity, both of which benefit episodic memory formation. However, to date little evidence exists from humans that would provide direct evidence for such a specific role of theta and gamma oscillations for episodic memory formation. Here we investigate how oscillations shape the temporal structure of neural firing during memory formation in the medial temporal lobe. We measured neural firing and local field potentials in human epilepsy patients via micro-wire electrode recordings to analyze whether brain oscillations are related to co-incidences of firing between neurons during successful and unsuccessful encoding of episodic memories. The results show that phase-coupling of neurons to faster theta and gamma oscillations correlates with co-firing at short latencies (~20-30 ms) and occurs during successful memory formation. Phase-coupling at slower oscillations in these same frequency bands, in contrast, correlates with longer co-firing latencies and occurs during memory failure. Thus, our findings suggest that neural oscillations play a role for the synchronization of neural firing in the medial temporal lobe during the encoding of episodic memories.

Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus

“…The effects of eye movement evoked responses on this theta were not reported but saccadelocked increases in reported theta power, thus, it remains unclear what effect saccadic responses may have had on the reported theta gamma coupling. In the third study, using microwires, the most applicable measures to our study produced generally consistent results, including decreased theta and increased gamma power associated with successful associative memory, and no difference in low-frequency spike field coherence for locally measured fields and spikes (Roux et al, 2022). Here, unlike the first study (Axmacher et al, 2010), the modulation of gamma power by peak 5-11 Hz phase was greater with successful memory (hits vs. misses).…”

“…The results of the current study show that theta oscillations are not prominent during awake behavior and do not couple with gamma, and thus, are not a good candidate for structuring possible gamma sub-bands. Although most studies in humans focus on coupling via slower or faster bands outside this range, we note two exceptions that ostensibly find increases in hippocampal theta-gamma coupling associated with active processing in the theta band (Axmacher et al, 2010; Stangl et al, 2021) and a third that included 5-11 Hz, for which the low-frequency-granting signal may have included the alpha band (Roux et al, 2022). Both of the former studies use macro-electrode iEEG with >1 mm contacts and 3-10mm spacing between contacts, along with MR/CT coregistration, which are estimated to be in some regions of the hippocampus proper in only a subset of participants.…”

Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus

“…The results of the current study show that theta oscillations are not prominent during awake behavior and do not couple with gamma, and thus, are not a good candidate for structuring possible gamma sub-bands. Although most studies in humans focus on coupling via slower or faster bands outside this range, we note two exceptions that ostensibly find increases in hippocampal theta-gamma coupling associated with active processing in the theta band ( Axmacher et al, 2010 ; Stangl et al, 2021 ) and a third that included 5–11 Hz, for which the low-frequency-granting signal may have included the alpha band ( Roux et al, 2022 ). Both of the former studies use macro-electrode iEEG with >1 mm contacts and 3–10 mm spacing between contacts, along with MR/CT coregistration, which are estimated to be in some regions of the hippocampus proper in only a subset of participants.…”

“…As such, each ripple is likely contributing disproportionately to the spike-locked activity. In addition, we know that visual ( Katz et al, 2020 ; Rey et al, 2014 ; Roux et al, 2022 ) and saccade-elicited (‘ERP-like’) responses in the hippocampus ( Hoffman et al, 2013 ; Jutras et al, 2009 ; Katz et al, 2022 ) increase theta-band power without necessarily producing harmonic oscillations. This would presumably only affect the segments from search, not sleep.…”

Gamma sensory stimulation and effects on the brain

“…To obtain the PSD, the signal was high-pass filtered at 2 Hz and then re-referenced using the Gram-Schmidt process 24 to subtract the average signal of all other electrodes whilst avoiding the introduction of a spurious 40 Hz signal measured in other electrodes (see 24,30 ). The signal was then subdivided into 2s long segments and spectral power in each segment was calculated using Welch’s method.…”