Cross-Frequency Phase-Amplitude Coupling between Hippocampal Theta and Gamma Oscillations during Recall Destabilizes Memory and Renders It Susceptible to Reconsolidation Disruption

Abstract

Avoidance memory reactivation at recall triggers theta-gamma hippocampal phase amplitude coupling (hPAC) only when it elicits hippocampus-dependent reconsolidation. However, it is not known whether there is a causal relationship between these phenomena. We found that in adult male Wistar rats, silencing the medial septum during recall did not affect avoidance memory expression or maintenance but abolished hPAC and the amnesia caused by the intrahippocampal administration of reconsolidation blockers, both of which were restored by concomitant theta burst stimulation of the fimbria-fornix pathway. Remarkably, artificial hPAC generated by fimbria-fornix stimulation during recall of a learned avoidance response naturally resistant to hippocampus-dependent reconsolidation made it susceptible to reactivation-dependent amnesia. Our results indicate that hPAC mediates the destabilization required for avoidance memory reconsolidation and suggest that the generation of artificial hPAC at recall overcomes the boundary conditions of this process.

The Medial Septum as a Potential Target for Treating Brain Disorders Associated With Oscillopathies

“…The MS-governed theta oscillations provide temporal windows for temporal organization of these frequency-, pathway-, and function-specific gamma oscillations in theta cycles in a phase–phase coupling or phase–amplitude coupling manner ( Canolty and Knight, 2010 ; Belluscio et al, 2012 ; Schomburg et al, 2014 ). The MS is essential for the cross-frequency coupling ( Neymotin et al, 2011 ; Radiske et al, 2020 ), which is thought to be important in learning and memory ( Lisman and Buzsáki, 2008 ; Tort et al, 2009 ; Amemiya and Redish, 2018 ).…”

Neuromodulation of Hippocampal-Prefrontal Cortical Synaptic Plasticity and Functional Connectivity: Implications for Neuropsychiatric Disorders

“… Zheng and Zhang (2015) showed that LTP induction in the vHPC-mPFC pathway increased theta phase coupling rather than the power of either region. Also, stimulation protocols that resemble more physiological activity, such as TBS, induce theta-gamma cross-frequency coupling and interfere with memory consolidation ( Radiske et al, 2020 ). Future studies need to investigate the relationship between synaptic plasticity and network coupling in freely moving animals and control for the effects of stimulation per se .…”

Event-Related Phase-Amplitude Coupling During Working Memory of Musical Chords

“…Various studies have reported that theta-gamma PAC and theta-beta PAC were related to cognitive tasks in humans [3], [14], [19], [22], [25], [28], [31], [32], [34], [35], [43], [48] and animals [2], [3], [5], [14], [18]- [20], [28], [32], [84], [90]- [96]. However, most of these studies were performed using traditional PAC.…”