Disentangling the roles of neocortical alpha/beta and hippocampal theta/gamma activity in human episodic memory

Abstract

Abstract Episodic memory relies on two processes: 1) our ability to process a vast amount of sensory information, and 2) our ability to bind these sensory representations together to form a coherent memory. The first process is thought to rely on neocortical alpha/beta desynchronisation while the second is thought to be supported by hippocampal theta and gamma synchronisation. However, recent empirical evidence suggests that these two neural phenomena are contingent on one another, questioning whether alpha/beta desynchronisation and theta/gamma synchronisation truly reflect distinct processes. Here, we addressed this conundrum by asking seventeen participants to complete a paradigm that temporally separated sensory information representation and mnemonic binding while undergoing MEG recordings. We found that, during the perception and retrieval of task-relevant information, neocortical alpha/beta power monotonically decreased with the number of items recalled from a sequence. During mnemonic binding however, hippocampal theta/gamma phase-amplitude coupling monotonically increased with the number of sequence items later recalled. These results suggest a double dissociation between neocortical alpha/beta and hippocampal theta/gamma activity, with alpha/beta desynchronisation uniquely relating to information representation and theta/gamma phase-amplitude coupling uniquely relating to mnemonic binding. As such, we conclude that alpha/beta desynchronisation and hippocampal theta/gamma synchronisation represent two separable processes in episodic memory. Significance Statement Episodic memories are highly detailed snapshots of our personally experienced past. The formation and retrieval of episodic memories have consistently been shown to rely on the hippocampus and the sensory neocortex. However, it is unknown whether the memory-related neural activity in the hippocampus and neocortex reflect separate, interacting cognitive processes, or are two neural responses to a singular process. Here, we find evidence in favour of the former. Memory-related decreases in neocortical alpha/beta power uniquely arise to the perception and retrieval of event-related information, while memory-related increases in hippocampal theta/gamma phase-amplitude coupling uniquely arise during mnemonic binding. This double dissociation suggests that the neocortex and hippocampus play distinct and separable roles in the formation and retrieval of episodic memories Preregistration available at: https://osf.io/4nt23/ (also included in supplementary materials). Data available at: TBC Code available at: https://github.com/benjaminGriffiths/dissociable_markers_of_memory.