Flexibility of Functional Neuronal Assemblies Supports Human Memory

BACKGROUND: Assemblies, groups of neurons that fire together on short timescales, could provide the fundamental building block of cognition but have eluded observation in human recordings. OBJECTIVE: Leveraging a large single unit dataset obtained from human epilepsy patients, we observe neuronal assemblies and relate their composition and dynamics to human memory for the first time. METHODS: We enrolled human epilepsy patients implanted with electrodes capable of recording both large-scale brain oscillations as well as the spiking activity of single neurons. Using established methods, we identified groups of neurons that consistently fire within 25 ms of each other across recording. We extracted several features of these assemblies, such as the order of neuron firing within the identified groups, the relationship of assembly activity to underlying gamma oscillations (40 Hz), and the dynamics of neuron membership in assemblies across recording. RESULTS: We find that assemblies are comprised of sequences of neurons phase-locked to underlying gamma oscillations, and that both the consistency of these sequences and their reactivation rate correlates with successful memory. Further, we find that the relative contribution of each neuron to the assembly drifts across recording. The magnitude of drift predicts memory performance and varies along the hippocampal longitudinal axis. CONCLUSION: Our data provide human validation to the hypothesized relevance of transiently co-active neurons to memory. This work has important implications for the continuing efforts to develop brain computer interface devices that rescue cognitive deficits and for elucidating the fundamental mechanisms by which the brain constructs thought.