Combined single neuron unit activity and local field potential oscillations in a human visual recognition memory task

Combined single neuron unit activity and local field potential oscillations in a human visual recognition memory task 170 177 IEEE Transactions on Biomedical Engineering (TBME)

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Kucewicz, M.T., Berry, B.M., Bower, M.R., Cimbalnik, J., Svehlik, V., Stead, S.M., Worrell, G.A., Mayo Clinic, USA

Current neurotechnologies typically probe only a limited range of the vast scale of human brain electrophysiological activities, focusing either on the micro-electrode recordings of single neurons and their local assemblies (action potentials and local field potential) or the macro-electrode field potential of large neural populations (e.g. electrocorticogram). This paper compares the two scales through intracranial hybrid electrode recordings from micro-contacts (40 μm diameter) embedded between macro-contacts (1300 μm diameter) in epilepsy patients performing a recognition memory task. High frequency oscillations (HFOs) recorded on the macro-contacts were transformed to point processes and directly compared to single neuron action potentials (SUA) detected on adjacent micro-contacts during epochs of memory encoding and retrieval of emotionally charged images. HFOs showed more robust average response to image presentations than SUA with up to 80% increase in HFO counts compared to 2% increase in SUA firing rates. A large proportion of the macro-contacts also showed significantly different HFO responses to affectively charged vs neutral images (up to 18%) and to previously seen versus new images (up to 32%), compared to approx. 5% of all SUA recorded from all micro-contacts. These results offer a new analytical approach to combined micro- and macro-contact recordings during cognitive processing and support development of new high-density hybrid electrode technologies as envisioned in the BRAIN initiative. Such large-scale electrophysiology will enable simultaneous sampling of the activity of multiple individual neurons on the micro-scale, and their coordinated networks on the macro-scale to provide biomarkers of neuronal assemblies underlying human memory and other brain functions.

Keywords: high frequency oscillations, hybrid electrodes, large-scale electrophysiology, neuronal assemblies, neurons, human brain, memory, cognition, local field potential.