Abstract
According to dual-process theories, recognition memory draws upon both familiarity and recollection. It remains unclear how primate prefrontal cortex (PFC) contributes to familiarity and recollection processes but frequency-specific neuronal oscillations are considered to play a key role. Here, non-human primate (NHP) electrophysiological recordings first showed that a specific subregion of macaque PFC (i.e., dorsolateral PFC, dlPFC) was implicated at a specific frequency (i.e., increased beta oscillatory power) in a specific phase of a recognition memory task (i.e., during sample presentation). Then, to assess generalization to humans we targeted left human dlPFC (BA 9/46) as well as left dorsomedial prefrontal cortex (BA 8/9) for comparison, and also vertex as a control, with low-beta frequency transcranial magnetic stimulation (compared to non-frequency-specific stimulation, and to no-stimulation control) during occasional sample presentations within a similar task; hence we investigated the causal importance for human memory of a location-specific, frequency-specific, and task-epoch-specific intervention derived directly from the NHP electrophysiological observations. Using a dual-process signal detection (DPSD) model based on analysing receiver operating characteristics (ROC) curves, we showed beta-frequency TMS caused decreased recollection when targeted to human dlPFC, but enhanced familiarity when targeted to dorsomedial prefrontal cortex. Non-frequency-specific patterns of stimulation to all sites, and beta-frequency stimulation to vertex, were all without behavioural effect. This study provides causal evidence that PFC-mediated contributions to object recognition memory are modulated by beta-frequency oscillations; more broadly it provides translational evidence bridging NHPs and humans by emphasizing functional roles of beta oscillations in homologous brain regions in recognition memory.
Significance Statement Recognition memory is assumed to draw upon both familiarity and recollection. Little is known yet about how neural oscillations in different sub-regions of primate prefrontal cortex (PFC) underlies these two processes. By recording macaque local field potentials we first observed modulation of beta-frequency oscillatory power in dorsolateral PFC during sample stimulus encoding. Then, in an analogous recognition memory task in humans, we used targeted transcranial magnetic stimulation (TMS) to causally influence PFC mnemonic function during encoding. We revealed a double dissociation between the effects of beta-frequency stimulation to dorsolateral PFC in suppressing recollection process and dorsomedial PFC in enhancing familiarity process. These cross-species translational studies demonstrate a causal role of beta-frequency oscillations in PFC to primate recognition memory performance.








