Corticothalamic phase synchrony and cross-frequency coupling predict human memory formation

Abstract

The anterior thalamic nucleus (ATN) is thought to play an important role in a brain network involving the hippocampus and neocortex, which enables human memories to be formed. However, its small size and location deep within the brain have impeded direct investigation in humans with non-invasive techniques. Here we provide direct evidence for a functional role for the ATN in memory formation from rare simultaneous human intrathalamic and scalp electroencephalogram (EEG) recordings from eight volunteering patients receiving intrathalamic electrodes implanted for the treatment of epilepsy, demonstrating real-time communication between neocortex and ATN during successful memory encoding. Neocortical-ATN theta oscillatory phase synchrony of local field potentials and neocortical-theta-to-ATN-gamma cross-frequency coupling during presentation of complex photographic scenes predicted later memory for the scenes, demonstrating a key role for the ATN in human memory encoding.DOI:http://dx.doi.org/10.7554/eLife.05352.001

Dynamic Network Communication as a Unifying Neural Basis for Cognition, Development, Aging, and Disease

“…Thus, a possible mechanism of DBS is to induce enhanced high frequency neural activity of the basal ganglia-thalamocortical network to disrupt abnormal excessive coupling (95) and regularize neuronal firing (96), a phenomenon that has been called an “informational lesion”(97). We should also note that there is emerging evidence of the involvement of thalamic structures in control of cortical oscillations in both attention via the pulvinar (98) and memory via the anterior thalamic nucleus (45). These findings suggest that thalamic modulation might provide a venue for treatment of deficits outside the motor domain.…”

“…We propose that PAC provides a bridge between local microscale (36; 37) and systems-level macroscale neuronal ensembles (29; 31; 38; 39) allowing for dynamic network communication (40–43). This assertion is supported by the fact that PAC tracks behavior, including learning (44; 45), working memory performance (46), attention (47), and reward processing (48; 49), across species (50) (see Johnson and Knight, 2015 (51) for a review). Recent evidence suggests that PAC might operate over short (< 500 ms) timescales, providing a mechanism for interregional coordination between the oscillatory local field and broadband gamma (52).…”

Oscillatory Dynamics of Prefrontal Cognitive Control

“…For example, a recent intracranial study in humans investigated the role of phase synchrony between frontal areas and the anterior thalamic nucleus (ATN) for memory formation (Figure 2A, [49]). The authors found increased PFC-ATN phase-locking in the theta-band (4-8 Hz) for successfully encoded items.…”

Formation of visual memories controlled by gamma power phase-locked to alpha oscillations

“…Coupling between gamma activity and the phase of theta or alpha oscillations has been reported in several MEG studies8910, and in invasive recordings from humans and non-human primates4111213141516171819. The CFC has been proposed to play a fundamental role for organizing neuronal processing in space and time362021.…”