Theta Oscillations in the Human Medial Temporal Lobe during Real World Ambulatory Movement

Abstract

Theta oscillations play a critical role in learning and memory by coordinating the spiking activity of neuronal ensembles via mechanisms such as spike timing dependent plasticity1-7. This rhythm is present in rodents where it is continuously evident during movement at frequencies within 6-12Hz8,9. In humans, however, the presence of continuous theta rhythm has been elusive; indeed, a functionally similar theta is thought to occur at lower frequency ranges (3-7Hz) and in shorter bouts10-12. This lower frequency theta rhythm is observed during a variety of behaviors, including virtual navigation, but has never been tested during real world ambulatory movement. Here we examined the oscillatory properties of theta within the human medial temporal lobe (MTL) in freely moving human subjects chronically implanted with the clinical NeuroPace RNS(R) responsive neurostimulator device, capable of wireless recordings of continuous intracranial deep brain electroencephalographic (iEEG) activity. MTL iEEG recordings, together with sub-millimeter position tracking, revealed the presence of high frequency theta oscillations (6-12Hz) during ambulation. The prevalence of these oscillations was increased during fast movement compared to slow movement. These theta bouts, although occurring more frequently, were not significantly different in durations during fast versus slow movements. In a rare opportunity to study one subject with congenital blindness, we found that both the prevalence and duration of theta bouts were much greater than those in sighted subjects. Our results suggest that higher frequency theta indeed exists in humans during movement providing critical support for conserved neurobiological mechanisms for spatial navigation. The precise link between this pattern and its behavioral correlates will be an exciting area for future studies given this novel methodology for simultaneous motion capture and long term chronic recordings from deep brain targets during ambulatory human behavior.