A Theoretical and Experimentally-Driven take on Theta Time-Scale Dynamics Across the Areal Axis of the Hippocampus: Theta Prediction, Prospective Speed-Theta Relationships and its Relationship to Sensorimotor Integration

Theta (6-12 Hz) rhythmicity in the local field potential (LFP) reflects a clocking mechanism that brings physically isolated neurons together in time, allowing for the integration and segregation of distributed cell assemblies. Variation in the theta signal has been linked to locomotor speed, sensorimotor integration as well as cognitive processing. Here, we first discuss the basic anatomy of the hippocampal formation (HPC and EC) as well as the neurophysiological underpinnings of theta rhythm and current generation. Then, Chapter 2 provides an experimentally and theoretically driven overview of variation in the theta signal across the long axis of the HPC as well as the functional significance of that variation. Next, Chapter 3 provides novel experimental data into the dynamics of theta in relation to sensorimotor prediction or prospective coding along the longitudinal axis of the HPC and the EC. More specifically, in that study, we exposed rodents to environments that varied in regards to the predictability of future sensorimotor events (open field versus linear track) and subsequently manipulated their behavior to shape open field navigation into linear navigation while currently recording theta local field potentials across the septotemporal axis of the hippocampus and entorhinal cortex. We demonstrate that while navigating in an open field, theta signals in the septal hippocampus are instantaneously related to locomotor speed. In contrast, on a linear track, septal hippocampal theta signals were prospective and predicted changes in speed by hundreds of milliseconds. This prospective temporal relationship systematically decreased across the long axis of the hippocampus, but was as robust as septal hippocampus at sites in the caudomedial entorhinal cortex. Experimental manipulation of open field task demands, which morphed behavior into linear track-like behavioral output, systematically increased the time lag between speed and theta within individual rats, over days. Finally, Chapter 4 reflects more broadly on how this work contributes to our understanding of the functional significance of the theta rhythm and theta’s involvement in sensorimotor integration. The current experiments suggest that neuronal ensembles, as reflected in synchronized synaptic input, are organized into predictive patterns that allow for the predictability of sensorimotor events