Five key topics have been reverberating in hippocampal-entorhinal cortex research over the past five decades: episodic and semantic memory, path integration (“dead reckoning”) and landmark (“map”) navigation, and theta oscillation. We suggest that the systematic relations between single cell discharge and the activity of neuronal ensembles reflected in local field theta oscillations, provide a useful insight into the relationship among these terms. In rats trained to run in direction-guided (1-dimensional) tasks, hippocampal cell assemblies discharge sequentially, with different assemblies active on opposite runs, that is place cells are unidirectional. Such tasks do not require map representation and are formally identical with learning sequentially occurring items in an episode. Hebbian plasticity, acting within the temporal window of the theta cycle, converts the travel distances into synaptic strengths between the sequentially activated and unidirectionally connected assemblies. In contrast, place representations by hippocampal neurons in 2‑dimensional environments are typically omnidirectional, characteristic of a map. Generation of a map requires exploration, essentially a dead reckoning behavior. I suggest that orthogonal and omnidirectional navigation through the same places (junctions) during exploration gives rise to omnidirectional place cells and, consequently, maps free of temporal context. Analogously, multiple crossings of common junction(s) of episodes convert the common junction(s) into context-free or semantic memory. Theta oscillation can hence be conceived as the navigation rhythm through both physical and mnemonic space, facilitating the formation of maps and episodic/semantic memories.
A longstanding conjecture in neuroscience is that aspects of cognition depend on the brain’s ability to self-generate sequential neuronal activity. We found that reliably and continually-changing cell assemblies in the rat hippocampus appeared not only during spatial navigation but also in the absence of changing environmental or body-derived inputs. During the delay period of a memory task each moment in time was characterized by the activity of a unique assembly of neurons. Identical initial conditions triggered a similar assembly sequence, whereas different conditions gave rise, uniquely, to different sequences, thereby predicting behavioral choices, including errors. Such sequences were not formed in control, non-memory, tasks. We hypothesize that neuronal representations, evolved for encoding distance in spatial navigation, also support episodic recall and the planning of action sequences.
