Ripple Band Phase Precession of Place Cell Firing during Replay

Phase coding offers several theoretical advantages for information transmission compared to an equivalent rate code. Phase coding is shown by place cells in the rodent hippocampal formation, which fire at progressively earlier phases of the movement related 6-12Hz theta rhythm as their spatial receptive fields are traversed. Importantly, however, phase coding is independent of carrier frequency, and so we asked whether it might also be exhibited by place cells during 150-250Hz ripple band activity, when they are thought to replay information to neocortex. We demonstrate that place cells which fire multiple spikes during candidate replay events do so at progressively earlier ripple phases, and that spikes fired across all replay events exhibit a negative relationship between decoded location within the firing field and ripple phase. These results provide insights into the mechanisms underlying phase coding and place cell replay, as well as the neural code propagated to downstream neurons.

Rhythmic Accessibility to Sequential Working Memory in a Theta Phase-Dependent Manner

Working memory is active short-term memory storage that is easily accessible and underlies various activities, such as maintaining phone numbers in mind for a short period [1,2]. There is accumulating theoretical and physiological evidence that memorized items are represented rhythmically by neural oscillation in the theta range (4-7 Hz) [3,4]. However, the impact of this process on human behavior is yet to be examined. Here we show that simply memorizing sequential information affects a behavioral index (i.e., reaction time, RT) in a rhythmic manner. In the main experiment (Experiment 1), we measured RTs to a visual probe that appeared at one of two sequentially memorized locations after a random interval. Consequently, RTs to the first and second probes each fluctuated in the theta range as a function of the random interval, and the phases of the two theta fluctuations were not in phase or anti-phase, but shifted by approximately 270 degree. Interestingly, the 270 degree phase difference corresponded to the rhythm of "phase coding", where sequential information is represented on the specific phase of theta oscillation [5-7]. These relationships were not observed in tasks simply requiring attention (Experiment 2) or memorization (Experiment 3) of spatial locations without sequential order. In conclusion, the current results demonstrate that our behavior fluctuates when recalling memorized sequential items in the theta-range, suggesting that accessibility to sequential working memory is rhythmic rather than stable, possibly reflecting theta-phase coding.

Volitional learning promotes theta phase coding in the human hippocampus

Electrophysiological studies in rodents show that active navigation enhances hippocampal theta oscillations (4–12 Hz), providing a temporal framework for stimulus-related neural codes. Here we show that active learning promotes a similar phase coding regime in humans, although in a lower frequency range (3–8 Hz). We analyzed intracranial electroencephalography (iEEG) from epilepsy patients who studied images under either volitional or passive learning conditions. Active learning increased memory performance and hippocampal theta oscillations and promoted a more accurate reactivation of stimulus-specific information during memory retrieval. Representational signals were clustered to opposite phases of the theta cycle during encoding and retrieval. Critically, during active but not passive learning, the temporal structure of intracycle reactivations in theta reflected the semantic similarity of stimuli, segregating conceptually similar items into more distant theta phases. Taken together, these results demonstrate a multilayered mechanism by which active learning improves memory via a phylogenetically old phase coding scheme.