Memory reactivation in rat medial prefrontal cortex occurs in a subtype of cortical UP state during slow-wave sleep

Interaction between hippocampal sharp-wave ripples (SWRs) and UP states,
possibly by coordinated reactivation of memory traces, is conjectured to
play an important role in memory consolidation. Recently, it was reported
that SWRs were differentiated into multiple subtypes. However, whether
cortical UP states can also be classified into subtypes is not known.
Here, we analysed neural ensemble activity from the medial prefrontal
cortex from rats trained to run a spatial sequence-memory task.
Application of the hidden Markov model (HMM) with three states to epochs
of UP–DOWN oscillations identified DOWN states and two subtypes of UP
state (UP-1 and UP-2). The two UP subtypes were distinguished by
differences in duration, with UP-1 having a longer duration than UP-2, as
well as differences in the speed of population vector (PV) decorrelation,
with UP-1 decorrelating more slowly than UP-2. Reactivation of recent
memory sequences predominantly occurred in UP-2. Short-duration
reactivating UP states were dominated by UP-2 whereas long-duration ones
exhibit transitions from UP-1 to UP-2. Thus, recent memory reactivation,
if it occurred within long-duration UP states, typically was preceded by a
period of slow PV evolution not related to recent experience, and which we
speculate may be related to previously encoded information. If that is the
case, then the transition from UP-1 to UP-2 subtypes may help gradual
integration of recent experience with pre-existing cortical memories by
interleaving the two in the same UP state. This article is part of the
Theo Murphy meeting issue ‘Memory reactivation: replaying events past,
present and future'.