Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval

Abstract

The hippocampus is required for the encoding, consolidation and retrieval of event memories. Although the neural mechanisms that underlie these processes are only partially understood, a series of recent papers point to awake memory replay as a potential contributor to both consolidation and retrieval. Replay is the sequential reactivation of hippocampal place cells that represent previously experienced behavioral trajectories and occurs frequently in the awake state, particularly during periods of relative immobility. Awake replay may reflect trajectories through either the current environment or previously visited environments that are spatially remote. The repetition of learned sequences on a compressed time scale is well suited to promote memory consolidation in distributed circuits beyond the hippocampus, suggesting that consolidation occurs in both the awake and sleeping animal. Moreover, sensory information can influence the content of awake replay, suggesting a role for awake replay in memory retrieval.

Figure 1. Place cell sequences experienced during behavior are replayed in both the forward and reverse direction during awake SWRs

Spike trains for 13 neurons with place fields on the track are shown before, during, and after a single traversal. Sequences that occur during running (center) are reactivated during awake SWRs. Forward replay (left inset, red box) occurs before traversal of the environment and reverse replay (right inset, blue box) afterwards. The CA1 local field potential is shown on top and the animal’s velocity is shown below. Adapted with permission from Diba and Buzsaki, 2007.

Figure 2. Awake replay reinstates representations of both current and past experiences

(a) The animal’s physical location during a local replay event. (b) Sequential spiking of neurons with place fields in the current environment during an SWR. At top is the filtered CA1 local field potential. The color bar shows the colors associated with each 15ms time bin used for decoding. (c) Probability distribution of decoded location for each time bin. Each color corresponds to the spiking in the associated time bin, gray indicates time bins where no spikes occurred. (d) A diagram of the local replay event, emanating away from the animal’s current location. (e) The animal’s physical location during a remote replay event. (f) Spiking of cells during the SWR for cells with place fields in either the remote (top) or local (bottom) environment. (g,h) Decoded locations reflect a coherent trajectory through the remote environment. Adapted with permission from Karlsson and Frank, 2009.

Figure 3. Spatial inputs could lead to retrieval of either local or remote sequences

Schematic illustrating how current sensory input could trigger either local or remote replay. Current sensory information relating to the animal’s current location activates cells with place fields near by. These cells act as “initiator” cells and lead to sequential reactivation of previously stored sequences. Because the initiator cell also has a place field in a spatially remote environment, this cell can initiate replay of either environment. The initiator cell leads to reactivation of stored sequences (top) through either the current environment-- local replay, (bottom left) or a previously experienced environment-- remote replay (bottom right). Note that the geometry of the neural ensemble is for illustration only and does not represent any actual topography of representations in the hippocampus.