The content of hippocampal “replay”

Abstract

One of the most striking features of the hippocampal network is its ability to self-generate neuronal sequences representing temporally compressed, spatially coherent paths. These brief events, often termed "replay" in the scientific literature, are largely confined to non-exploratory states such as sleep or quiet rest. Early studies examining the content of replay noted a strong correlation between the encoded spatial information and the animal's prior behavior; thus, replay was initially hypothesized to play a role in memory formation and/or systems-level consolidation via "off-line" reactivation of previous experiences. However, recent findings indicate that replay may also serve as a memory retrieval mechanism to guide future behavior or may be an incidental reflection of pre-existing network assemblies. Here, I will review what is known regarding the content of replay events and their correlation with past and future actions, and I will discuss how this knowledge might inform or constrain models which seek to explain the circuit-level mechanisms underlying these events and their role in mnemonic processes.memory, place cells, reactivation, review, ripple | I N TR ODU C TI ONAdaptive behavior requires the brain to preserve coherent representations of experience and later extract that stored information to inform future behaviors. For decades, researchers have utilized goal-directed navigation and the brain's spatial memory system as a specific example to explore more general questions regarding memory processes (Tolman, 1948). Two discoveries in particular have prompted researchers to focus such studies on the hippocampus: (a) Human patients and animal models with damage to their medial temporal lobe (and the hippocampus in particular) display severe impairments in their ability to form new episodic and spatial memories (Morris et al., 1982;Scoville & Milner, 1957;Squire et al., 2004); and (b) individual neurons within the hippocampus represent spatial information in their firing patterns during exploration, implicating the hippocampus in the processing and storage of spatial memories (Moser et al., 2008;O'Keefe and Dostrovsky, 1971). A persistent, fundamental question within this domain is how an entire experience or spatial trajectory, which may be represented within the hippocampus by the activity of tens of thousands of neurons ordered in a precise temporal sequence, can be coherently stored within that neural network or purposefully retrieved at the exact time when the stored information would be useful for guiding future decisions.Among several lines of investigation attempting to address this question (Garner et al., 2012;Josselyn et al., 2015; Ramirez et al., 2013;Tse et al., 2007), hippocampal ripples and ripple-based "replay" have emerged as strong candidate mechanisms which may facilitate both the initial storage and later retrieval of complex, temporally ordered information about experience. Ripples are brief (50-100 ms duration), high-frequency (150-300 Hz) network oscillations within ...

Three brain states in the hippocampus and cortex

“…The third is representational, and perhaps the most evocative. During SWRs, populations of place cells often fire in temporally compressed sequences reflecting spatial trajectories (example in Figure ; reviewed in O'Neill, Pleydell‐Bouverie, Dupret, & Csicsvari, ; Carr, Jadhav, & Frank, ; Buzsaki, ; Foster, ; Pfeiffer, ; Olafsdottir, Bush, & Barry, ). This sequential firing pattern, termed “replay sequences” or “replay,” has been shown to represent (a) spatial trajectories in both forward and reverse order (Csicsvari, O'Neill, Allen, & Senior, ; Davidson, Kloosterman, & Wilson, ; Diba & Buzsaki, ; Foster & Wilson, ; Gupta, van der Meer, Touretzky, & Redish, ), (b) spatial trajectories in locations or environments remote from the subjects (Davidson, Kloosterman, & Wilson, ; Gupta et al, ; Karlsson & Frank, ), (c) spatial trajectories in novel combinations not seen in prior behavior (Gupta et al, ), (4) spatial trajectories extending over meters (Davidson, Kloosterman, & Wilson, ), and (5) spatial trajectories taken by subjects in subsequent goal‐directed navigational behavior (Pfeiffer & Foster, ; see also Wu, Haggerty, Kemere, & Ji, ).…”

“…One is that the distinction between localizing versus generative is expected to be most relevant in the awake and task‐engaged subject, for whom the appropriate synthesis of localizing and generative neural activity has short‐term consequences for the subject by way of upcoming behavior. The other is that theta sequences and replay sequences each have both localizing and generative properties (Buzsaki, ; Carr et al, ; Foster, ; Olafsdottir et al, ; Pfeiffer, ; Redish, ).…”

“…Prospection may offer insight into the function of hippocampal brain states, and vice versa. Recent reviews of theta sequences (Redish, ) and replay sequences (Buzsaki, ; Foster, ; Olafsdottir et al, ; Pfeiffer, ) respectively cover what is currently known of neural‐level prospection in the hippocampus in the locomotor and SWR states. Given these available perspectives, we choose a particular approach in the present section.…”

“…A number of mechanisms for biasing replay sequences have been proposed (Buzsaki, ; Foster, ; Pfeiffer, ), but so far none are adequate. To begin with, it is clear that inputs encoding an animal's current location in a manner continuous with the classic place representation (e.g., place field “tails”) are not sufficient to account for various capacities of awake replay (discussed in Atherton et al (); Buzsaki ()), for instance, remote representation (Davidson, Kloosterman, & Wilson, ; Gupta et al, ; Karlsson & Frank, ).…”

Awake reactivation and suppression after brief task exposure depend on task novelty

“…A large number of studies have shown that post-learning neural processes play a critical role in consolidating new memories (Diekelmann & Born, 2010;McGaugh, 2000;Sasaki, Nanez, & Watanabe, 2010). One of the consolidation processes is the reemergence of the brain activities involved in the initial task during following wakefulness and sleep (Foster, 2017;Pfeiffer, 2017;Tambini & Davachi, 2019).…”