Place‐selective firing contributes to the reverse‐order reactivation of CA1 pyramidal cells during sharp waves in open‐field exploration

Abstract

On the linear track, the recent firing sequences of CA1 place cells recur during sharp wave ⁄ ripple patterns (SWRs) in a reverse temporal order [Foster & Wilson (2006) Nature, 440, 680-683]. We have found similar reverse-order reactivation during SWRs in open-field exploration where the firing sequence of cells varied before each SWR. Both the onset times and the firing patterns of cells showed a tendency for reversed sequences during SWRs. These effects were observed for SWRs that occurred during exploration, but not for those during longer immobility periods. Additionally, reverse reactivation was stronger when it was preceded by higher speed (> 5 cm ⁄ s) run periods. The trend for reverse-order SWR reactivation was not significantly different in familiar and novel environments, even though SWR-associated firing rates of both pyramidal cells and interneurons were reduced in novel environments as compared with familiar. During exploration-associated SWRs (eSWR) place cells retain place-selective firing [O'Neill et al. (2006) Neuron, 49, 143-155]. Here, we have shown that each cell's firing onset was more delayed and firing probability more reduced during eSWRs the further the rat was from the middle of the cell's place field; that is, cells receiving less momentary place-related excitatory drive fired later during SWR events. However, even controlling for place field distance, the recent firing of cells was still significantly correlated with SWR reactivation sequences. We therefore propose that both place-related drive and the firing history of cells contribute to reverse reactivation during eSWRs.

The content of hippocampal “replay”

“…Many subsequent studies replicated this surprising finding (Csicsvari et al, 2007;Davidson et al, 2009;Diba & Buzs aki, 2007;Gupta et al, 2010;Karlsson & Frank, 2009;Wu & Foster, 2014), and the term "reverse replay" entered the lexicon. Presciently, reverse reactivation of prior activity in ripples had been predicted to arise from the rekindling of recently stimulated synaptic traces nearly two decades earlier in one of the first models of two-stage memory formation (Buzs aki, 1989).…”

About Sleep's Role in Memory

“…Reactivations of hippocampal cell firing patterns occur also during waking when the animal rests after task performance or during brief pauses of active behavior like exploration or running in a maze (191, (243,406). In a task requiring the rat to run back and forth on the same elevated linear track, replay in the reverse order occurred mainly at the end of a run, whereas replay in a forward direction transpired in the anticipatory period before a new run (288, 492).…”

Early Deficits in Spatial Memory and Theta Rhythm in Experimental Temporal Lobe Epilepsy

“…However, we cannot rule out more complex correlations, such as the presence of ILA in structures connected to the CA1 region and not recorded here. Alternatively, ILA could have a negative impact when occurring during critical periods, e.g., trace reactivation (Chrobak and Buzsaki, 1994;Csicsvari et al, 2007) or place cell replay (Foster and Wilson, 2006;Molter et al, 2007). In epileptic patients, IA, unlike seizures, has no direct effect on cognition (Aldenkamp et al, 2001).…”