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

By J. Csicsvari, J. O’Neill, Kevin Allen, Timothy J. Senior. 2007

149 citations recorded by the source corpus.

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.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience

How researchers see this paper

The researchers whose trusted networks rank it highest, strongest advocate first. Every researcher gets a different order.

In Cellular and Molecular Neuroscience

In Cognitive Neuroscience

Citations in the corpus

Awake replay of remote experiences in the hippocampus (2009, positive): “Complementary studies have shown that entire sequences can be replayed at high speeds14–16, 19.”
Hippocampal Replay is Not a Simple Function of Experience (2010, background): “…and step backward to replay the immediate past (Foster and Wilson, 2006; Csicsvari et al., 2007), supporting the idea that backward replay arises from a decaying remnant signal in recently active neurons (Buzsáki, 1989; Foster and Wilson, 2006; Csicsvari et al., 2007; O’Neill et al., 2008).”
Hippocampal replay of extended experience (2009, neutral): “There are significantly more remote replay events than the number of false positives expected to be generated by our replay detection procedure (52 of 1656 events; p < 10 11 under a binomial distribution, using false-positive rate of 1%).”
The Role of Hippocampal Replay in Memory and Planning (2018, background): “Indeed, in 1978, O’Keefe and Nadel [2] noted that, during quiescence and quiet wakefulness, the local field potential (LFP) of CA1 was interrupted by short bouts (40–120 ms) of high frequency (140–250 Hz) oscillations superimposed on lower frequency deflections; the high frequency components were te”
Replay Comes of Age. (2017, background): “…later results from several different labs that established highly robust replay sequences across tens of simultaneously recorded cells occurring during the awake state (Csicsvari et al. 2007, Davidson et al. 2009, Diba & Buzsaki 2007, Foster & Wilson 2006, Gupta et al. 2010, Karlsson & Frank 2009).”
Sequence Learning and the Role of the Hippocampus in Rodent Navigation (2012, unknown): “The phenomenon has been extensively replicated [53,54,55 ,56 ,57].”
Rewarded Outcomes Enhance Reactivation of Experience in the Hippocampus (2009, unknown): “…activity of pairs of CA1 place cells during SWRs (Kudrimoti et al., 1999; Cheng and Frank, 2008) as well as sequential replay of CA3 and CA1 place cells during SWRs (Foster and Wilson, 2006; Diba and Buzsá ki, 2007; Csicsvari et al., 2007; Karlsson and Frank, 2009; Davidson et al., 2009).”
The restless engram: consolidations never end. (2012, background): “Such replay is observed time locked either to an immediate experience (Foster & Wilson 2006, Csicsvari et al. 2007, Diba & Buzsaki 2007) or to a spatially and temporally remote one (Davidson et al. 2009, Karlsson & Frank 2009).”
Hippocampal sharp wave‐ripple: A cognitive biomarker for episodic memory and planning (2015, background): “The hypothesis that the “tail” of place-fields is responsible for reverse replay (O’Neill et al., 2006; Csicsvari et al., 2007) applies also to the forward replay (Fig.”
New experiences enhance coordinated neural activity in the hippocampus. (2008, unknown): “…McNaughton, 1994; Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Kudrimoti et al., 1999; Louie and Wilson, 2001; Lee and Wilson, 2002; Jackson et al., 2006; Ji and Wilson, 2007) or waking activity (O'Neill et al., 2006; Foster and Wilson, 2006; Diba and Buzsaki, 2007; Csicsvari et al., 2007).”
Reverse replay of hippocampal place cells is uniquely modulated by changing reward (2016, unknown): “Subsequently, reverse replay was replicated, but additionally, it was found that forward replay also occurred during awake immobility (Csicsvari et al., 2007; Davidson et al., 2009; Diba and Buzsáki, 2007; Gupta et al., 2010; Karlsson and Frank, 2009).”
Distinct hippocampal-cortical memory representations for experiences associated with movement versus immobility (2017, unknown): “These reinstated activity patterns correspond to representations of trajectories through space (Csicsvari et al., 2007; Davidson et al., 2009; Diba and Buzsáki, 2007; Foster and Wilson, 2006; Gupta et al., 2010; Jackson et al., 2006; Karlsson and Frank, 2009; Pfeiffer and Foster, 2013; Wu and Foster”