Temporal Encoding of Place Sequences by Hippocampal Cell Assemblies

Abstract

Both episodic memory and spatial navigation require temporal encoding of the relationships between events or locations. In a linear maze, ordered spatial distances between sequential locations were represented by the temporal relations of hippocampal place cell pairs within cycles of theta oscillation in a compressed manner. Such correlations could arise due to spike "phase precession" of independent neurons driven by common theta pacemaker or as a result of temporal coordination among specific hippocampal cell assemblies. We found that temporal correlation between place cell pairs was stronger than predicted by a pacemaker drive of independent neurons, indicating a critical role for synaptic interactions and precise timing within and across cell assemblies in place sequence representation. CA1 and CA3 ensembles, identifying spatial locations, were active preferentially on opposite phases of theta cycles. These observations suggest that interleaving CA3 neuronal sequences bind CA1 assemblies representing overlapping past, present, and future locations into single episodes.

Interaction between neocortical and hippocampal networks via slow oscillations

“…The timing of spikes within the theta cycle (i.e. their phase) is determined by the dynamic interaction between intra-and extra-hippocampal networks so that the phase of spikes correlates with the spatial position of the animal (O' Keefe and Recce, 1993;Harris et al, 2002;Mehta et al, 2002;Dragoi and Buzsáki, 2006). …”

Phase Precession Through Synaptic Facilitation

“…Adapted, with permission, from Skaggs et al (1996). subsequent papers has confirmed and refined this observation (e.g., Skaggs et al, 1996;Yamaguchi, Aota, McNaughton, & Lipa, 2002;Harris et al, 2002;Mehta et al, 2002;Huxter, Burgess, & O'Keefe, 2003;Dragoi & Buzsáki, 2006;Maurer, Cowen, Burke, Barnes, & McNaughton, 2006a;Chen & Frank, 2007; see also the reviews by McNaughton, 2007, andYamaguchi et al, 2007). Phase precession exists in both CA3 and CA1 pyramidal cells, but it is much less pronounced in CA1 interneurons (Maurer, Cowen, Burke, Barnes, & McNaughton, 2006b;Ego-Stengel & Wilson, 2007) and the dentate gyrus Yamaguchi et al, 2002).…”

“…To bridge the long temporal gap between an early input phase of DG granule cells (for example ψ = 90 • ) and late firing phases ≈ 360 • in CA3 pyramidal cells, we assumed a slow decay of EPSPs (see Figure 2B), due to a membrane integration time τ m that is comparable to the (2002) and Dragoi & Buzsáki (2006) determined phases via a Hilbert transform of the CA1 sp EEG, which assigns phase 0 • to the field potential peaks. A third convention is used by Huxter et al (2003), who take phase 0 • as "the + to − zero crossings" of CA1 sp theta.…”

“…Place cells with small place fields exhibit rapid phase precession, whereas cells with large fields display slow phase precession such that the range of firing phases is the same in both cases (Ekstrom et al, 2001;Dragoi & Buzsáki, 2006;Geisler et al, 2007). Mossy fiber facilitation should therefore be strong for small place fields where a CA3 place cell receives only few DG input spikes on average.…”

“…Here we propose that synaptic facilitation, for example, at the hippocampal mossy fiber (mf) synapse, allows for generating a relational spike code. This code might be important for one-shot learning and episodic-like memory, that is, the association of events in a behavioral sequence that occur on a timescale of seconds (Skaggs, McNaughton, Wilson, & Barnes, 1996;Silva et al, 1996;Brun et al, 2002;Fortin, Agster, & Eichenbaum, 2002;Kesner, Gilbert, & Barua, 2002;Mehta, Lee, & Wilson, 2002;Sato & Yamaguchi, 2003;Melamed, Gerstner, Maass, Tsodyks, & Markram, 2004;Jensen & Lisman, 2005;Dragoi & Buzsáki, 2006).…”