Abstract
Hippocampal place-cell sequences observed during awake immobility often represent previous experience, suggesting a role in memory processes. However, recent reports of goals being overrepresented in sequential activity suggest a role in short-term planning, although a detailed understanding of the origins of hippocampal sequential activity and of its functional role is still lacking. In particular, it is unknown which mechanism could support efficient planning by generating place-cell sequences biased toward known goal locations, in an adaptive and constructive fashion. To address these questions, we propose a model of spatial learning and sequence generation as interdependent processes, integrating cortical contextual coding, synaptic plasticity and neuromodulatory mechanisms into a map-based approach. Following goal learning, sequential activity emerges from continuous attractor network dynamics biased by goal memory inputs. We apply Bayesian decoding on the resulting spike trains, allowing a direct comparison with experimental data. Simulations show that this model (1) explains the generation of never-experienced sequence trajectories in familiar environments, without requiring virtual self-motion signals, (2) accounts for the bias in place-cell sequences toward goal locations, (3) highlights their utility in flexible route planning, and (4) provides specific testable predictions.
Highlights
By their remarkable spatial selectivity, hippocampal place cells have qualified as a model system for studying neural coding in relation to behavior (O’Keefe and Nadel, 1978; Burgess, 2014)
We present a model of place-cell sequences, implemented in a large-scale spiking network with physiologically interpretable parameters, in which goal learning by reward-based plasticity shapes the sequence generation process, and in which sequential activity guides spatial behavior
We describe the generation and development of place-cell sequences, resulting from memory recall of learned goal locations, in more detail
Summary
By their remarkable spatial selectivity, hippocampal place cells have qualified as a model system for studying neural coding in relation to behavior (O’Keefe and Nadel, 1978; Burgess, 2014). According to the “two-stage” model of memory, SWR events are involved in memory consolidation, facilitating the transfer of labile hippocampal memory traces to neocortical areas (Marr, 1971; Buzsáki, 1989) During these events, place cell activity displays sequential patterns termed forward replay and reverse replay: Time-compressed, and sometimes time-reversed, replicas of place cell activity during previous runs Goal locations are over-represented in place cell activity during SWRs in open-field tasks (Dupret et al, 2010), even in the form of trajectories which predict immediate future behavior (Pfeiffer and Foster, 2013). It has been proposed that awake place-cell sequences can guide ongoing behavior by planning future trajectories, toward goal locations (Diba and Buzsáki, 2007; Dupret et al, 2010; Pfeiffer and Foster, 2013; Olafsdóttir et al, 2015) or by evaluating options and decision-making (Carr et al, 2011; Jadhav et al, 2012)
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