Abstract
The prefrontal cortex and hippocampus are crucial for memory-guided decision-making. Neural activity in the hippocampus exhibits place-cell sequences at multiple timescales, including slow behavioral sequences (~seconds) and fast theta sequences (~100-200 ms) within theta oscillation cycles. How prefrontal ensembles interact with hippocampal sequences to support decision-making is unclear. Here, we examined simultaneous hippocampal and prefrontal ensemble activity in rats during learning of a spatial working-memory decision task. We found clear theta sequences in prefrontal cortex, nested within its behavioral sequences. In both regions, behavioral sequences maintained representations of current choices during navigation. In contrast, hippocampal theta sequences encoded alternatives for deliberation and were coordinated with prefrontal theta sequences that predicted upcoming choices. During error trials, these representations were preserved to guide ongoing behavior, whereas replay sequences during inter-trial periods were impaired prior to navigation. These results establish cooperative interaction between hippocampal and prefrontal sequences at multiple timescales for memory-guided decision-making.
Highlights
The neural substrates that support decision-making are still not fully understood
As a result of spatially specific firing, sequences of CA1 and prefrontal cortex (PFC) cells successively activated on the timescale of seconds as the rat ran through a trajectory, as previously reported by several groups (Frank et al, 2000; Fujisawa et al, 2008; Ito et al, 2015; Kinsky et al, 2020; Shin et al, 2019; Stout and Griffin, 2020; Wood et al, 2000)
Within each cycle of theta oscillations during navigation, which corresponds to expression of fast CA1 theta sequences (Dragoi and Buzsaki, 2006; Foster and Wilson, 2007; Gupta et al, 2012; Skaggs et al, 1996), we found that PFC cells were organized into sequences as well and could occur concurrently with the hippocampal sequences (Figure 1C)
Summary
The neural substrates that support decision-making are still not fully understood. The link between decision-making and neural representations at the behavioral timescale has been studied extensively in various cortical and sub-cortical circuits of different species. Heterogenous activity patterns comprising sequences of neuronal activation that span entire task periods have emerged as a common coding scheme in many brain regions, including PFC (Baeg et al, 2003; Fujisawa et al, 2008; Ito et al, 2015), hippocampus (Ito et al, 2015; Pastalkova et al, 2008), PPC (Crowe et al, 2010; Harvey et al, 2012), and striatum (Bakhurin et al, 2016; Barnes et al, 2005) In addition to this behavioral-timescale activity, recent work has raised the possibility that neural dynamics at fast, cognitive timescales that occur transiently during discrete subsets of task periods can underlie upcoming decisions.
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