Abstract
Hippocampal place field sequences are supported by sensory cues and network internal mechanisms. In contrast, sharp-wave (SPW) sequences, theta sequences, and episode field sequences are internally generated. The relationship of these sequences to memory is unclear. SPW sequences have been shown to support learning and have been assumed to also support episodic memory. Conversely, we demonstrate these SPW sequences were present in trained rats even after episodic memory was impaired and after other internal sequences - episode field and theta sequences - were eliminated. SPW sequences did not support memory despite continuing to 'replay' all task-related sequences - place- field and episode field sequences. Sequence replay occurred selectively during synchronous increases of population excitability -- SPWs. Similarly, theta sequences depended on the presence of repeated synchronized waves of excitability - theta oscillations. Thus, we suggest that either intermittent or rhythmic synchronized changes of excitability trigger sequential firing of neurons, which in turn supports learning and/or memory.
Highlights
It has been suggested that the composition of these internal sequences reflects the synaptic connectivity of the network, first, because the formation of internal sequences frequently requires learning (Gill et al, 2011; Xu et al, 2012) and, second, because similar sequences can be repeated in the absence of prominent sensory cues (Wilson and McNaughton, 1994; Ji and Wilson, 2007; Pastalkova et al, 2008; Carrillo-Reid et al, 2015; Markowitz et al, 2015)
SPW sequences are thought to play an important role in learning (Buzsaki, 1989, 2015), in part, because neuronal sequences with an order highly similar to place field sequences are replayed during SPWs
We identified episode field sequences generated during wheel running (Figure 1A-purple, Pastalkova et al, 2008) and place field sequences in the arms of the maze (Figure 1A-green)
Summary
Sequences generated in the absence of sensory cues have been observed in various cortical areas, basal ganglia, and the hippocampus (Wilson and McNaughton, 1994; Nadasdy et al, 1999; Louie and Wilson, 2001; Dragoi and Buzsaki, 2006; O’Neil et al, 2006; Foster and Wilson, 2006; Ji and Wilson, 2007; Lee and Wilson, 2002; Pastalkova et al, 2008; Luczak et al, 2009; Peyrache et al, 2009; Havenith et al, 2011; Harvey et al, 2012; Xu et al, 2012; CarrilloReid et al, 2015; Markowitz et al, 2015; Mello et al, 2015). Episode field sequences might appear to be like place field sequences (O’Keefe and Dostrovsky, 1971); but unlike place field sequences, episode field sequences are formed independently of sensory cues and only during memory tasks (Wang et al, 2015)
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