Abstract
Spatial learning requires the hippocampus, and the replay of spatial sequences during hippocampal sharp wave-ripple (SPW-R) events of quiet wakefulness and sleep is believed to play a crucial role. To test whether the coordination of VTA reward prediction error signals with these replayed spatial sequences could contribute to this process, we recorded from neuronal ensembles of the hippocampus and VTA as rats performed appetitive spatial tasks and subsequently slept. We found that many reward responsive (RR) VTA neurons coordinated with quiet wakefulness-associated hippocampal SPW-R events that replayed recent experience. In contrast, coordination between RR neurons and SPW-R events in subsequent slow wave sleep was diminished. Together, these results indicate distinct contributions of VTA reinforcement activity associated with hippocampal spatial replay to the processing of wake and SWS-associated spatial memory.DOI: http://dx.doi.org/10.7554/eLife.05360.001
Highlights
Hippocampal dependent learning and memory formation are influenced by reward and are believed to occur during distinct behavioral states
Many VTA units modified their firing rate during goal approach and with acquisition of food rewards (n = 47/84), consistent with prior observations (Morris et al, 2006; Roesch et al, 2007; Totah et al, 2013) (Figure 1B; Materials and methods). These results have been interpreted as the representation of reward prediction error in instrumental tasks (Morris et al, 2006; Roesch et al, 2007; Totah et al, 2013)
Hippocampal dependent learning and memory are influenced by reward, and sharp wave-ripple (SPW-R) events contribute to these functions (Jadhav et al, 2012; Girardeau et al, 2009; Ego-Stengel and Wilson, 2010)
Summary
Hippocampal dependent learning and memory formation are influenced by reward and are believed to occur during distinct behavioral states. SPW-R events contribute to spatial learning (Jadhav et al, 2012; Girardeau et al, 2009; Ego-Stengel and Wilson, 2010), and the capacity for reward to influence reactivation of CA3 place cell pairs in SPW-R events (Singer and Frank, 2009) suggests that reward-related neural activity is likely to play an important role in this process It has been unclear whether replay events of quiet wakefulness and sleep differ in their contribution to learning and memory, but the observation that replay events during slow wave sleep (SWS) are lower fidelity than replay events during quiet wakefulness (Karlsson and Frank, 2009) supports this possibility. Electrical stimulation of the medial forebrain bundle triggered on a hippocampal place cell’s spikes has recently been shown to drive goal-directed behavior
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