Abstract
The hippocampal network produces sequences of neural activity even when there is no time-varying external drive. In offline states, the temporal sequence in which place cells fire spikes correlates with the sequence of their place fields. Recent experiments found this correlation even between offline sequential activity (OSA) recorded before the animal ran in a novel environment and the place fields in that environment. This preplay phenomenon suggests that OSA is generated intrinsically in the hippocampal network, and not established by external sensory inputs. Previous studies showed that continuous attractor networks with asymmetric patterns of connectivity, or with slow, local negative feedback, can generate sequential activity. This mechanism could account for preplay if the network only represented a single spatial map, or chart. However, global remapping in the hippocampus implies that multiple charts are represented simultaneously in the hippocampal network and it remains unknown whether the network with multiple charts can account for preplay. Here we show that it can. Driven with random inputs, the model generates sequences in every chart. Place fields in a given chart and OSA generated by the network are highly correlated. We also find significant correlations, albeit less frequently, even when the OSA is correlated with a new chart in which place fields are randomly scattered. These correlations arise from random correlations between the orderings of place fields in the new chart and those in a pre-existing chart. Our results suggest two different accounts for preplay. Either an existing chart is re-used to represent a novel environment or a new chart is formed.
Highlights
While we know since patient HM that the human hippocampus is involved in the formation and consoldation of episodic memories (Scoville and Milner, 1957), the neural mechanisms underlying these processes are still not understood
We first examined the properties of the bump attractor in a continuous attractor neural network (CANN) that stores multiple charts with the adaptation currents Ji removed from the network dynamics in Equation 1
We showed that a continuous attractor neural network with spike frequency adaptation that includes multiple spatial maps, or charts, can intrinsically generate sequential activity and account for preplay
Summary
While we know since patient HM that the human hippocampus is involved in the formation and consoldation of episodic memories (Scoville and Milner, 1957), the neural mechanisms underlying these processes are still not understood. One promising candidate for a mechanism underlying consolidation is the reactivation of neural activity patterns during sleep and awake quiescent states (offline states) (McClelland et al, 1995). Since replay events are accompanied by sharp wave/ripple (SWR) events in the hippocampal local field potential (LFP), it is possible to detect SWR and electrically stimulate the hippocampus to suppress replay activity. When this protocol was applied during sleep (Girardeau et al, 2009) or the awake state (Jadhav et al, 2012), rats showed significant impairments on spatial memory tasks
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