Abstract
Reverse replay of hippocampal place cells occurs frequently at rewarded locations, suggesting its contribution to goal-directed path learning. Symmetric spike-timing dependent plasticity (STDP) in CA3 likely potentiates recurrent synapses for both forward (start to goal) and reverse (goal to start) replays during sequential activation of place cells. However, how reverse replay selectively strengthens forward synaptic pathway is unclear. Here, we show computationally that firing sequences bias synaptic transmissions to the opposite direction of propagation under symmetric STDP in the co-presence of short-term synaptic depression or afterdepolarization. We demonstrate that significant biases are created in biologically realistic simulation settings, and this bias enables reverse replay to enhance goal-directed spatial memory on a W-maze. Further, we show that essentially the same mechanism works in a two-dimensional open field. Our model for the first time provides the mechanistic account for the way reverse replay contributes to hippocampal sequence learning for reward-seeking spatial navigation.
Highlights
The hippocampus plays an important role in episodic memory and spatial processing in the brain (O’Keefe and Dostrovsky, 1971; Scoville and Milner, 1957)
The network consists of 500 rate neurons, which were connected with distance-dependent excitatory synaptic weights modulated by short-term synaptic plasticity (STP) (Romani and Tsodyks, 2015; Wang et al, 2015)
We showed that the modified Hebbian plasticity rule modulated by STP biases synaptic weights toward the reverse direction of the firing sequences that traveled through a recurrent network
Summary
The hippocampus plays an important role in episodic memory and spatial processing in the brain (O’Keefe and Dostrovsky, 1971; Scoville and Milner, 1957). Reward-based optimization requires selective reinforcement of forward pathways as it will strengthen prospective place-cell sequences in subsequent trials and forward replay events in the consolidation phase Such bias toward forward sequences in post-experience sleep (Wikenheiser and Redish, 2013) and goaldirected behavior (Johnson and Redish, 2007; Pfeiffer and Foster, 2013; Wikenheiser and Redish, 2015) is observed in hippocampus. By simulating the model with various spiking patterns, we confirm this effect for a broad range of spiking patterns and parameters of plasticity rules, including those observed in experiments Based on this mechanism, we built a two-dimensional recurrent network model of place cells with the combination of reverse replay, Hebbian plasticity with short-term plasticity, and reward-induced enhancement of replay frequency (Ambrose et al, 2016; Singer and Frank, 2009). Unlike the previous models for hippocampal sequence learning (Blum and Abbott, 1996; Gerstner and Abbott, 1997; Jahnke et al, 2015; Jensen and Lisman, 1996; Sato and Yamaguchi, 2003; Tsodyks and Sejnowski, 1995) in which recurrent networks learn and strengthen forward sequences through forward movements, our model proposes goal-directed path learning through reverse sequences
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