Spike-timing dependent plasticity and the cognitive map

Abstract

Since the discovery of place cells – single pyramidal neurons that encode spatial location – it has been hypothesized that the hippocampus may act as a cognitive map of known environments. This putative function has been extensively modeled using auto-associative networks, which utilize rate-coded synaptic plasticity rules in order to generate strong bi-directional connections between concurrently active place cells that encode for neighboring place fields. However, empirical studies using hippocampal cultures have demonstrated that the magnitude and direction of changes in synaptic strength can also be dictated by the relative timing of pre- and post-synaptic firing according to a spike-timing dependent plasticity (STDP) rule. Furthermore, electrophysiology studies have identified persistent “theta-coded” temporal correlations in place cell activity in vivo, characterized by phase precession of firing as the corresponding place field is traversed. It is not yet clear if STDP and theta-coded neural dynamics are compatible with cognitive map theory and previous rate-coded models of spatial learning in the hippocampus. Here, we demonstrate that an STDP rule based on empirical data obtained from the hippocampus can mediate rate-coded Hebbian learning when pre- and post-synaptic activity is stochastic and has no persistent sequence bias. We subsequently demonstrate that a spiking recurrent neural network that utilizes this STDP rule, alongside theta-coded neural activity, allows the rapid development of a cognitive map during directed or random exploration of an environment of overlapping place fields. Hence, we establish that STDP and phase precession are compatible with rate-coded models of cognitive map development.

Cellular and System Biology of Memory: Timing, Molecules, and Beyond

“…Finally, for hippocampal place cells, it could be shown that the sequence learning of spatial positions is compatible with Hebbian-STPD-LTP on the cellular level (293). Moreover, the rate and timing dependent STDP model fits to results obtained by Bush et al (49) to explain spatial sequence learning of place cells with overlapping place fields.…”

Sharp-Wave Ripples Orchestrate the Induction of Synaptic Plasticity during Reactivation of Place Cell Firing Patterns in the Hippocampus

“…Indeed, we found that SWR-associated synaptic stimulation can powerfully modulate STDP at mature SC-CA1 synapses. These findings demonstrate how the temporal structure of reactivated place cell firing patterns interacts dynamically with network oscillations to sculpt plasticity in the hippocampus, providing important data to inform models of the impact of plasticity’s impact on place cell firing patterns ( Mehta et al., 2000 , Bush et al., 2010b ). Indeed, previous models have demonstrated the importance of bursts of coincident dendritic activity to induce LTP at distal synapses in the absence of strong back-propagating action potentials ( Kumar and Mehta, 2011 ).…”

The Spike-Timing Dependence of Plasticity

“…This shift was observed experimentally by Mehta et al (1999), and was shown to be consistent with both simple Hebbian STDP (Mehta et al, 2000) and with a biophysically inspired, unified model of rate-and timing-dependent plasticity (Yu et al, 2006). Recently, Bush et al (2010) showed that a rate- and timing-dependent plasticity model explains both learning of spatial sequences and increased functional connectivity between neurons with overlapping place fields. Thus, STDP is an appropriate candidate to mediate learning within the hippocampal cognitive map.…”