Propagation of specific network patterns through the mouse hippocampus

Abstract

Network oscillations bind neurons into transient assemblies with coherent activity, enabling temporal coding. In the mammalian hippocampus, spatial relationships are represented by sequences of action potentials of place cells. Such patterns are established during memory acquisition and are re-played during sharp wave-ripple complexes in CA1 in subsequent sleep episodes. These events originate in CA3 and travel towards CA1 and downstream cortical areas. It is unclear, however, whether specific sequences of ripple-associated firing are solely defined within the CA1 network or whether these patterns are directly entrained by preceding activities of neurons within CA3. Using a model of sharp wave-ripple oscillations (SPW-R) in mouse hippocampal slices we analyzed the propagation of these signals between CA3 and CA1. We found tight coupling between high-frequency network activity in CA3 and CA1. Propagation of ripples through the hippocampal loop maintained precise temporal relationships at the network and cellular level, as indicated by coupling of field potentials, multiunit and single cell activity between major portions of CA3 and CA1. Moreover, SPW-R-like activity in CA1 could be elicited by electrical stimulation within area CA3 while antidromic activation of CA1 failed to induce organized high-frequency oscillations. Our data show that the specificity of neuronal assemblies is maintained with cell-to-cell precision while SPW-R propagate along the hippocampal loop.