Circuit topology for synchronizing neurons in spontaneously active networks.
Spike synchronization underlies information processing and storage in the brain. But how can neurons synchronize in a noisy network? By exploiting a high-speed (500-2,000 fps) multineuron imaging technique and a large-scale synapse mapping method, we directly compared spontaneous activity patterns and anatomical connectivity in hippocampal CA3 networks ex vivo. As compared to unconnected pairs, synaptically coupled neurons shared more common presynaptic neurons, received more correlated excitatory synaptic inputs, and emitted synchronized spikes with approximately 10(7) times higher probability. Importantly, common presynaptic parents per se synchronized more than unshared upstream neurons. Consistent with this, dynamic-clamp stimulation revealed that common inputs alone could not account for the realistic degree of synchronization unless presynaptic spikes synchronized among common parents. On a macroscopic scale, network activity was coordinated by a power-law scaling of synchronization, which engaged varying sets of densely interwired (thus highly synchronized) neuron groups. Thus, locally coherent activity converges on specific cell assemblies, thereby yielding complex ensemble dynamics. These segmentally synchronized pulse packets may serve as information modules that flow in associatively parallel network channels.
Takahashi
Naoya
N
Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo 113-0033, Japan.
Sasaki
Takuya
T
Matsumoto
Wataru
W
Matsuki
Norio
N
Ikegaya
Yuji
Y
D000200:Action Potentials; D000818:Animals; D001931:Brain Mapping / Q000379:methods; D056547:CA1 Region, Hippocampal / Q000166:cytology / Q000502:physiology; D056654:CA3 Region, Hippocampal / Q000166:cytology / Q000502:physiology; D020013:Calcium Signaling; D055724:Electrophysiological Phenomena; D019706:Excitatory Postsynaptic Potentials; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials; D008959:Models, Neurological; D009415:Nerve Net / Q000166:cytology / Q000502:physiology*; D009474:Neurons / Q000502:physiology; D018408:Patch-Clamp Techniques; D051381:Rats; D017208:Rats, Wistar