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 a...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2010-06, Vol.107 (22), p.10244-10249
Main Authors: Takahashi, Naoya, Sasaki, Takuya, Matsumoto, Wataru, Matsuki, Norio, Ikegaya, Yuji
Format: Article
Language:English
Subjects:
Action Potentials
Animals
Behavioral neuroscience
Biological Sciences
Brain
Brain Mapping - methods
CA1 Region, Hippocampal - cytology
CA1 Region, Hippocampal - physiology
CA3 Region, Hippocampal - cytology
CA3 Region, Hippocampal - physiology
Calcium
Calcium Signaling
Comparative analysis
Connectivity
Correlation coefficients
Electrophysiological Phenomena
Excitatory Postsynaptic Potentials
In Vitro Techniques
Inhibitory Postsynaptic Potentials
Interneurons
Kolmogorov Smirnov test
Medical imaging
Models, Neurological
Nerve Net - cytology
Nerve Net - physiology
Neurology
Neurons
Neurons - physiology
Neuroscience
Patch-Clamp Techniques
Rats
Rats, Wistar
Synapses
Topology
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Summary: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 10⁷ 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.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0914594107