Abstract
Cortical microcircuits are nonrandomly wired by neurons. As a natural consequence, spikes emitted by microcircuits are also nonrandomly patterned in time and space. One of the prominent spike organizations is a repetition of fixed patterns of spike series across multiple neurons. However, several questions remain unsolved, including how precisely spike sequences repeat, how the sequences are spatially organized, how many neurons participate in sequences, and how different sequences are functionally linked. To address these questions, we monitored spontaneous spikes of hippocampal CA3 neurons ex vivo using a high-speed functional multineuron calcium imaging (fMCI) technique that allowed us to monitor spikes with millisecond resolution and to record the location of spiking and non-spiking neurons. Multineuronal spike sequences (MSSs) were overrepresented in spontaneous activity compared to the statistical chance level. Approximately 75% of neurons participated in at least one sequence during our observation period. The participants were sparsely dispersed and did not show specific spatial organization. The number of sequences relative to the chance level decreased when larger time frames were used to detect sequences. Thus, sequences were precise at the millisecond level. Sequences often shared common spikes with other sequences; parts of sequences were subsequently relayed by following sequences, generating complex chains of multiple sequences.
Highlights
The brain uses a limited number of neurons to process virtually unlimited patterns of information from external environments
HIGH-SPEED IMAGING OF SPIKING CA3 NETWORKS ex vivo Hippocampal slice cultures were incubated in OGB1AM, and OGB1-loaded neurons were imaged from the CA3 stratum pyramidale at 500 Hz using a spinning-disk confocal microscope and a high-speed electron-multiplying charge-coupled device (EM-CCD) camera (Takahashi et al, 2011)
Each video was 130 s in length, and a total of 9 videos were recorded from 9 slices (n = 9 rat pups borned from 9 mothers)
Summary
The brain uses a limited number of neurons to process virtually unlimited patterns of information from external environments. Individual neurons are unlikely to independently process specific information, and it is more plausible that they cooperatively form subgroups that work as functional units This idea, called the “cell assembly” hypothesis (Hebb, 1949; Harris, 2005; Buzsaki, 2010), leads to two important predictions about neuronal circuit operation. The weight is strengthened when the neurons work cooperatively, otherwise it is weakened This bidirectional synaptic plasticity has been experimentally proven by studies showing that cortical synapses are capable of exhibiting long-term potentiation (LTP) and long-term depression (LTD) of synaptic transmission. These two features suggest that neuronal networks self-organize through reorganization of neuronal connectivity due to ongoing external stimuli and are thereby functionally compartmentalized to form cell assemblies. We have demonstrated, by using an optical synapse mapping technique, that in such restored CA3 networks, pyramidal cells are nonrandomly connected to generate diverse repertoires of synchronized activity, like the in vivo conditions (Takahashi et al, 2010)
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