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Heterogeneity and independency of unitary synaptic outputs from hippocampal CA3 pyramidal cells
Author(s) -
Sasaki Takuya,
Matsuki Norio,
Ikegaya Yuji
Publication year - 2012
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jphysiol.2012.237685
Subject(s) - hippocampal formation , neuroscience , pyramidal cell , hippocampus , unitary state , chemistry , biology , political science , law
Key points• Excitatory neurotransmission in the cortex is a local event that occurs at chemical synaptic junctions, but it has not been experimentally addressed at the large network scale. • Here we show that trial‐to‐trial variability in the synaptic transmission at hippocampal synapses is attributable to fluctuations in calcium elevations in axonal boutons, rather than to changes in the action potential waveform in axons. • Multiple patch‐clamp recordings from synaptically connected neural circuits revealed no correlation between synaptic outputs to two different postsynaptic cells from a common presynaptic cell. • This independency of synapses was likely to arise from unique calcium dynamics within presynaptic terminals.Abstract The variation of individual synaptic transmission impacts the dynamics of complex neural circuits. We performed whole‐cell recordings from monosynaptically connected hippocampal neurons in rat organotypic slice cultures using a synapse mapping method. The amplitude of unitary excitatory postsynaptic current (uEPSC) varied from trial to trial and was independent of the physical distance between cell pairs. To investigate the source of the transmission variability, we obtained patch‐clamp recordings from intact axons. Axonal action potentials (APs) were reliably transmitted throughout the axonal arbour and showed modest changes in width. In contrast, calcium imaging from presynaptic boutons revealed that the amplitude of AP‐evoked calcium transients exhibited large variations both among different boutons at a given trial and among trials in a given bouton. These results suggest that a factor contributing to the uEPSC fluctuations is the variability in calcium dynamics at presynaptic terminals. Finally, we acquired triple whole‐cell recordings from divergent circuit motifs with one presynaptic neuron projecting to two postsynaptic neurons. Consistent with the independency of calcium dynamics among axonal boutons, a series of uEPSC fluctuations was not correlated between the two postsynaptic cells, indicating that different synapses even from the same neuron act independently. We conclude that the intra‐bouton and inter‐bouton variability in AP‐induced calcium dynamics determine the heterogeneity and independency of uEPSCs.