Distinct Neuronal Coding Schemes in Memory Revealed by Selective Erasure of Fast Synchronous Synaptic Transmission

Wei Xu, Wade Morishita, Paul S. Buckmaster, Zhiping Pang, Robert C. Malenka, Thomas C. Südhof

Research output: Contribution to journalArticle

102 Citations (Scopus)

Abstract

Neurons encode information by firing spikes in isolation or bursts and propagate information by spike-triggered neurotransmitter release that initiates synaptic transmission. Isolated spikes trigger neurotransmitter release unreliably but with high temporal precision. In contrast, bursts of spikes trigger neurotransmission reliably (i.e., boost transmission fidelity), but the resulting synaptic responses are temporally imprecise. However, the relative physiological importance of different spike-firing modes remains unclear. Here, we show that knockdown of synaptotagmin-1, the major Ca 2+ sensor for neurotransmitter release, abrogated neurotransmission evoked by isolated spikes but only delayed, without abolishing, neurotransmission evoked by bursts of spikes. Nevertheless, knockdown of synaptotagmin-1 in the hippocampal CA1 region did not impede acquisition of recent contextual fear memories, although it did impair the precision of such memories. In contrast, knockdown of synaptotagmin-1 in the prefrontal cortex impaired all remote fear memories. These results indicate that different brain circuits and types of memory employ distinct spike-coding schemes to encode and transmit information. Xu et al. selectively erase fast, synchronous synaptic transmission in vivo, thereby blocking information transfer of isolated spikes, but not of bursts of spikes. This approach reveals distinct coding schemes in memory circuits, with spike bursts sufficient for hippocampal encoding of memories.

Original languageEnglish (US)
Pages (from-to)990-1001
Number of pages12
JournalNeuron
Volume73
Issue number5
DOIs
StatePublished - Mar 8 2012
Externally publishedYes

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Synaptic Transmission
Synaptotagmin I
Neurotransmitter Agents
Fear
Hippocampal CA1 Region
Long-Term Memory
Prefrontal Cortex
Neurons
Brain

All Science Journal Classification (ASJC) codes

  • Neuroscience(all)

Cite this

Xu, Wei ; Morishita, Wade ; Buckmaster, Paul S. ; Pang, Zhiping ; Malenka, Robert C. ; Südhof, Thomas C. / Distinct Neuronal Coding Schemes in Memory Revealed by Selective Erasure of Fast Synchronous Synaptic Transmission. In: Neuron. 2012 ; Vol. 73, No. 5. pp. 990-1001.
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Distinct Neuronal Coding Schemes in Memory Revealed by Selective Erasure of Fast Synchronous Synaptic Transmission. / Xu, Wei; Morishita, Wade; Buckmaster, Paul S.; Pang, Zhiping; Malenka, Robert C.; Südhof, Thomas C.

In: Neuron, Vol. 73, No. 5, 08.03.2012, p. 990-1001.

Research output: Contribution to journalArticle

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