Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons

Scott F. Owen, Sebnem N. Tuncdemir, Patrick L. Bader, Natasha N. Tirko, Gordon Fishell, Richard W. Tsien

Research output: Contribution to journalArticle

Abstract

Neuromodulatory control by oxytocin is essential to a wide range of social, parental and stress-related behaviours. Autism spectrum disorders (ASD) are associated with deficiencies in oxytocin levels and with genetic alterations of the oxytocin receptor (OXTR). Thirty years ago, Mühlethaler et al. found that oxytocin increases the firing of inhibitory hippocampal neurons, but it remains unclear how elevated inhibition could account for the ability of oxytocin to improve information processing in the brain. Here we describe in mammalian hippocampus a simple yet powerful mechanism by which oxytocin enhances cortical information transfer while simultaneously lowering background activity, thus greatly improving the signal-to-noise ratio. Increased fast-spiking interneuron activity not only suppresses spontaneous pyramidal cell firing, but also enhances the fidelity of spike transmission and sharpens spike timing. Use-dependent depression at the fast-spiking interneuron-pyramidal cell synapse is both necessary and sufficient for the enhanced spike throughput. We show the generality of this novel circuit mechanism by activation of fast-spiking interneurons with cholecystokinin or channelrhodopsin-2. This provides insight into how a diffusely delivered neuromodulator can improve the performance of neural circuitry that requires synapse specificity and millisecond precision.

Original languageEnglish (US)
Pages (from-to)458-462
Number of pages5
JournalNature
Volume500
Issue number7463
DOIs
StatePublished - Aug 8 2013

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Interneurons
Oxytocin
Pyramidal Cells
Synapses
Oxytocin Receptors
Aptitude
Cholecystokinin
Signal-To-Noise Ratio
Automatic Data Processing
Neurotransmitter Agents
Hippocampus
Depression
Neurons
Brain

ASJC Scopus subject areas

  • General

Cite this

Owen, S. F., Tuncdemir, S. N., Bader, P. L., Tirko, N. N., Fishell, G., & Tsien, R. W. (2013). Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. Nature, 500(7463), 458-462. https://doi.org/10.1038/nature12330

Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. / Owen, Scott F.; Tuncdemir, Sebnem N.; Bader, Patrick L.; Tirko, Natasha N.; Fishell, Gordon; Tsien, Richard W.

In: Nature, Vol. 500, No. 7463, 08.08.2013, p. 458-462.

Research output: Contribution to journalArticle

Owen, SF, Tuncdemir, SN, Bader, PL, Tirko, NN, Fishell, G & Tsien, RW 2013, 'Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons', Nature, vol. 500, no. 7463, pp. 458-462. https://doi.org/10.1038/nature12330
Owen, Scott F. ; Tuncdemir, Sebnem N. ; Bader, Patrick L. ; Tirko, Natasha N. ; Fishell, Gordon ; Tsien, Richard W. / Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons. In: Nature. 2013 ; Vol. 500, No. 7463. pp. 458-462.
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