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Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons
Open accessAbstract
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.
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In the citing paper
“In contrast to hippocampal CA2, oxytocin does not depolarize CA1 pyramidal cells but instead activates parvalbumin-positive fast-spiking interneurons”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Owen et al. 2013
Experimental — accuracy not yet measuredIn the citing paper
“OTR and V1aR are classic neuromodulators, mediating both short- and long-term changes in neural and hence behavioral outcomes (Owen et al., 2013).”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Owen et al., 2013
In the citing paper
“Oxytocin is thought to modulate neural activity by affecting the excitatory/inhibitory balance and also seems to improve the signal-to-noise ration by stimulating fast spiking parvalbumin inter-neuron activity (Owen et al. 2013).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Owen et al. 2013
In the citing paper
“Together with recent findings showing that OT can increase processing efficiency at the neuronal level by optimizing signal-to-noise during cell firing43”
From Intranasal oxytocin enhances connectivity in the neural circuitry supporting social motivation and social perception in children with autism (2016) · cites this paper as [43]
In the citing paper
“these results show that in ASD, OT may not only serve to enhance neural activity to “preferred” stimuli, but also improve communication among brain regions involved in social motivation and perception.”
From Intranasal oxytocin enhances connectivity in the neural circuitry supporting social motivation and social perception in children with autism (2016) · cites this paper as [43]
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Citations
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“demonstrated that OT activates feedforward fast-spiking parvalbumin (PV) interneurons which 1) suppresses CA1 pyramidal cell firing and 2) enhances information transfer from the PV interneurons to pyramidal cells(Owen et al., 2013).”
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“Approaches to noise reduction include the use of oxytocin (Owen et al., 2013); oxytocin is lower in autism (Modahl et al., 1998;Wuet al., 2005), and oxytocin-related treatments for autism are on the rise (Kuehn, 2011; Modi and Young, 2012; Gordon et al., 2013).”
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“Furthermore, neuromodulation of PV INs is mediated by oxytocin, which increases PV IN firing rate through GABAA receptors (Owen et al., 2013) and by D4-dopamine receptors that enhances the CA3 SC input-driven from CA1 to mediate PV FFI upon PNs to suppress SC pathway output (Rosen et al.”
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“Oxytocin can increase the firing of inhibitory PV+ hippocampal interneurons and enhance spike transmission in hippocampal pyramidal neurons through the modulation of fast-spiking interneurons [85].”
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New therapeutic options for autism spectrum disorder: experimental evidences
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Sex-Specific Differences in Oxytocin Receptor Expression and Function for Parental Behavior
Mitre, M., Kranz, T. M., Marlin, B. J., Schiavo, J. K., Erdjument‐Bromage, H., Zhang, X., Minder, J. L., Neubert, T. A., Hackett, T. A., Chao, M. V., et al. (2017) · Gender and the Genome · doi:10.1089/gg.2017.0017 · Cited by 22
Sexual Activity and Cognitive Decline in Older Adults
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“This result is consistent with reports that OTR activation increases inhibitory transmission in the hippocampus (Harden and Frazier 2016; Owen et al. 2013; Zaninetti and Raggenbass 2000), the auditory and piriform cortices (Mitre et al. 2016), the hypothalamic paraventricular nucleus (Mitre et al.…”
BackgroundResultPark, C., Chen, X., Tian, C.-L., Park, G. N., Chenouard, N., Lee, H., Yeo, X. Y., Jung, S., Tsien, R. W., Bi, G., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2022133118 · Cited by 23
Evidence for cognitive plasticity during pregnancy via enhanced learning and memory
Callaghan, B. L., McCormack, C. A., Tottenham, N., & Monk, C. E. (2022) · Memory · doi:10.1080/09658211.2021.2019280 · Cited by 25
“Notably, hormones involved in pregnancy have been shown to affect hippocampal long-term potentiation (LTP), and modulate fast spiking interneurons in the hippocampus (Owen et al., 2013), both of which are critical physiological functions involved in learning and memory.”
BackgroundBrief synaptic inhibition persistently interrupts firing of fast-spiking interneurons
Chamberland, S., Nebet, E. R., Valero, M., Hanani, M., Egger, R., Larsen, S. B., Eyring, K. W., Buzsáki, G., & Tsien, R. W. (2023) · Neuron · doi:10.1016/j.neuron.2023.01.017 · Cited by 25
“This disinhibitory scenario complements a distinct mechanism wherein spontaneous firing of PV-INs acts over many seconds to fatigue GABAergic synapses and thus weaken feedforward inhibition.(62,98) The common feature is an interplay between slow neuromodulators and fast GABAergic transmission that causes a net disinhi…”
Oxytocin excites BNST interneurons and inhibits BNST output neurons to the central amygdala
Francesconi, W., Berton, F., Olivera-Pasilio, V., & Dabrowska, J. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108601 · Cited by 22
GABAergic microcircuitry of fear memory encoding
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Parvalbumin interneuron cell-to-network plasticity: mechanisms and therapeutic avenues
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Oxytocin decreases colonic motility of cold water stressed ratsviaoxytocin receptors
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Interaction effects of oxytocin receptor gene polymorphism and depression on hippocampal volume
Na, K., Won, E., Kang, J. C., Kim, A., Choi, S.-Y., Kim, Y., Lee, M.-S., & Ham, B. (2018) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2018.10.004 · Cited by 20
Epigenetic tuning of brain signal entropy in emergent human social behavior
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The neurobiology of parenting and infant-evoked aggression
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Oxytocin enhances neural approach towards social and non-social stimuli of high personal relevance
Alaerts, K., Taillieu, A., Daniëls, N., Soriano, J. R., & Prinsen, J. (2021) · Scientific Reports · doi:10.1038/s41598-021-02914-8 · Cited by 21
Oxytocin and vasopressin in the hippocampus
Zăgrean, A., Georgescu, I.-A., Ieșanu, M. I., Ionescu, R.-B., Haret, R. M., Panaitescu, A. M., & Zăgrean, L. (2022) · Vitamins and hormones · doi:10.1016/bs.vh.2021.11.002 · Cited by 20
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Oxytocin in dorsal hippocampus facilitates auditory fear memory extinction in rats
Bazaz, A., Ghanbari, A., Vafaei, A. A., Khaleghian, A., & Rashidy‐Pour, A. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108844 · Cited by 19
Metadata
- Authors
- Owen, S. F., Tuncdemir, S. N., Bader, P. L., Tirko, N. N., Fishell, G., & Tsien, R. W.
- Affiliations
- Stanford Medicine (US)
- New York University (US)
- Corresponding author
- Tsien, Richard W.
- Venue
- Nature
- Published
- 2013-08
- Volume
- 500
- Issue
- 7463
- Pages
- 458-462
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5283693
- OpenAlex
- W2008069212
- Cited by
- 339
- References
- 36
- Citations by year
- 2026: 8 · 2025: 16 · 2024: 21 · 2023: 26 · 2022: 22 · 2021: 28 · 2020: 21 · 2019: 23 · 2018: 35 · 2017: 35 · 2016: 33 · 2015: 37 · 2014: 26 · 2013: 7
- FWCI
- 51.39
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- National Institute of Mental Health (F31MH084430, MH071739, MH064070, R01MH071739, R37MH071739)
- National Institute of Neurological Disorders and Stroke (NS024067, R01NS024067, R01NS074785)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- oxytocin, hippocampus, fast-spiking interneurons, signal-to-noise ratio, neuromodulation, synaptic depression, pyramidal neurons, cholecystokinin, channelrhodopsin-2, autism spectrum disorder, oxytocin receptor, inhibitory interneurons
- MeSH terms
- Action Potentials, Animals, Brain, Cholecystokinin, Glycine, Hippocampus, Interneurons, Neural Pathways, Synaptic Transmission, Oxytocin, Rhodopsin, Synapses, Threonine, Pyramidal Cells, Receptors, Oxytocin, Excitatory Postsynaptic Potentials, Feedback, Physiological, Mice, Rats
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