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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 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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Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,478
Oxytocin improves “mind-reading” in humans
Domes, G., Heinrichs, M., Michel, A., Berger, C., & Herpertz, S. C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.07.015 · Cited by 1,298 · cited 6×
“TGOT was simulated by (1) reducing the evoked somatic IPSC conductance to 60% of “baseline”, while sparing the evoked EPSC and the dendritic IPSC, (2) doubling the spontaneous IPSC amplitude, and (3) increasing the spontaneous IPSC rate from 5 Hz to 35 Hz.”
BackgroundMethodInfluentialVerret, L., Mann, E. O., Hang, G. B., Barth, A. M. I., Cobos, I., Ho, K., Devidze, N., Masliah, E., Kreitzer, A. C., Mody, I., et al. (2012) · Cell · doi:10.1016/j.cell.2012.02.046 · Cited by 1,216
A Developmental Switch in the Response of DRG Neurons to ETS Transcription Factor Signaling
Hippenmeyer, S., Pecho‐Vrieseling, E., Sigrist, M., Portmann, T., Laengle, C., Ladle, D. R., & Arber, S. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030159 · Cited by 1,111
Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition
Pouille, F., & Scanziani, M. (2001) · Science · doi:10.1126/science.1060342 · Cited by 1,097
Evoked axonal oxytocin release in the central amygdala attenuates fear response
Knobloch, H. S., Charlet, A., Hoffmann, L. C., Eliava, M., Khrulev, S., Cetin, A. H., Osten, P., Schwarz, M. K., Seeburg, P. H., Stoop, R., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.030 · Cited by 1,049
Oxytocin in the Medial Amygdala is Essential for Social Recognition in the Mouse
Ferguson, J. N., Aldag, J. M., Insel, T. R., & Young, L. J. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08278.2001 · Cited by 1,043 · cited 9×
“TGOT increased the spontaneous firing of presynaptic FSIs and also diminished the FSI-pyramidal cell unitary IPSC, without affecting RS interneurons (Fig 3a,b).”
BackgroundMethodInfluentialIntranasal oxytocin improves emotion recognition for youth with autism spectrum disorders.
Guastella, A. J., Einfeld, S. L., Gray, K. M., Rinehart, N. J., Tonge, B. J., Lambert, T. J., & Hickie, I. B. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.09.020 · Cited by 962
Plasma oxytocin levels in autistic children
Modahl, C., Green, L. A., Fein, D., Morris, M., Waterhouse, L., Feinstein, C., & Levin, H. (1998) · Biological Psychiatry · doi:10.1016/s0006-3223(97)00439-3 · Cited by 728
Instantaneous Modulation of Gamma Oscillation Frequency by Balancing Excitation with Inhibition
Atallah, B. V., & Scanziani, M. (2009) · Neuron · doi:10.1016/j.neuron.2009.04.027 · Cited by 614
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Robertson, C. E., & Baron-Cohen, S. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.112 · Cited by 1,157
The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889
Advancing the understanding of autism disease mechanisms through genetics
de la Torre-Ubieta, L., Won, H., Stein, J. L., & Geschwind, D. H. (2016) · Nature Medicine · doi:10.1038/nm.4071 · Cited by 827
The Neurobiology of Human Attachments
Feldman, R. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.11.007 · Cited by 839
Oxytocin enables maternal behaviour by balancing cortical inhibition
Marlin, B. J., Mitre, M., D’amour, J. A., Chao, M. V., & Froemke, R. C. (2015) · Nature · doi:10.1038/nature14402 · Cited by 744
Oxytocin-Mediated GABA Inhibition During Delivery Attenuates Autism Pathogenesis in Rodent Offspring
Tyzio, R., Nardou, R., Ferrari, D. C., Tsintsadze, T., Shahrokhi, A., Eftekhari, S., Khalilov, I., Tsintsadze, V., Brouchoud, C., Chazal, G., et al. (2014) · Science · doi:10.1126/science.1247190 · Cited by 601
Gating of social reward by oxytocin in the ventral tegmental area
Hung, L. W., Neuner, S., Polepalli, J. S., Beier, K. T., Wright, M., Walsh, J. J., Lewis, E. M., Luo, L., Deisseroth, K., Dölen, G., et al. (2017) · Science · doi:10.1126/science.aan4994 · Cited by 578
Oxytocin, Neural Plasticity, and Social Behavior
Froemke, R. C., & Young, L. J. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102320-102847 · Cited by 480
Amygdala inputs to the ventral hippocampus bidirectionally modulate social behavior
Felix-Ortiz, A. C., & Tye, K. M. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.4257-13.2014 · Cited by 473
“In another study, oxytocin was recently shown to increase the signal-to-noise ratio of CA1 pyramidal neurons in mice in an ex vivo preparation (Owen et al., 2013), providing one possible mechanism underlying the ability of oxytocin to reduce social deficits associated with autism spectrum disorders…”
BackgroundPlasticity of Cortical Excitatory-Inhibitory Balance
Froemke, R. C. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034002 · Cited by 458
The adaptive human parental brain: implications for children's social development
Feldman, R. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.04.004 · Cited by 419
Disinhibition, a Circuit Mechanism for Associative Learning and Memory
Letzkus, J. J., Wolff, S. B. E., & Lüthi, A. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.024 · Cited by 430
Exogenous and evoked oxytocin restores social behavior in the Cntnap2 mouse model of autism
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Walum, H., & Young, L. J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0072-6 · Cited by 353
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Oettl, L.-L., Ravi, N., Schneider, M., Scheller, M. F., Schneider, P., Mitre, M., da Silva Gouveia, M., Froemke, R. C., Chao, M. V., Young, W. S., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.033 · Cited by 359
Feldman, R., Monakhov, M., Pratt, M., & Ebstein, R. P. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.08.008 · Cited by 352
Oxytocin enhances brain function in children with autism
Gordon, I., Vander Wyk, B. C., Bennett, R. H., Cordeaux, C., Lucas, M. V., Eilbott, J. A., Zagoory-Sharon, O., Leckman, J. F., Feldman, R., & Pelphrey, K. A. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1312857110 · Cited by 336
A distributed network for social cognition enriched for oxytocin receptors
Mitre, M., Marlin, B. J., Schiavo, J. K., Morina, E., Norden, S. E., Hackett, T. A., Aoki, C. J., Chao, M. V., & Froemke, R. C. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2409-15.2016 · Cited by 305
“11E,F), similar to the effects of oxytocin receptor agonist application in hippocampal slices (Owen et al., 2013).”
BackgroundResultInfluentialHippocampal oxytocin receptors are necessary for discrimination of social stimuli
Raam, T., McAvoy, K. M., Besnard, A., Veenema, A. H., & Sahay, A. (2017) · Nature Communications · doi:10.1038/s41467-017-02173-0 · Cited by 292
What is resilience: an affiliative neuroscience approach
Feldman, R. (2020) · World Psychiatry · doi:10.1002/wps.20729 · Cited by 324
Insular cortex mediates approach and avoidance responses to social affective stimuli
Rogers-Carter, M. M., Varela, J. A., Gribbons, K. B., Pierce, A. F., McGoey, M. T., Ritchey, M., & Christianson, J. P. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0071-y · Cited by 277
“OT significantly increased EPSP amplitude beginning at 2V with further enhancement during the washout (FSTIMULUS(10, 90) = 598.”
BackgroundNakajima, M., Görlich, A., & Heintz, N. (2014) · Cell · doi:10.1016/j.cell.2014.09.020 · Cited by 262
Evolution of oxytocin pathways in the brain of vertebrates
Knobloch, H. S., & Grinevich, V. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00031 · Cited by 259
“OT is supposed to preferentially act on interneurons (Knobloch et al., 2012; Owen et al., 2013), which, in turn, relatively rapidly (i.e., within the range of seconds) modify the network activity of certain brain region(s), resulting in fast emotional, behavioral or cognitive responses.”
BackgroundPelkey, K. A., Barksdale, E., Craig, M. T., Yuan, X., Sukumaran, M., Vargish, G. A., Mitchell, R. M., Wyeth, M. S., Petralia, R. S., Chittajallu, R., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.020 · Cited by 245
Feldman, R. (2015) · Development and Psychopathology · doi:10.1017/s0954579415000048 · Cited by 271
A Hypothalamic Midbrain Pathway Essential for Driving Maternal Behaviors
Fang, Y., Yamaguchi, T., Song, S. C., Tritsch, N. X., & Lin, D. (2018) · Neuron · doi:10.1016/j.neuron.2018.02.019 · Cited by 274
Johnson, Z. V., & Young, L. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.034 · Cited by 242
The Corticohippocampal Circuit, Synaptic Plasticity, and MemoryPreprint
Basu, J., & Siegelbaum, S. A. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a021733 · Cited by 269
Early somatostatin interneuron connectivity mediates the maturation of deep layer cortical circuits
Tuncdemir, S. N., Wamsley, B., Stam, F. J., Osakada, F., Goulding, M., Callaway, E. M., Rudy, B., & Fishell, G. (2016) · Neuron · doi:10.1016/j.neuron.2015.11.020 · Cited by 224
Prefrontal–amygdala circuits in social decision-making
Gangopadhyay, P., Chawla, M., Monte, O. D., & Chang, S. W. C. (2020) · Nature Neuroscience · doi:10.1038/s41593-020-00738-9 · Cited by 266
Guastella, A. J., & Hickie, I. B. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.028 · Cited by 223
A Cortical Circuit for Sexually Dimorphic Oxytocin-Dependent Anxiety Behaviors
Li, K., Nakajima, M., Ibañez-Tallon, I., & Heintz, N. (2016) · Cell · doi:10.1016/j.cell.2016.08.067 · Cited by 234
Tasks for inhibitory interneurons in intact brain circuits
Roux, L., & Buzsáki, G. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.09.011 · Cited by 218
Tone, E. B., & Tully, E. C. (2014) · Development and Psychopathology · doi:10.1017/s0954579414001199 · Cited by 253
Baribeau, D. A., & Anagnostou, E. A. (2015) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00335 · Cited by 241
“…the balance of excitatory to inhibitory transmission within the circuit was altered, such that the strength and fidelity of firing within the principal cells was increased and made more efficient, effectively enhancing the coordinated signal in the overall network (Owen et al., 2013).”
BackgroundGenetic origins of social networks in rhesus macaques
Brent, L. J. N., Heilbronner, S. R., Horvath, J. E., Gonzalez-Martinez, J., Ruiz-Lambides, A., Robinson, A. G., Skene, J. H. P., & Platt, M. L. (2013) · Scientific Reports · doi:10.1038/srep01042 · Cited by 220
Structural foundations of optogenetics: Determinants of channelrhodopsin ion selectivity
Berndt, A., Lee, S. Y., Wietek, J., Ramakrishnan, C., Steinberg, E. E., Rashid, A. J., Kim, H., Park, S., Santoro, A., Frankland, P. W., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1523341113 · Cited by 214
Ko, J. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00041 · Cited by 229
“It is likely that OXT increases signal-to-noise ratios of target social circuits by improving the temporal precision and fidelity of information transfer and elevating inhibitory tone (Owen et al., 2013; Marlin et al., 2015).”
BackgroundOxytocin signaling in the lateral septum prevents social fear during lactation
Menon, R., Grund, T., Zoicas, I., Althammer, F., Fiedler, D., Biermeier, V., Bosch, O. J., Hiraoka, Y., Nishimori, K., Eliava, M., et al. (2018) · Current Biology · doi:10.1016/j.cub.2018.02.044 · Cited by 211
Oxytocin Signaling in the Central Amygdala Modulates Emotion Discrimination in Mice
Ferretti, V., Maltese, F., Contarini, G., Nigro, M., Bonavia, A., Huang, H., Gigliucci, V., Morelli, G., Scheggia, D., Managò, F., et al. (2019) · Current Biology · doi:10.1016/j.cub.2019.04.070 · Cited by 212
Young, L. J., & Barrett, C. E. (2015) · Science · doi:10.1126/science.aaa8120 · Cited by 200
Li, X., Matsuura, T., Xue, M., Chen, Q., Liu, R., Lu, J.-S., Shi, W., Fan, K., Zhou, Z., Miao, Z., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109411 · Cited by 194
Freeman, S. M., Inoue, K., Smith, A. L., Goodman, M. M., & Young, L. J. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.03.023 · Cited by 185
Neural circuits of social behaviors: Innate yet flexible
Wei, D., Talwar, V., & Lin, D. (2021) · Neuron · doi:10.1016/j.neuron.2021.02.012 · Cited by 199
Developmental Perspectives on Oxytocin and Vasopressin
Hammock, E. A. D. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.120 · Cited by 184
Lin, Y.-T., Hsieh, T.-Y., Tsai, T.-C., Chen, C.-C., Huang, C.-C., & Hsu, K.-S. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.1896-17.2017 · Cited by 165
“Owen et al. (2013) have previously demonstrated that OXT can enhance hippocampal spike transmission in CA1 pyramidal neurons by increasing fast-spiking GABAergic interneuron activity.”
BackgroundNeural mechanisms of social decision-making in the primate amygdala
Chang, S. W. C., Fagan, N. A., Toda, K., Utevsky, A. V., Pearson, J. M., & Platt, M. L. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1514761112 · Cited by 157
Single-cell transcriptomic evidence for dense intracortical neuropeptide networks
Smith, S. J., Sümbül, U., Graybuck, L. T., Collman, F., Seshamani, S., Gala, R., Gliko, O., Elabbady, L., Miller, J. A., Bakken, T. E., et al. (2019) · eLife · doi:10.7554/elife.47889 · Cited by 156
“, 1979) and there 430 certainly is an excellent literature on cortical neuropeptide signaling (Crawley, 1985; Férézou et al., 2007; 431 Gallopin et al., 2006; Gomtsian et al., 2018; Hamilton et al., 2013; Liu et al., 2018; Mena et al., 2013; Mitre 432 et al., 2018; Owen et al., 2013; Rossier and Chapouthier, 1982; Wil…”
BackgroundOxytocin transforms firing mode of CA2 hippocampal neurons
Tirko, N. N., Eyring, K. W., Carcea, I., Mitre, M., Chao, M. V., Froemke, R. C., & Tsien, R. W. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.008 · Cited by 157
“Additionally, OXTR stimulation of CA2 inhibitory neuron firing might dampen the initially strong GABAergic transmission in CA2 (Piskorowski and Chevaleyre, 2013) via activity-dependent synaptic depression (Figure 8H; Owen et al., 2013; Marlin et al., 2015; Oettl et al., 2016).”
InfluentialSmith, C. J. W., Poehlmann, M. L., Li, S., Ratnaseelan, A. M., Bredewold, R., & Veenema, A. H. (2017) · Brain Structure and Function · doi:10.1007/s00429-016-1260-7 · Cited by 143
Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues
Yao, S., Bergan, J., Lanjuin, A., & Dulac, C. (2017) · eLife · doi:10.7554/elife.31373 · Cited by 151
“…documented to increase neuronal firing rates, mainly, though not exclusively in fast-spiking interneurons, resulting in lower background activity and enhanced information transfer in cortical and non-cortical circuits (Owen et al., 2013; Marlin et al., 2015; Oettl et al., 2016; Xiao et al., 2017).”
BackgroundOwen, S. F., Berke, J. D., & Kreitzer, A. C. (2018) · Cell · doi:10.1016/j.cell.2018.01.005 · Cited by 158
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Lin, Y.-T., Chen, C., Huang, C., Nishimori, K., & Hsu, K. (2017) · Nature Communications · doi:10.1038/s41467-017-00675-5 · Cited by 149
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139
Effects of MDMA and intranasal oxytocin on social and emotional processing
Kirkpatrick, M. G., Lee, R., Wardle, M. C., Jacob, S., & de Wit, H. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.12 · Cited by 143
Interplay between Oxytocin and Sensory Systems in the Orchestration of Socio-Emotional Behaviors
Grinevich, V., & Stoop, R. (2018) · Neuron · doi:10.1016/j.neuron.2018.07.016 · Cited by 139
“A C1 C2 AON piriform cortex MC MC GC OSN = OTR expression B CA1 CA3 entorhinal cortex + oxytocin = GABA Figure 4 B Auditory system IC Aud Ctx MG DC Tz SOc inner year IO A Visual system SC LGThalamus Visual cortex pigment epitheliumretina Figure 3 trigeminal ganglion SpTN STN Somatosensory system SS Ctx PAG Cg Ctx NTS…”
InfluentialNeural Circuits for Social Cognition: Implications for Autism
Fernández, M. C., Mollinedo-Gajate, I., & Peñagarikano, O. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.07.013 · Cited by 143
Cortical variability in the sensory-evoked response in autism
Haigh, S. M., Heeger, D. J., Dinstein, I., Minshew, N., & Behrmann, M. (2015) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-014-2276-6 · Cited by 113
Oxytocin mediates entrainment of sensory stimuli to social cues of opposing valence
Choe, H. K., Reed, M. D., Benavidez, N., Montgomery, D., Soares, N., Yim, Y. S., & Choi, G. B. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.022 · Cited by 124
Is birth a critical period in the pathogenesis of autism spectrum disorders?
Ben-Ari, Y. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3956 · Cited by 117
Valeeva, G. R., Tressard, T., Mukhtarov, M. R., Baude, A., & Khazipov, R. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3482-15.2016 · Cited by 121
“…in the generation of cortical rhythms (Stark et al., 2013; Schlingoff et al., 2014), signal processing (Atallah et al., 2012; Lee et al., 2012; Lovett-Barron et al., 2012; Owen et al., 2013; Sachidhanandam et al., 2013), and control of epileptic discharges (Ledri et al., 2014; Ladas et al., 2015).”
BackgroundHammock, E. A. D. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00195 · Cited by 115
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Johnson, Z. V., Walum, H., Xiao, Y., Riefkohl, P. C., & Young, L. J. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.009 · Cited by 113
Gordon, I., Jack, A., Pretzsch, C. M., Vander Wyk, B., Leckman, J. F., Feldman, R., & Pelphrey, K. A. (2016) · Scientific Reports · doi:10.1038/srep35054 · Cited by 114
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Social Decision-Making and the Brain: A Comparative Perspective
Tremblay, S., Sharika, K. M., & Platt, M. L. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.01.007 · Cited by 116
Herman, A. M., Huang, L., Murphey, D. K., Garcia, I., & Arenkiel, B. R. (2014) · eLife · doi:10.7554/elife.01481 · Cited by 104
Priel, A., Djalovski, A., Zagoory‐Sharon, O., & Feldman, R. (2018) · Journal of Child Psychology and Psychiatry · doi:10.1111/jcpp.12880 · Cited by 106
From Autism to Eating Disorders and More: The Role of Oxytocin in Neuropsychiatric Disorders
Romano, A., Tempesta, B., Bonaventura, M. V. M. D., & Gaetani, S. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2015.00497 · Cited by 106
Molecular Mechanisms of Oxytocin Signaling at the Synaptic Connection
Bakos, J., Srancikova, A., Havranek, T., & Bacova, Z. (2018) · Neural Plasticity · doi:10.1155/2018/4864107 · Cited by 104
“This conclusion is supported by other studies in different brain areas: the auditory cortex, piriform cortex, hypothalamus, and hippocampus [51, 52].”
BackgroundResultLin, Y.-T., & Hsu, K. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.10.003 · Cited by 102
Oxytocin and Parental Behaviors
Yoshihara, C., Numan, M., & Kuroda, K. O. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_11 · Cited by 104
Insular function in autism: Update and future directions in neuroimaging and interventions
Nomi, J. S., Molnar-Szakacs, I., & Uddin, L. Q. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.10.015 · Cited by 98
Adaptations for social cognition in the primate brain
Platt, M. L., Seyfarth, R. M., & Cheney, D. L. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0096 · Cited by 95
“For example, OT applied to hippocampus in rats enhances signal-to-noise ratio of neurons by increasing spike probability while simultaneously decreasing spontaneous background activity [129], potentially providing a foundation for enhanced learning and memory.”
BackgroundOxytocin and vasopressin in the rodent hippocampus
Cilz, N. I., Cymerblit‐Sabba, A., & Young, W. S. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12535 · Cited by 92
Stoop, R. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.09.012 · Cited by 84
Beery, A. K., McEwen, L. M., MacIsaac, J. L., Francis, D. D., & Kobor, M. S. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.022 · Cited by 81
Lonstein, J. S., Maguire, J. L., Meinlschmidt, G., & Neumann, I. D. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12188 · Cited by 89
Transient oxytocin signaling primes the development and function of excitatory hippocampal neurons
Ripamonti, S., Ambrozkiewicz, M. C., Guzzi, F., Gravati, M., Biella, G. R., Bormuth, I., Hammer, M., Tuffy, L. P., Sigler, A., Kawabe, H., et al. (2017) · eLife · doi:10.7554/elife.22466 · Cited by 84
“…publications reporting that, in rat, Oxt acutely activates interneurons located in the stratum pyramidale and modulates fast-spiking interneurons, thus enhancing inhibitory synaptic transmission in the hippocampus (Mühlethaler et al., 1984, 1983; Owen et al., 2013; Zaninetti and Raggenbass, 2000).”
BackgroundResultOxytocin normalizes altered circuit connectivity for social rescue of the Cntnap2 knockout mouse
Choe, K. Y., Bethlehem, R. A. I., Safrin, M., Dong, H., Salman, E., Li, Y., Grinevich, V., Golshani, P., DeNardo, L. A., Peñagarikano, O., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.11.031 · Cited by 81
Neuroscience: The hard science of oxytocin
Shen, H. H. (2015) · Nature · doi:10.1038/522410a · Cited by 80
GABAergic interneurons: The orchestra or the conductor in fear learning and memory?
Lucas, E. K., & Clem, R. L. (2017) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2017.11.016 · Cited by 80
“Nevertheless, it is now clear that, similar to excitatory PNs, inhibitory interneurons exhibit diverse forms of synaptic potentiation and depression in response to artificial stimulation (Cohen et al., 2016; Huang et al., 2013; Mahanty and Sah, 1998; Owen et al., 2013; Pelkey et al., 2005; Woodin et al., 2003), raisin…”
BackgroundOxytocin Modulation of Neural Circuits
Mitre, M., Minder, J. L., Morina, E., Chao, M. V., & Froemke, R. C. (2017) · Current topics in behavioral neurosciences · doi:10.1007/7854_2017_7 · Cited by 79
CA2 beyond social memory: Evidence for a fundamental role in hippocampal information processing
Lehr, A. B., Kumar, A., Tetzlaff, C., Hafting, T., Fyhn, M., & Stöber, T. M. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.03.020 · Cited by 84
“In both regions, oxytocin receptor activation increases their excitability (Owen et al., 2013; Tirko et al., 2018).”
Olazábal, D. E., & Alsina‐Llanes, M. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.04.006 · Cited by 72
Oxytocin promotes prefrontal population activity via the PVN-PFC pathway to regulate pain
Liu, Y., Li, A., Bair-Marshall, C. J., Xu, H. Z., Jee, H. J., Zhu, E., Sun, M., Zhang, Q., Lefèvre, A., Chen, Z. S., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.03.014 · Cited by 77
Control of response reliability by parvalbumin-expressing interneurons in visual cortex
Zhu, Y., Qiao, W., Liu, K., Zhong, H., & Yao, H. (2015) · Nature Communications · doi:10.1038/ncomms7802 · Cited by 72
Oxytocin and Serotonin Brain Mechanisms in the Nonhuman Primate
Lefèvre, A., Richard, N., Jazayeri, M., Beuriat, P.-A., Fieux, S., Zimmer, L., Duhamel, J., & Sirigu, A. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0659-17.2017 · Cited by 73
“Moreover, amygdala, hippocampus, and prefrontal cortex have also been found to be influenced by OT in experiments on rodents (Viviani et al., 2011; Knobloch et al., 2012; Owen et al., 2013; Nakajima et al., 2014).”
BackgroundAssociation of Social Support With Brain Volume and Cognition
Salinas, J., O’Donnell, A., Kojis, D. J., Pase, M. P., DeCarli, C. S., Rentz, D. M., Berkman, L. F., Beiser, A., & Seshadri, S. S. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.21122 · Cited by 76
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66
“OTR and V1aR are classic neuromodulators, mediating both 490 short- and long-term changes in neural and hence behavioral out491 comes (Owen et al., 2013).”
Oxytocin and Rodent Models of Addiction
Leong, K.-C., Cox, S. S., King, C. E., Becker, H. C., & Reichel, C. M. (2018) · International review of neurobiology · doi:10.1016/bs.irn.2018.07.007 · Cited by 72
Zebrafish oxytocin neurons drive nocifensive behavior via brainstem premotor targets
Wee, C. L., Nikitchenko, M., Wang, W., Luks-Morgan, S. J., Song, E. Y., Gagnon, J. A., Randlett, O., Bianco, I. H., Lacoste, A. M. B., Glushenkova, E., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0452-x · Cited by 69
Oxytocin: Parallel Processing in the Social Brain?
Dölen, G. (2015) · Journal of Neuroendocrinology · doi:10.1111/jne.12284 · Cited by 65
Lesse, A., Rether, K., Gröger, N., Braun, K., & Bock, J. (2016) · Molecular Neurobiology · doi:10.1007/s12035-016-0043-8 · Cited by 66
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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