Oxytocin functions as a spatiotemporal filter for excitatory synaptic inputs to VTA dopamine neurons

Xiao, Lei; Priest, Michael F; Kozorovitskiy, Yevgenia

doi:10.7554/elife.33892

Cited by 83Neurotransmitter Receptor Influence on BehaviorNeuroendocrine regulation and behaviorNeuroscience and Neuropharmacology Research

Oxytocin functions as a spatiotemporal filter for excitatory synaptic inputs to VTA dopamine neurons

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Xiao, Lei, Priest, Michael F, Kozorovitskiy, Yevgenia·2018·eLife

DOI 10.7554/elife.33892PMC PMC5910020

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Abstract

The experience of rewarding or aversive stimuli is encoded by distinct afferents to dopamine (DA) neurons of the ventral tegmental area (VTA). Several neuromodulatory systems including oxytocin regulate DA neuron excitability and synaptic transmission that process socially meaningful stimuli. We and others have recently characterized oxytocinergic modulation of activity in mouse VTA DA neurons, but the mechanisms underlying oxytocinergic modulation of synaptic transmission in DA neurons remain poorly understood. Here, we find that oxytocin application or optogenetic release decrease excitatory synaptic transmission, via long lasting, presynaptic, endocannabinoid-dependent mechanisms. Oxytocin modulation of excitatory transmission alters the magnitude of short and long-term depression. We find that only some glutamatergic projections to DA neurons express CB1 receptors. Optogenetic stimulation of three major VTA inputs demonstrates that oxytocin modulation is limited to projections that show evidence of CB1R transcripts. Thus, oxytocin gates information flow into reward circuits in a temporally selective and pathway-specific manner.

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Oxytocin enhances social reward.
“Oxytocin promotes maternal nurturing and bonding, enhances social reward, and increases the salience of social stimuli.”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [83]
Paraventricular oxytocin can facilitate social reward through its actions on brain dopamine systems originating in the ventral tegmental area and through endocannabinoid-dependent mechanisms.
“PVN OXT can also facilitate social reward through its actions on brain dopamine systems (82), originating, for example, in the ventral tegmental area (VTA), and through endocannabinoid-dependent mechanisms (83).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [83]

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“Endocannabinoid signaling is suggested to be neuroprotective across multiple brain regions, including the hippocampus and midbrain dopamine regions (Melis and Pistis, 2007; Xu and Chen, 2015).”
Background
Synaptic plasticity in the mesolimbic dopamine system
Thomas, M. J., & Malenka, R. C. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1236 · Cited by 137 · see citing works
Synaptic plasticity in the mesolimbic system
Chen, B. T., Hopf, F. W., & Bonci, A. (2010) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.05154.x · Cited by 128 · cited 2× · see citing works
“…transmission Synaptic plasticity of glutamatergic transmission in VTA DA neurons provides a critical substrate relevant to learning and addiction (Chen et al., 2010; Kauer and Malenka, 2007; Niehaus et al., 2009), and endocannabinoids play a pivotal role in synaptic plasticity by depressing…”
Background
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 · cited 2× · see citing works
“Oxytocin is one of the two major neurohypophyseal peptides that function centrally as a neuromodulator and has been linked to the processing of socially rewarding stimuli via actions in the stria- tum and in the neocortex (Choe et al., 2015; Dölen et al., 2013; Marlin et al., 2015).”
Background
Oxytocin action in the ventral tegmental area affects sucrose intake
Mullis, K., Kay, K., & Williams, D. L. (2013) · Brain Research · doi:10.1016/j.brainres.2013.03.026 · Cited by 122 · cited 2× · see citing works
“Consistent with oxytocin-driven enhancement in the activity of VTA DA neurons, oxytocin infusions into the VTA potentiate social reward (Song et al., 2016) and modulate reward- based behavior (Mullis et al., 2013).”
Background
Input- and Cell-Type-Specific Endocannabinoid-Dependent LTD in the Striatum
Wu, Y., Kim, J., Tawfik, V. L., Lalchandani, R. R., Scherrer, G., & Ding, J. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.12.005 · Cited by 117 · cited 20× · see citing works
“In a subset of experiments LTD was induced using 1 s long periods of 100 Hz stimulation, repeated 4 times with 10 second-long inter-train intervals (Kreitzer and Malenka, 2005).”
BackgroundInfluential
Oxytocin-receptor-expressing neurons in the parabrachial nucleus regulate fluid intake
Ryan, P. J., Ross, S. I., Campos, C., Derkach, V. A., & Palmiter, R. D. (2017) · Nature Neuroscience · doi:10.1038/s41593-017-0014-z · Cited by 113 · cited 3× · see citing works
“Depth-matched z-stacks of 1 mm-thick optical sections were analyzed in ImageJ (FIJI) (Schindelin et al., 2012).”
MethodInfluential
Oxytocin suppresses basal glutamatergic transmission but facilitates activity-dependent synaptic potentiation in the medial prefrontal cortex
Ninan, I. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07430.x · Cited by 110 · cited 2× · see citing works
“, 2013), and in the mPFC, oxytocin application dampens glutamatergic synaptic transmission through presynaptic endocannabinoid signaling (Ninan, 2011).”
Background
Activation of oxytocin receptors, but not arginine-vasopressin V1a receptors, in the ventral tegmental area of male Syrian hamsters is essential for the reward-like properties of social interactions
Song, Z., Borland, J. M., Larkin, T. E., O’Malley, M., & Albers, H. E. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2016.09.001 · Cited by 101 · cited 1× · see citing works
“…in reward-based behavior (Howe and Dombeck, 2016; Russo and Nestler, 2013; Schultz, 1998), drug abuse and addiction (Jones and Bonci, 2005; Kauer and Malenka, 2007; Niehaus et al., 2009; Stelly et al., 2016), as well as neurodevelopmental and neurodegenerative disorders (Dichter et al., 2012).”
Background
Phasic dopamine signals: from subjective reward value to formal economic utility
Schultz, W., Carelli, R. M., & Wightman, R. M. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.09.006 · Cited by 88 · cited 2× · see citing works
“…clinical implications, given the involvement of midbrain DA regions in reward-based behavior (Howe and Dombeck, 2016; Russo and Nestler, 2013; Schultz, 1998), drug abuse and addiction (Jones and Bonci, 2005; Kauer and Malenka, 2007; Niehaus et al., 2009; Stelly et al., 2016), as well as…”
Background
Oxytocin modulates GABAAR subunits to confer neuroprotection in stroke in vitro
Kaneko, Y., Pappas, C. A., Tajiri, N., & Borlongan, C. V. (2016) · Scientific Reports · doi:10.1038/srep35659 · Cited by 88 · cited 2× · see citing works
“Given the vast literature on the neuroprotective properties of oxytocin (Ceanga et al., 2010; Kaneko et al., 2016; Tyzio et al., 2006) and the broad expression of oxytocin receptors throughout the vertebrate brain (Mitre et al., 2016), the therapeutic potential of developing oxytocin…”
Background
An Increase in AMPA and a Decrease in SK Conductance Increase Burst Firing by Different Mechanisms in a Model of a Dopamine Neuron In Vivo
Canavier, C. C., & Landry, R. S. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00704.2006 · Cited by 69 · see citing works
Inhibition of phospholipase A2 and phospholipase C by polyamines
Sechi, A. M., Cabrini, L., Landi, L., Pasquali, P., & Lenaz, G. (1978) · Archives of Biochemistry and Biophysics · doi:10.1016/0003-9861(78)90433-2 · Cited by 69 · cited 1× · see citing works
“1(cre)Dolsn/J mice (Oxti-Cre, #024234), which express the enzyme Cre recombinase under control of the oxytocin promoter (Shah et al., 2014), were used to target oxytocinergic neurons in PVN. Slc17a6tm2(cre)Lowl/J mice (Slc17a6i-Cre, # 016963), which express Cre recombinase under the control of…”
Method
Neuromodulation of excitatory synaptogenesis in striatal development
Kozorovitskiy, Y., Peixoto, R. T., Wang, W., Saunders, A. B., & Sabatini, B. L. (2015) · eLife · doi:10.7554/elife.10111 · Cited by 69 · cited 2× · see citing works
“We used a version of Scanimage to control scanning parameters and image acquisition (Kozorovitskiy et al., 2015; Pologruto et al., 2003).”
Method
Oxytocin activation of neurons in ventral tegmental area and interfascicular nucleus of mouse midbrain
Tang, Y., Chen, Z., Tao, H., Li, C., Zhang, X., Tang, A., & Liu, Y. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.10.004 · Cited by 68 · cited 1× · see citing works
“To determine the identify and function of endocannabinoids in oxytocinergic modulation of synaptic transmission in VTA DA neurons, we blocked the 2-AG synthesizing enzyme DAG lipase a (DGLa) with orlistat (THL) (Gantz and Bean, 2017; Tanimura et al., 2010).”
Method
Visualization of Oxytocin Release that Mediates Paired Pulse Facilitation in Hypothalamic Pathways to Brainstem Autonomic Neurons
Piñol, R. A., Jameson, H. S., Popratiloff, A. S., Lee, N. H., & Mendelowitz, D. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112138 · Cited by 67 · cited 1× · see citing works
“PLC cleaves phosphatidylinositol 1,4,5-bisphosphate into diacylglycerol (DAG) and inositol 1,4,5-trisphosphate; DAG is subsequently converted into 2-AG by DAG lipase (Di Marzo et al., 1998; Piomelli, 2003).”
Background
Oxytocin is neuroprotective against oxygen–glucose deprivation and reoxygenation in immature hippocampal cultures
Ceangă, M., Spataru, A., & Zăgrean, A. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.04.024 · Cited by 66 · cited 2× · see citing works
“Given the vast literature on the neuroprotective properties of oxytocin (Ceanga et al., 2010; Kaneko et al., 2016; Tyzio et al., 2006) and the broad expression of oxytocin receptors throughout the vertebrate brain (Mitre et al., 2016), the therapeutic potential of developing oxytocin…”
Background
Afferent-Specific AMPA Receptor Subunit Composition and Regulation of Synaptic Plasticity in Midbrain Dopamine Neurons by Abused Drugs
Good, C. H., & Lupica, C. R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1507-10.2010 · Cited by 60 · see citing works
Activation of Pedunculopontine Glutamate Neurons Is Reinforcing
Yoo, J. H., Zell, V., Wu, J., Punta, C., Ramajayam, N., Shen, X., Faget, L. C., Lilascharoen, V., Lim, B. K., & Hnasko, T. S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3082-16.2016 · Cited by 59 · cited 1× · see citing works
“Meanwhile, mPFC glutamatergic afferents increase VTA activity and may promote the development of addiction (Gariano and Groves, 1988; Wu et al., 2013), and pedunculopontine glutamatergic afferents to VTA DA neurons drive motivated behavior (Yoo et al., 2017).”
Background
Cell-Autonomous Excitation of Midbrain Dopamine Neurons by Endocannabinoid-Dependent Lipid Signaling
Gantz, S. C., & Bean, B. P. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.025 · Cited by 59 · cited 9× · see citing works
“Drugs were applied by bath perfusion: oxytocin (10 nM - 1 mM), L368,899 hydrochloride (10 mM), U73122 (10 mM), SR49059 (10 mM), CP945598 hydrochloride (10 mM), WIN55212-2 (5 mM), AM251 (5 mM), orlistat (THL, 5 mM)), MNI-L-glutamate (2.5 mM), SR95531 hydrobromide (10 mM), NBQX (10 mM), and CPP (10 mM).”
BackgroundMethodInfluential
Vasopressin receptors in the mouse (Mus musculus) brain: sex-related expression in the medial preoptic area and hypothalamus
Dubois-Dauphin, M., Barberis, C., & de Bilbao, F. (1996) · Brain Research · doi:10.1016/s0006-8993(96)01019-0 · Cited by 57 · cited 1× · see citing works
“Indeed, vasopressin 1a receptor (V1aR) transcripts are present in the rodent VTA, including in DA neurons (Dubois-Dauphin et al., 1996; Xiao et al. eLife 2018;7:e33892.”
Background
Synaptic Plasticity onto Dopamine Neurons Shapes Fear Learning
Pignatelli, M., Umanah, G. K. E., Ribeiro, S. P., Chen, R., Karuppagounder, S. S., Yau, H., Eacker, S. M., Dawson, V. L., Dawson, T. M., & Bonci, A. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.030 · Cited by 54 · see citing works
Endocannabinoid Signaling in Midbrain Dopamine Neurons: More than Physiology?
Melis, M., & Pistis, M. (2007) · Current Neuropharmacology · doi:10.2174/157015907782793612 · Cited by 53 · cited 1× · see citing works
“Endocannabinoid signaling is suggested to be neuroprotective across multiple brain regions, including the hippocampus and midbrain dopamine regions (Melis and Pistis, 2007; Xu and Chen, 2015).”
Background
Ventral tegmental area dopamine and GABA neurons: Physiological properties and expression of mRNA for endocannabinoid biosynthetic elements
Merrill, C. B., Friend, L. N., Newton, S. T., Hopkins, Z. H., & Edwards, J. G. (2015) · Scientific Reports · doi:10.1038/srep16176 · Cited by 49 · cited 2× · see citing works
“The two major mammalian endocannabinoids are the bioactive lipid 2-arachidonoylglycerol (2AG) and anandamide, and previous evidence suggests that 2-AG is a primary endocannabinoid synthesized and released by VTA DA neurons (Gantz and Bean, 2017; Mátyás et al., 2008; Merrill et al., 2015).”
Background
Repeated social defeat stress enhances glutamatergic synaptic plasticity in the VTA and cocaine place conditioning
Stelly, C. E., Pomrenze, M. B., Cook, J. B., & Morikawa, H. (2016) · eLife · doi:10.7554/elife.15448 · Cited by 49 · cited 2× · see citing works
“OxtRs primarily couple to Gaq protein effectors, which activate the phospholipase C (PLC) pathway to mobilize intracellular Ca2+ store release (Gimpl and Fahrenholz, 2001; Stoop, 2012).”
Background
Polyamines inhibit phospholipase C-catalysed polyphosphoinositide hydrolysis. Studies with permeabilized GH3 cells
Wojcikiewicz, R. J. H., & Fain, J. N. (1988) · Biochemical Journal · doi:10.1042/bj2551015 · Cited by 47 · cited 1× · see citing works
“However, spermine can modulate and inhibit the PLC cascade (Sechi et al., 1978; Wojcikiewicz and Fain, 1988) which is downstream of the OxtR.”
Background
Spermine and Arcaine Block and Permeate N-Methyl-d-Aspartate Receptor Channels
Araneda, R. C., Lan, J.-Y., Zheng, X., Zukin, R. S., & Bennett, M. V. L. (1999) · Biophysical Journal · doi:10.1016/s0006-3495(99)77445-x · Cited by 44 · cited 2× · see citing works
“Additionally, Hung et al. include spermine in their recording pipette solution, presumably in order to intracellularly block NMDARs (Araneda et al., 1999) for tight pharmacological control important when recording EPSCs and IPSCs from the same neurons.”
Background
Properties of distinct ventral tegmental area synapses activated via pedunculopontine or ventral tegmental area stimulationin vitro
Good, C. H., & Lupica, C. R. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.164194 · Cited by 44 · see citing works
Plasticity of Addiction: A Mesolimbic Dopamine Short‐Circuit?
Niehaus, J. L., Cruz‐Bermúdez, N. D., & Kauer, J. A. (2009) · The American Journal on Addictions · doi:10.1080/10550490902925946 · Cited by 42 · cited 3× · see citing works
“…in reward-based behavior (Howe and Dombeck, 2016; Russo and Nestler, 2013; Schultz, 1998), drug abuse and addiction (Jones and Bonci, 2005; Kauer and Malenka, 2007; Niehaus et al., 2009; Stelly et al., 2016), as well as neurodevelopmental and neurodegenerative disorders (Dichter et al., 2012).”
Background
Cortical control of VTA function and influence on nicotine reward
Wu, J., Gao, M., Shen, J.-X., Shi, W., Oster, A. M., & Gutkin, B. S. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.013 · Cited by 40 · cited 1× · see citing works
“Meanwhile, mPFC glutamatergic afferents increase VTA activity and may promote the development of addiction (Gariano and Groves, 1988; Wu et al., 2013), and pedunculopontine glutamatergic afferents to VTA DA neurons drive motivated behavior (Yoo et al., 2017).”
Background
Synaptic Neurotransmission Depression in Ventral Tegmental Dopamine Neurons and Cannabinoid-Associated Addictive Learning
Liu, Z., Han, J., Jia, L., Maillet, J., Bai, G., Xu, L., Jia, Z., Zheng, Q., Zhang, W., Monette, R., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015634 · Cited by 32 · cited 2× · see citing works
“VTA DA LTD has been implicated in addiction, fear learning, satiety, and aversion behaviors (Labouèbe et al., 2013; Liu et al., 2010; Pignatelli et al., 2017; Thomas and Malenka, 2003).”
Background

Flagged first, then by citations

Sorted by citations

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 487 · see citing works
“An additional level of input selection and control of circuit function in mouse VTA is provided by oxytocinergic downregulation of excitation via presynaptic endocannabinoid receptors (Xiao et al. 2018).”
Background
Wireless multilateral devices for optogenetic studies of individual and social behaviors
Yang, Y., Wu, M., Vázquez‐Guardado, A., Wegener, A. J., Grajales‐Reyes, J. G., Deng, Y., Wang, T., Avila, R. O., Moreno, J. A., Minkowicz, S., et al. (2021) · Nature Neuroscience · doi:10.1038/s41593-021-00849-x · Cited by 214 · see citing works
Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities
Rigney, N., de Vries, G. J., Petrulis, A., & Young, L. J. (2022) · Endocrinology · doi:10.1210/endocr/bqac111 · Cited by 191 · see citing works
A near-infrared genetically encoded calcium indicator for in vivo imaging
Shemetov, A. A., Monakhov, M. V., Zhang, Q., Canton-Josh, J. E., Kumar, M., Chen, M., Matlashov, M. E., Li, X., Yang, W., Nie, L., et al. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0710-1 · Cited by 142 · see citing works
“Coronal 250 μm cortical brain slices were made using a Leica VT1200s vibratome, as previously described 46, 47 .”
Detection, processing and reinforcement of social cues: regulation by the oxytocin system
Menon, R., & Neumann, I. D. (2023) · Nature Reviews Neuroscience · doi:10.1038/s41583-023-00759-w · Cited by 100 · see citing works
“…VTA dopaminergic neurons 29 , electrophysiological evidence has shown that OXT simultaneously dampens the excitatory input to the VTA from other sources, such as the medial prefrontal cortex and the pedunculopon-tine nucleus, via an endocannabinoid signalling-mediated presynaptic mechanism 39 .”
Background
Role of oxytocin in the control of stress and food intake
Onaka, T., & Takayanagi, Y. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12700 · Cited by 98 · see citing works
Oxytocin receptor signaling in the hippocampus: Role in regulating neuronal excitability, network oscillatory activity, synaptic plasticity and social memory
Lin, Y.-T., & Hsu, K. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.10.003 · Cited by 97 · see citing works
Dopamine pathways mediating affective state transitions after sleep loss
Wu, M., Zhang, X., Feng, S., Freda, S. N., Kumari, P., Dumrongprechachan, V., & Kozorovitskiy, Y. (2023) · Neuron · doi:10.1016/j.neuron.2023.10.002 · Cited by 90 · see citing works
Cell-type and subcellular compartment-specific APEX2 proximity labeling reveals activity-dependent nuclear proteome dynamics in the striatum
Dumrongprechachan, V., Salisbury, R. B., Soto, G., Kumar, M., MacDonald, M. L., & Kozorovitskiy, Y. (2021) · Nature Communications · doi:10.1038/s41467-021-25144-y · Cited by 85 · see citing works
A fluorescent sensor for real-time measurement of extracellular oxytocin dynamics in the brain
Ino, D., Tanaka, Y., Hibino, H., & Nishiyama, M. (2022) · Nature Methods · doi:10.1038/s41592-022-01597-x · Cited by 84 · see citing works
Wireless, battery-free, subdermally implantable platforms for transcranial and long-range optogenetics in freely moving animals
Ausra, J., Wu, M., Zhang, X., Vázquez‐Guardado, A., Skelton, P. D., Peralta, R., Avila, R. O., Murickan, T., Haney, C. R., Huang, Y. Y., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2025775118 · Cited by 76 · see citing works
“A-31573, RRID: AB_2536183), and washing three times in PBS as described in previous publications (50 – 53).”
Method
The role of oxytocin and vasopressin dysfunction in cognitive impairment and mental disorders
Abramova, O. V., Zorkina, Y., Ushakova, V. M., Zubkov, E. A., Morozova, A. Y., & Chekhonin, V. P. (2020) · Neuropeptides · doi:10.1016/j.npep.2020.102079 · Cited by 74 · see citing works
D1 receptor-expressing neurons in ventral tegmental area alleviate mouse anxiety-like behaviors via glutamatergic projection to lateral septum
Tong, Q., Cui, X., Xu, H., Zhang, X., Hu, S., Huang, F., & Xiao, L. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01809-y · Cited by 62 · see citing works
“Quantitative fluorescence single molecule in situ hybridization (smFISH) smFISH was conducted following previously published procedures [43, 44].”
Neuromodulation of maternal circuits by oxytocin
Valtcheva, S., & Froemke, R. C. (2019) · Cell and Tissue Research · doi:10.1007/s00441-018-2883-1 · Cited by 54 · see citing works
“Actions of central oxytocin are fast, on the order of seconds to minutes (Dölen et al. 2013; Hung et al. 2017; Knobloch et al. 2012; Mitre et al. 2016; Ninan 2011; Oettl et al. 2016; Owen et al. 2013; Tang et al. 2014; Xiao et al. 2018; Xiao et al. 2017).”
Morpho-Electric Properties and Diversity of Oxytocin Neurons in Paraventricular Nucleus of Hypothalamus in Female and Male Mice
Chen, S., Xu, H., Dong, S., & Xiao, L. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.2494-21.2022 · Cited by 58 · see citing works
“Acute brain sections were prepared from male and female Oxt-Cre: Ai3 mice (postnatal 85-97 days) as previously described (Xiao et al., 2017, 2018).”
Method
Oxytocin and Food Intake Control: Neural, Behavioral, and Signaling Mechanisms
Liu, C. M., Spaulding, M. O., Rea, J. J., Noble, E. E., & Kanoski, S. E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910859 · Cited by 53 · see citing works
Oxytocin and excitation/inhibition balance in social recognition
Lopatina, O. L., Komleva, Y. K., Gorina, Y. V., Olovyannikova, R. Y., Труфанова, Л. В., Hashimoto, T., Takahashi, T., Kikuchi, M., Minabe, Y., Higashida, H., et al. (2018) · Neuropeptides · doi:10.1016/j.npep.2018.09.003 · Cited by 51 · see citing works
Attenuated dopamine signaling after aversive learning is restored by ketamine to rescue escape actions
Wu, M., Minkowicz, S., Dumrongprechachan, V., Hamilton, P., Xiao, L., & Kozorovitskiy, Y. (2021) · eLife · doi:10.7554/elife.64041 · Cited by 53 · see citing works
“Quantitative fluorescence in situ hybridization (FISH) was conducted following previously published procedures ( Xiao et al., 2018 ; Xiao et al., 2017 ).”
Influential
Pathway-specific dysregulation of striatal excitatory synapses by LRRK2 mutations
Chen, C., Soto, G., Dumrongprechachan, V., Bannon, N. M., Kang, S., Kozorovitskiy, Y., & Parisiadou, L. (2020) · eLife · doi:10.7554/elife.58997 · Cited by 48 · see citing works
“(species) or resource Designation Source or reference Identifiers Additional information Chemical compound, drug Tris Buffered Saline (10x) Sigma-Aldrich T5912 Chemical compound, drug TWEEN 20 Sigma-Aldrich P1379 Chemical compound, drug MNI-L-glutamate Tocris 1490 Chemical compound, drug Alexa Fluor 594 Thermo Fisher…”
Method
Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles
Borie, A. M., Agezo, S., Lunsford, P., Boender, A. J., Guo, J.-D., Zhu, H., Berman, G. J., Young, L. J., & Liu, R. C. (2022) · Current Biology · doi:10.1016/j.cub.2022.01.014 · Cited by 39 · see citing works
Neural circuit control of innate behaviors
Wei, X., Jiao, Z., Senol, E., Yao, J., Zhao, M., Zhao, Z., Chen, X., Cao, P., Fu, Y., Gao, Z., et al. (2021) · Science China Life Sciences · doi:10.1007/s11427-021-2043-2 · Cited by 38 · see citing works
“Oxytocin plays a critical role in linking social signals to the mesocorticolimbic dopamine reinforcement system (Xiao et al., 2018).”
Background
Ginsenoside Rg1 enriches gut microbial indole-3-acetic acid to alleviate depression-like behavior in mice via oxytocin signaling
Yu, S., Yin, Z., Ling, M., Chen, Z., Zhang, Y., Pan, Y., Zhang, Y., Cai, X., Chen, Z., Hao, H., et al. (2024) · Phytomedicine · doi:10.1016/j.phymed.2024.156186 · Cited by 36 · see citing works
What can we learn from PWS and SNORD116 genes about the pathophysiology of addictive disorders?
Salles, J., Lacassagne, E., Eddiry, S., Franchitto, N., Salles, J., & Tauber, M. (2020) · Molecular Psychiatry · doi:10.1038/s41380-020-00917-x · Cited by 36 · see citing works
NTS and VTA oxytocin reduces food motivation and food seeking
Wald, H. S., Chandra, A., Kalluri, A. L., Ong, Z. Y., Hayes, M. R., & Grill, H. J. (2020) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00201.2020 · Cited by 34 · see citing works
In the face of stress: Interpreting individual differences in stress-induced facial expressions
Mayo, L. M., & Heilig, M. A. (2019) · Neurobiology of Stress · doi:10.1016/j.ynstr.2019.100166 · Cited by 33 · see citing works
“Oxytocin appears to gate social behavior via interactions with dopamine (Hung et al., 2017), a finding which has recently been extended to include modulation via CB1 receptor activity (Xiao et al., 2018).”
Romantic love evolved by co-opting mother-infant bonding
Bode, A. (2023) · Frontiers in Psychology · doi:10.3389/fpsyg.2023.1176067 · Cited by 31 · see citing works
“Evidence from rodents suggest that activation of oxytocin receptors in the VTA is probably critical for the rewarding and reinforcing properties of social interaction (see Hung et al., 2017; Borland et al., 2018; Xiao et al., 2018).”
Background
Oxytocin and Addiction: Potential Glutamatergic Mechanisms
Sundar, M., Patel, D., Young, Z., & Leong, K.-C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052405 · Cited by 29 · see citing works
“Similarly, glutamatergic synaptic transmission in the NAc was dampened in the presence of OXT through a presynaptic mechanism involving serotonergic inputs [9].”
BackgroundInfluential
Peptidergic and functional delineation of the Edinger-Westphal nucleus
Priest, M. F., Freda, S. N., Rieth, I. J., Badong, D., Dumrongprechachan, V., & Kozorovitskiy, Y. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112992 · Cited by 36 · see citing works
“Cartpt transcript was frequently so abundant that individual puncta could not be observed at this or higher magnification levels; a conservative checkerboard counting system was used, 82 assuming that the fluorescence signals from puncta were approximately 2 pixels (1.248 μm) in diameter.”
Influential
Central oxytocin signaling inhibits food reward-motivated behaviors and VTA dopamine responses to food-predictive cues in male rats
Liu, C. M., Hsu, T. M., Suarez, A. N., Subramanian, K. S., Fatemi, R. A., Cortella, A. M., Noble, E. E., Roitman, M. F., & Kanoski, S. E. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104855 · Cited by 28 · see citing works
Oxytocin modulates neurocomputational mechanisms underlying prosocial reinforcement learning
Martins, D., Lockwood, P. L., Cutler, J., Moran, R., & Paloyelis, Y. (2022) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2022.102253 · Cited by 28 · see citing works
Actions of feeding-related peptides on the mesolimbic dopamine system in regulation of natural and drug rewards
Dunigan, A. I., & Roseberry, A. G. (2022) · Addiction Neuroscience · doi:10.1016/j.addicn.2022.100011 · Cited by 28 · see citing works
Identification of the significant pathways of Banxia Houpu decoction in the treatment of depression based on network pharmacology
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Background
Additional file 2 of Activation of oxytocin receptors in mouse GABAergic amacrine cells modulates retinal dopaminergic signaling
Hu, S., Wang, Y., Han, X., Dai, M., Zhang, Y., Ma, Y., Weng, S., & Xiao, L. (2022) · Figshare · doi:10.6084/m9.figshare.21175657
Additional file 1 of Activation of oxytocin receptors in mouse GABAergic amacrine cells modulates retinal dopaminergic signaling
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Authors: Xiao, L., Priest, M. F., & Kozorovitskiy, Y.
Affiliations: Northwestern University (US)
Corresponding author: Kozorovitskiy, Yevgenia
ORCID: Xiao, Lei
Priest, Michael F
Kozorovitskiy, Yevgenia
Venue: eLife
Publisher: eLife Sciences Publications, Ltd
Published: 2018-04-20
Volume: 7
ISSN: 2050-084X (ISSN-L)
DOI: 10.7554/elife.33892
PMC: PMC5910020
OpenAlex: W2799430681
Cited by: 83
References: 86
Citations by year: 2026: 6 · 2025: 9 · 2024: 8 · 2023: 13 · 2022: 16 · 2021: 13 · 2020: 10 · 2019: 5 · 2018: 3
FWCI: 3.53
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
creativecommons.org/licenses/by/4.0/ (am)
creativecommons.org/licenses/by/4.0/ (tdm)
Locations: eLife (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Arnold and Mabel Beckman Foundation (Arnold O. Beckman Postdoctoral Fellowship, BYI Award)
William and Bernice E Bumpus Foundation (Young Innovator Award)
Rita Allen Foundation (Scholar Award)
Alfred P. Sloan Foundation (Research Fellowship)
Kinship Foundation (Searle Scholar Award)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: oxytocin, ventral tegmental area, dopaminergic neurons, excitatory synaptic transmission, endocannabinoid signaling, CB1 receptor, presynaptic modulation, synaptic depression, glutamatergic projections, reward systems, aversive stimuli, neuromodulation
MeSH terms: Animals, Mice, Inbred C57BL, Synaptic Transmission, Oxytocics, Oxytocin, Synapses, Ventral Tegmental Area, Disease Transmission, Infectious, Dopaminergic Neurons, Optogenetics

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Oxytocin functions as a spatiotemporal filter for excitatory synaptic inputs to VTA dopamine neurons

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