Oxytocin promotes prefrontal population activity via the PVN-PFC pathway to regulate pain

Salzman, 2010, Emotion, cognition, and mental state representation in amygdala and prefrontal cortex, Annu. Rev. Neurosci., 33, 173, 10.1146/annurev.neuro.051508.135256 Dale, 2018, Scaling up cortical control inhibits pain, Cell Rep., 23, 1301, 10.1016/j.celrep.2018.03.139 Hardy, 1985, Analgesia elicited by prefrontal stimulation, Brain Res., 339, 281, 10.1016/0006-8993(85)90093-9 Kiritoshi, 2016, Rescue of impaired mGluR5-driven endocannabinoid signaling restores prefrontal cortical output to inhibit pain in arthritic rats, J. Neurosci., 36, 837, 10.1523/JNEUROSCI.4047-15.2016 Lee, 2015, Activation of corticostriatal circuitry relieves chronic neuropathic pain, J. Neurosci., 35, 5247, 10.1523/JNEUROSCI.3494-14.2015 Martinez, 2017, Corticostriatal regulation of acute pain, Front. Cell. Neurosci., 11, 146, 10.3389/fncel.2017.00146 Talay, 2021, Pharmacological restoration of anti-nociceptive functions in the prefrontal cortex relieves chronic pain, Prog. Neurobiol., 201, 102001, 10.1016/j.pneurobio.2021.102001 Zhang, 2015, Role of prelimbic GABAergic circuits in sensory and emotional aspects of neuropathic pain, Cell Rep., 12, 752, 10.1016/j.celrep.2015.07.001 Li, 2021, Disrupted population coding in the prefrontal cortex underlies pain aversion, Cell Rep., 37, 109978, 10.1016/j.celrep.2021.109978 Ji, 2011, Pain-related deactivation of medial prefrontal cortical neurons involves mGluR1 and GABA(A) receptors, J. Neurophysiol., 106, 2642, 10.1152/jn.00461.2011 Kelly, 2016, Reduced glutamatergic currents and dendritic branching of Layer 5 pyramidal cells contribute to medial prefrontal cortex deactivation in a rat model of neuropathic pain, Front. Cell. Neurosci., 10, 133, 10.3389/fncel.2016.00133 Radzicki, 2017, Loss of M1 receptor dependent cholinergic excitation contributes to mPFC deactivation in neuropathic pain, J. Neurosci., 37, 2292, 10.1523/JNEUROSCI.1553-16.2017 Cheriyan, 2018, Altered excitability and local connectivity of mPFC-PAG neurons in a mouse model of neuropathic pain, J. Neurosci., 38, 4829, 10.1523/JNEUROSCI.2731-17.2018 Huang, 2019, A neuronal circuit for activating descending modulation of neuropathic pain, Nat. Neurosci., 22, 1659, 10.1038/s41593-019-0481-5 Ji, 2014, CB1 augments mGluR5 function in medial prefrontal cortical neurons to inhibit amygdala hyperactivity in an arthritis pain model, Eur. J. Neurosci., 39, 455, 10.1111/ejn.12432 Zhou, 2018, Inhibition of the prefrontal projection to the nucleus accumbens enhances pain sensitivity and affect, Front. Cell. Neurosci., 12, 240, 10.3389/fncel.2018.00240 Gimpl, 2001, The oxytocin receptor system: structure, function, and regulation, Physiol. Rev., 81, 629, 10.1152/physrev.2001.81.2.629 Marlin, 2015, Oxytocin enables maternal behaviour by balancing cortical inhibition, Nature, 520, 499, 10.1038/nature14402 Nishimori, 1996, Oxytocin is required for nursing but is not essential for parturition or reproductive behavior, Proc. Natl. Acad. Sci. USA, 93, 11699, 10.1073/pnas.93.21.11699 Pedersen, 1979, Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin, Proc. Natl. Acad. Sci. USA, 76, 6661, 10.1073/pnas.76.12.6661 Hasan, 2019, A fear memory engram and its plasticity in the hypothalamic oxytocin system, Neuron, 103, 133, 10.1016/j.neuron.2019.04.029 Knobloch, 2012, Evoked axonal oxytocin release in the central amygdala attenuates fear response, Neuron, 73, 553, 10.1016/j.neuron.2011.11.030 Neumann, 2012, Balance of brain oxytocin and vasopressin: implications for anxiety, depression, and social behaviors, Trends Neurosci., 35, 649, 10.1016/j.tins.2012.08.004 Landgraf, 2004, Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication, Front. Neuroendocrinol., 25, 150, 10.1016/j.yfrne.2004.05.001 Sofroniew, 1983, Morphology of vasopressin and oxytocin neurones and their central and vascular projections, Prog. Brain Res., 60, 101, 10.1016/S0079-6123(08)64378-2 Swanson, 1983, Hypothalamic integration: organization of the paraventricular and supraoptic nuclei, Annu. Rev. Neurosci., 6, 269, 10.1146/annurev.ne.06.030183.001413 Grinevich, 2016, Assembling the puzzle: pathways of oxytocin signaling in the brain, Biol. Psychiatry, 79, 155, 10.1016/j.biopsych.2015.04.013 Nakajima, 2014, Oxytocin modulates female sociosexual behavior through a specific class of prefrontal cortical interneurons, Cell, 159, 295, 10.1016/j.cell.2014.09.020 Eliava, 2016, A new population of parvocellular oxytocin neurons controlling magnocellular neuron activity and inflammatory pain processing, Neuron, 89, 1291, 10.1016/j.neuron.2016.01.041 Jo, 1998, Oxytocin modulates glutamatergic synaptic transmission between cultured neonatal spinal cord dorsal horn neurons, J. Neurosci., 18, 2377, 10.1523/JNEUROSCI.18-07-02377.1998 Juif, 2013, Long-lasting spinal oxytocin analgesia is ensured by the stimulation of allopregnanolone synthesis which potentiates GABA(A) receptor-mediated synaptic inhibition, J. Neurosci., 33, 16617, 10.1523/JNEUROSCI.3084-12.2013 Schoenen, 1985, Substance P, enkephalins, somatostatin, cholecystokinin, oxytocin, and vasopressin in human spinal cord, Neurology, 35, 881, 10.1212/WNL.35.6.881 Swanson, 1979, The distribution of oxytocin- and neurophysin-stained fibers in the spinal cord of the rat and monkey, J. Comp. Neurol., 188, 87, 10.1002/cne.901880108 Condés-Lara, 2015, Hypothalamic paraventricular nucleus stimulation enhances c-Fos expression in spinal and supraspinal structures related to pain modulation, Neurosci. Res., 98, 59, 10.1016/j.neures.2015.04.004 Huber, 2005, Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala, Science, 308, 245, 10.1126/science.1105636 Yang, 2011, Oxytocin in the periaqueductal grey regulates nociception in the rat, Regul. Pept., 169, 39, 10.1016/j.regpep.2011.04.007 Campbell, 2009, Central vasopressin and oxytocin receptor distributions in two species of singing mice, J. Comp. Neurol., 516, 321, 10.1002/cne.22116 Vargas-Martínez, 2014, Neuropeptides as neuroprotective agents: oxytocin a forefront developmental player in the mammalian brain, Prog. Neurobiol., 123, 37, 10.1016/j.pneurobio.2014.10.001 Boll, 2018, Oxytocin and pain perception: from animal models to human Research, Neuroscience, 387, 149, 10.1016/j.neuroscience.2017.09.041 Singh, 2020, Mapping cortical integration of sensory and affective pain pathways, Curr. Biol., 30, 1703, 10.1016/j.cub.2020.02.091 Zhang, 2017, Chronic pain induces generalized enhancement of aversion, eLife, 6, 10.7554/eLife.25302 Johansen, 2001, The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex, Proc. Natl. Acad. Sci. USA, 98, 8077, 10.1073/pnas.141218998 King, 2009, Unmasking the tonic-aversive state in neuropathic pain, Nat. Neurosci., 12, 1364, 10.1038/nn.2407 Zhang, 2021, A prototype closed-loop brain-machine interface for the study and treatment of pain, Nat. Biomed. Eng., 10.1038/s41551-021-00736-7 Elands, 1988, 125I-labelled d(CH2)5[Tyr(Me)2,Thr4,Tyr-NH2(9)]OVT: a selective oxytocin receptor ligand, Eur. J. Pharmacol., 147, 197, 10.1016/0014-2999(88)90778-9 Grazzini, 1998, Inhibition of oxytocin receptor function by direct binding of progesterone, Nature, 392, 509, 10.1038/33176 Friedrich, 2017, Fast online deconvolution of calcium imaging data, PLoS Comput. Biol., 13, 10.1371/journal.pcbi.1005423 De Vico Fallani, 2014, Graph analysis of functional brain networks: practical issues in translational neuroscience, Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 10.1098/rstb.2013.0521 Kwon, 2019, A Physarum centrality measure of the human brain network, Sci. Rep., 9 Sun, 2022, Closed-loop stimulation using a multiregion brain-machine interface has analgesic effects in rodents, Sci. Transl. Med., 14, 10.1126/scitranslmed.abm5868 Basbaum, 1984, Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry, Annu. Rev. Neurosci., 7, 309, 10.1146/annurev.ne.07.030184.001521 Motojima, 2017, Comparison of the induction of c-fos-eGFP and Fos protein in the rat spinal cord and hypothalamus resulting from subcutaneous capsaicin or formalin injection, Neuroscience, 356, 64, 10.1016/j.neuroscience.2017.05.015 Owen, 2013, Oxytocin enhances hippocampal spike transmission by modulating fast-spiking interneurons, Nature, 500, 458, 10.1038/nature12330 Tirko, 2018, Oxytocin transforms firing mode of CA2 hippocampal neurons, Neuron, 100, 593, 10.1016/j.neuron.2018.09.008 Baliki, 2012, Corticostriatal functional connectivity predicts transition to chronic back pain, Nat. Neurosci., 15, 1117, 10.1038/nn.3153 Kano, 2020, Resting state functional connectivity of the pain matrix and default mode network in irritable bowel syndrome: a graph theoretical analysis, Sci. Rep., 10, 10.1038/s41598-020-67048-9 Mutso, 2012, Abnormalities in hippocampal functioning with persistent pain, J. Neurosci., 32, 5747, 10.1523/JNEUROSCI.0587-12.2012 Spisak, 2020, Pain-free resting-state functional brain connectivity predicts individual pain sensitivity, Nat. Commun., 11, 187, 10.1038/s41467-019-13785-z Vachon-Presseau, 2019, Identification of traits and functional connectivity-based neurotraits of chronic pain, PLoS Biol., 17, 10.1371/journal.pbio.3000349 Bonifazi, 2019, Reconstruction of functional connectivity from multielectrode recordings and calcium imaging, Adv. Neurobiol., 22, 207, 10.1007/978-3-030-11135-9_9 Sporns, 2018, Graph theory methods: applications in brain networks, Dial. Clin. Neurosci., 20, 111, 10.31887/DCNS.2018.20.2/osporns Bilbao, 2018, Longitudinal structural and functional brain network alterations in a mouse model of neuropathic pain, Neuroscience, 387, 104, 10.1016/j.neuroscience.2018.04.020 Komaki, 2016, Functional brain mapping using specific sensory-circuit stimulation and a theoretical graph network analysis in mice with neuropathic allodynia, Sci. Rep., 6, 10.1038/srep37802 Minati, 2013, From brain topography to brain topology: relevance of graph theory to functional neuroscience, NeuroReport, 24, 536, 10.1097/WNR.0b013e3283621234 Redcay, 2013, Intrinsic functional network organization in high-functioning adolescents with autism spectrum disorder, Front. Hum. Neurosci., 7, 10.3389/fnhum.2013.00573 Kobak, 2016, Demixed principal component analysis of neural population data, eLife, 5, 10.7554/eLife.10989 Markowitz, 2015, Multiple component networks support working memory in prefrontal cortex, Proc. Natl. Acad. Sci. USA, 112, 11084, 10.1073/pnas.1504172112 Murray, 2017, Stable population coding for working memory coexists with heterogeneous neural dynamics in prefrontal cortex, Proc. Natl. Acad. Sci. USA, 114, 394, 10.1073/pnas.1619449114 Dabrowska, 2011, Neuroanatomical evidence for reciprocal regulation of the corticotrophin-releasing factor and oxytocin systems in the hypothalamus and the bed nucleus of the stria terminalis of the rat: implications for balancing stress and affect, Psychoneuroendocrinology, 36, 1312, 10.1016/j.psyneuen.2011.03.003 Ebner, 2005, Release of oxytocin in the rat central amygdala modulates stress-coping behavior and the release of excitatory amino acids, Neuropsychopharmacology, 30, 223, 10.1038/sj.npp.1300607 Grund, 2017, Neuropeptide S activates paraventricular oxytocin neurons to induce anxiolysis, J. Neurosci., 37, 12214, 10.1523/JNEUROSCI.2161-17.2017 Neumann, 2016, Oxytocin in general anxiety and social fear: A translational approach, Biol. Psychiatry, 79, 213, 10.1016/j.biopsych.2015.06.004 Vacher, 2002, Activation by serotonin and noradrenaline of vasopressin and oxytocin expression in the mouse paraventricular and supraoptic nuclei, J. Neurosci., 22, 1513, 10.1523/JNEUROSCI.22-05-01513.2002 Wotjak, 1998, Dissociated central and peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: new insights into the secretory capacities of peptidergic neurons, Neuroscience, 85, 1209, 10.1016/S0306-4522(97)00683-0 Ji, 2010, Cognitive impairment in pain through amygdala-driven prefrontal cortical deactivation, J. Neurosci., 30, 5451, 10.1523/JNEUROSCI.0225-10.2010 Wang, 2015, Deactivation of excitatory neurons in the prelimbic cortex via Cdk5 promotes pain sensation and anxiety, Nat. Commun., 6, 7660, 10.1038/ncomms8660 Sheintuch, 2017, Tracking the same neurons across multiple days in Ca(2+) imaging data, Cell Rep., 21, 1102, 10.1016/j.celrep.2017.10.013 Sabihi, 2014, Oxytocin in the prelimbic medial prefrontal cortex reduces anxiety-like behavior in female and male rats, Psychoneuroendocrinology, 45, 31, 10.1016/j.psyneuen.2014.03.009 Tapp, 2020, Central but not peripheral oxytocin administration reduces risk-based decision-making in male rats, Horm. Behav., 125, 104840, 10.1016/j.yhbeh.2020.104840 Pnevmatikakis, 2016, Simultaneous denoising, deconvolution, and demixing of calcium imaging data, Neuron, 89, 285, 10.1016/j.neuron.2015.11.037 Vander Weele, 2018, Dopamine enhances signal-to-noise ratio in cortical-brainstem encoding of aversive stimuli, Nature, 563, 397, 10.1038/s41586-018-0682-1 Zhou, 2018, Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data, eLife, 7, 10.7554/eLife.28728 Goffer, 2013, Calcium-permeable AMPA receptors in the nucleus accumbens regulate depression-like behaviors in the chronic neuropathic pain state, J. Neurosci., 33, 19034, 10.1523/JNEUROSCI.2454-13.2013 Wang, 2011, A single subanesthetic dose of ketamine relieves depression-like behaviors induced by neuropathic pain in rats, Anesthesiology, 115, 812, 10.1097/ALN.0b013e31822f16ae Hargreaves, 1988, A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia, Pain, 32, 77, 10.1016/0304-3959(88)90026-7 Corder, 2019, An amygdalar neural ensemble that encodes the unpleasantness of pain, Science, 363, 276, 10.1126/science.aap8586