Pathway- and Cell-Specific Kappa-Opioid Receptor Modulation of Excitation-Inhibition Balance Differentially Gates D1 and D2 Accumbens Neuron Activity

Neuron - Tập 93 - Trang 147-163 - 2017
Hugo A. Tejeda1, Jocelyn Wu1, Alana R. Kornspun1, Marco Pignatelli1, Vadim Kashtelyan2, Michael J. Krashes1,3, Brad B. Lowell4, William A. Carlezon5, Antonello Bonci1,6
1Synaptic Plasticity Section, National Institute on Drug Abuse Intramural Research Program, Baltimore, MD 21224, USA
2Neuronal Networks Section, National Institute on Drug Abuse Intramural Research Program, Baltimore, MD 21224, USA
3Diabetes, Endocrinology, and Obesity Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, MD 20892, USA
4Division of Endocrinology, Diabetes, and Metabolism, Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, 02215, USA
5Behavioral Genetics Laboratory, Department of Psychiatry, Harvard Medical School, McLean Hospital, Belmont, MA 02578, USA
6Solomon H. Snyder Department of Neuroscience, Johns Hopkins University, Baltimore, MD 21205, USA

Tài liệu tham khảo

Al-Hasani, 2015, Distinct subpopulations of nucleus accumbens dynorphin neurons drive aversion and reward, Neuron, 87, 1063, 10.1016/j.neuron.2015.08.019 Ambroggi, 2008, Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons, Neuron, 59, 648, 10.1016/j.neuron.2008.07.004 Atwood, 2014, Opioids induce dissociable forms of long-term depression of excitatory inputs to the dorsal striatum, Nat. Neurosci., 17, 540, 10.1038/nn.3652 Bagetta, 2011, Dopamine-dependent long-term depression is expressed in striatal spiny neurons of both direct and indirect pathways: implications for Parkinson’s disease, J. Neurosci., 31, 12513, 10.1523/JNEUROSCI.2236-11.2011 Bagot, 2015, Ventral hippocampal afferents to the nucleus accumbens regulate susceptibility to depression, Nat. Commun., 6, 7062, 10.1038/ncomms8062 Banghart, 2015, Enkephalin disinhibits mu opioid receptor-rich striatal patches via delta opioid receptors, Neuron, 88, 1227, 10.1016/j.neuron.2015.11.010 Bocklisch, 2013, Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area, Science, 341, 1521, 10.1126/science.1237059 Britt, 2012, Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens, Neuron, 76, 790, 10.1016/j.neuron.2012.09.040 Bruchas, 2010, The dynorphin/kappa opioid system as a modulator of stress-induced and pro-addictive behaviors, Brain Res., 1314, 44, 10.1016/j.brainres.2009.08.062 Calipari, 2016, In vivo imaging identifies temporal signature of D1 and D2 medium spiny neurons in cocaine reward, Proc. Natl. Acad. Sci. USA, 113, 2726, 10.1073/pnas.1521238113 Carlezon, 1998, Regulation of cocaine reward by CREB, Science, 282, 2272, 10.1126/science.282.5397.2272 Castro, 2014, Opioid hedonic hotspot in nucleus accumbens shell: mu, delta, and kappa maps for enhancement of sweetness “liking” and “wanting”, J. Neurosci., 34, 4239, 10.1523/JNEUROSCI.4458-13.2014 Chavkin, 1982, Dynorphin is a specific endogenous ligand of the kappa opioid receptor, Science, 215, 413, 10.1126/science.6120570 Chefer, 2013, Kappa opioid receptors on dopaminergic neurons are necessary for kappa-mediated place aversion, Neuropsychopharmacology, 38, 2623, 10.1038/npp.2013.171 Crowley, 2015, Kappa opioid receptor signaling in the brain: Circuitry and implications for treatment, Prog. Neuropsychopharmacol. Biol. Psychiatry, 62, 51, 10.1016/j.pnpbp.2015.01.001 Crowley, 2016, Dynorphin controls the gain of an amygdalar anxiety circuit, Cell Rep., 14, 2774, 10.1016/j.celrep.2016.02.069 Ehrich, 2015, Kappa opioid receptor-induced aversion requires p38 MAPK activation in VTA dopamine neurons, J. Neurosci., 35, 12917, 10.1523/JNEUROSCI.2444-15.2015 Ferguson, 2011, Transient neuronal inhibition reveals opposing roles of indirect and direct pathways in sensitization, Nat. Neurosci., 14, 22, 10.1038/nn.2703 Floresco, 2001, Dopamine D1 and NMDA receptors mediate potentiation of basolateral amygdala-evoked firing of nucleus accumbens neurons, J. Neurosci., 21, 6370, 10.1523/JNEUROSCI.21-16-06370.2001 Gangarossa, 2013, Distribution and compartmental organization of GABAergic medium-sized spiny neurons in the mouse nucleus accumbens, Front. Neural Circuits, 7, 22, 10.3389/fncir.2013.00022 Gerfen, 1990, D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons, Science, 250, 1429, 10.1126/science.2147780 Grueter, 2010, Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens, Nat. Neurosci., 13, 1519, 10.1038/nn.2685 Hjelmstad, 2003, Kappa opioid receptor activation in the nucleus accumbens inhibits glutamate and GABA release through different mechanisms, J. Neurophysiol., 89, 2389, 10.1152/jn.01115.2002 Hurd, 1993, Molecular alterations in the neostriatum of human cocaine addicts, Synapse, 13, 357, 10.1002/syn.890130408 Hurd, 1997, Prodynorphin mRNA expression is increased in the patch vs matrix compartment of the caudate nucleus in suicide subjects, Mol. Psychiatry, 2, 495, 10.1038/sj.mp.4000319 Isaacson, 2011, How inhibition shapes cortical activity, Neuron, 72, 231, 10.1016/j.neuron.2011.09.027 Ishikawa, 2009, Homeostatic synapse-driven membrane plasticity in nucleus accumbens neurons, J. Neurosci., 29, 5820, 10.1523/JNEUROSCI.5703-08.2009 Jones, 2010, Basolateral amygdala modulates terminal dopamine release in the nucleus accumbens and conditioned responding, Biol. Psychiatry, 67, 737, 10.1016/j.biopsych.2009.11.006 Koos, 2004, Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum, J. Neurosci., 24, 7916, 10.1523/JNEUROSCI.2163-04.2004 Krashes, 2014, An excitatory paraventricular nucleus to AgRP neuron circuit that drives hunger, Nature, 507, 238, 10.1038/nature12956 Kravitz, 2012, Distinct roles for direct and indirect pathway striatal neurons in reinforcement, Nat. Neurosci., 15, 816, 10.1038/nn.3100 Kreitzer, 2009, Physiology and pharmacology of striatal neurons, Annu. Rev. Neurosci., 32, 127, 10.1146/annurev.neuro.051508.135422 Kreitzer, 2007, Endocannabinoid-mediated rescue of striatal LTD and motor deficits in Parkinson’s disease models, Nature, 445, 643, 10.1038/nature05506 Lobo, 2010, Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward, Science, 330, 385, 10.1126/science.1188472 Lovett-Barron, 2012, Regulation of neuronal input transformations by tunable dendritic inhibition, Nat Neurosci, 15, 423, 10.1038/nn.3024 Matsui, 2014, Separate GABA afferents to dopamine neurons mediate acute action of opioids, development of tolerance, and expression of withdrawal, Neuron, 82, 1346, 10.1016/j.neuron.2014.04.030 McDevitt, 2014, Serotonergic versus nonserotonergic dorsal raphe projection neurons: differential participation in reward circuitry, Cell Rep., 8, 1857, 10.1016/j.celrep.2014.08.037 Meng, 1993, Cloning and pharmacological characterization of a rat kappa opioid receptor, Proc. Natl. Acad. Sci. USA, 90, 9954, 10.1073/pnas.90.21.9954 Meshul, 2000, Kappa opioid receptor immunoreactivity in the nucleus accumbens and caudate-putamen is primarily associated with synaptic vesicles in axons, Neuroscience, 96, 91, 10.1016/S0306-4522(99)90481-5 Moratalla, 1996, Cellular responses to psychomotor stimulant and neuroleptic drugs are abnormal in mice lacking the D1 dopamine receptor, Proc. Natl. Acad. Sci. USA, 93, 14928, 10.1073/pnas.93.25.14928 Mu, 2011, Exposure to cocaine alters dynorphin-mediated regulation of excitatory synaptic transmission in nucleus accumbens neurons, Biol. Psychiatry, 69, 228, 10.1016/j.biopsych.2010.09.014 Muschamp, 2011, Activation of CREB in the nucleus accumbens shell produces anhedonia and resistance to extinction of fear in rats, J. Neurosci., 31, 3095, 10.1523/JNEUROSCI.5973-10.2011 O’Connor, 2015, Accumbal D1R neurons projecting to lateral hypothalamus authorize feeding, Neuron, 88, 553, 10.1016/j.neuron.2015.09.038 O’Donnell, 1995, Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input, J. Neurosci., 15, 3622, 10.1523/JNEUROSCI.15-05-03622.1995 Palmer, 2012, The cellular basis of GABA(B)-mediated interhemispheric inhibition, Science, 335, 989, 10.1126/science.1217276 Pascoli, 2014, Contrasting forms of cocaine-evoked plasticity control components of relapse, Nature, 509, 459, 10.1038/nature13257 Planert, 2010, Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways, J. Neurosci., 30, 3499, 10.1523/JNEUROSCI.5139-09.2010 Pliakas, 2001, Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated cAMP response element-binding protein expression in nucleus accumbens, J. Neurosci., 21, 7397, 10.1523/JNEUROSCI.21-18-07397.2001 Schlosburg, 2013, Long-term antagonism of κ opioid receptors prevents escalation of and increased motivation for heroin intake, J. Neurosci., 33, 19384, 10.1523/JNEUROSCI.1979-13.2013 Shen, 2008, Dichotomous dopaminergic control of striatal synaptic plasticity, Science, 321, 848, 10.1126/science.1160575 Shirayama, 2004, Stress increases dynorphin immunoreactivity in limbic brain regions and dynorphin antagonism produces antidepressant-like effects, J. Neurochem., 90, 1258, 10.1111/j.1471-4159.2004.02589.x Sohal, 2009, Parvalbumin neurons and gamma rhythms enhance cortical circuit performance, Nature, 459, 698, 10.1038/nature07991 Stuber, 2011, Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking, Nature, 475, 377, 10.1038/nature10194 Svingos, 1999, Cellular sites for dynorphin activation of kappa-opioid receptors in the rat nucleus accumbens shell, J. Neurosci., 19, 1804, 10.1523/JNEUROSCI.19-05-01804.1999 Tejeda, 2012, The dynorphin/κ-opioid receptor system and its role in psychiatric disorders, Cell. Mol. Life Sci., 69, 857, 10.1007/s00018-011-0844-x Tejeda, 2013, Prefrontal cortical kappa-opioid receptor modulation of local neurotransmission and conditioned place aversion, Neuropsychopharmacology, 38, 1770, 10.1038/npp.2013.76 Tejeda, 2015, Prefrontal cortical kappa opioid receptors attenuate responses to amygdala inputs, Neuropsychopharmacology, 40, 2856, 10.1038/npp.2015.138 Tepper, 2004, GABAergic microcircuits in the neostriatum, Trends Neurosci., 27, 662, 10.1016/j.tins.2004.08.007 Tunstall, 2002, Inhibitory interactions between spiny projection neurons in the rat striatum, J. Neurophysiol., 88, 1263, 10.1152/jn.2002.88.3.1263 Van’t Veer, 2013, Role of kappa-opioid receptors in stress and anxiety-related behavior, Psychopharmacology (Berl.), 229, 435, 10.1007/s00213-013-3195-5 Van’t Veer, 2013, Ablation of kappa-opioid receptors from brain dopamine neurons has anxiolytic-like effects and enhances cocaine-induced plasticity, Neuropsychopharmacology, 38, 1585, 10.1038/npp.2013.58 Wang, 1994, NMDA receptors mediate amphetamine-induced upregulation of zif/268 and preprodynorphin mRNA expression in rat striatum, Synapse, 18, 343, 10.1002/syn.890180410 Wee, 2010, The role of the dynorphin-kappa opioid system in the reinforcing effects of drugs of abuse, Psychopharmacology (Berl.), 210, 121, 10.1007/s00213-010-1825-8 Wilson, 2007, GABAergic inhibition in the neostriatum, Prog. Brain Res., 160, 91, 10.1016/S0079-6123(06)60006-X Yamaguchi, 2011, Mesocorticolimbic glutamatergic pathway, J. Neurosci., 31, 8476, 10.1523/JNEUROSCI.1598-11.2011