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Dendritic Release of Neurotransmitters

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Release of neuroactive substances by exocytosis from dendrites is surprisingly widespread and is not confined to a particular class of transmitters: it occurs in multiple brain regions, and includes a range of neuropeptides, classical neurotransmitters, and signaling molecules, such as nitric oxide, carbon monoxide, ATP, and arachidonic acid. This review is focused on hypothalamic neuroendocrine cells that release vasopressin and oxytocin and midbrain neurons that release dopamine. For these two model systems, the stimuli, mechanisms, and physiological functions of dendritic release have been explored in greater detail than is yet available for other neurons and neuroactive substances. © 2017 American Physiological Society. Compr Physiol 7:235‐252, 2017.

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Figure 1. Figure 1. Comparison of the mechanisms of somatodendritic release of oxytocin and vasopressin in the hypothalamus (A) and dopamine in the substantia nigra (B). (A) Neuropeptides are synthesized and packaged in the soma and stored in dendrites in a reserve pool (RP) containing large numbers of LDCVs in dendrites. Depolarization‐induced Ca2+ entry through VGCCs stimulates peptide release by exocytosis of LDCVs. This requires the depolymerization of F‐actin to G‐actin. Furthermore, the stimulation of G‐protein coupled receptors, such as the oxytocin receptor, stimulates the mobilization of Ca2+ from IP3‐dependent intracellular stores and an increase in both the number of LDCVs and N‐type VGCCs at the plasma membrane, thus priming the exocytosis machinery for subsequent activity‐dependent release. Although some members of the SNARE family are detectable by immunocytochemistry, there appears to be a lack of VAMP, SNAP‐25 and synaptotagmin‐1 in the somata‐dendrites, with their function presumably being replaced by other SNARE proteins. TG, thapsigargin; CPA, cyclopiazonic acid. (B). Features of somatodendritic dopamine release. Dopamine is synthesized in the intracellular compartment from tyrosine via TH. This process generates L‐DOPA, which is converted to dopamine by aromatic amino acid decarboxylase (AADC). Synthesized dopamine is stored in tubulovesicular structures that are part of the ER; these structures are the primary site of VMAT2, the vesicular monoamine transporter expressed in dopamine soma and proximal dendrites. Dopamine dendrites contain few vesicles, but those present appear to bud from tubulovesicles. Somatodendritic dopamine release is action potential dependent. Release also requires Ca2+ entry via VGCCs, but is amplified by both RyRs and metabotropic glutamate receptor (mGluR)‐dependent activation of IP3Rs that release Ca2+ from intracellular ER stores. Immunohistochemical evidence suggests that a novel constellation of SNARE proteins may be involved in the release, including SNAP‐25, VAMP2, and syntaxin3b. Release from dendrites has also been suggested to involved reversal of the DAT. Released dopamine is taken up and recycled via the DAT.

Figure 1. Comparison of the mechanisms of somatodendritic release of oxytocin and vasopressin in the hypothalamus (A) and dopamine in the substantia nigra (B). (A) Neuropeptides are synthesized and packaged in the soma and stored in dendrites in a reserve pool (RP) containing large numbers of LDCVs in dendrites. Depolarization‐induced Ca2+ entry through VGCCs stimulates peptide release by exocytosis of LDCVs. This requires the depolymerization of F‐actin to G‐actin. Furthermore, the stimulation of G‐protein coupled receptors, such as the oxytocin receptor, stimulates the mobilization of Ca2+ from IP3‐dependent intracellular stores and an increase in both the number of LDCVs and N‐type VGCCs at the plasma membrane, thus priming the exocytosis machinery for subsequent activity‐dependent release. Although some members of the SNARE family are detectable by immunocytochemistry, there appears to be a lack of VAMP, SNAP‐25 and synaptotagmin‐1 in the somata‐dendrites, with their function presumably being replaced by other SNARE proteins. TG, thapsigargin; CPA, cyclopiazonic acid. (B). Features of somatodendritic dopamine release. Dopamine is synthesized in the intracellular compartment from tyrosine via TH. This process generates L‐DOPA, which is converted to dopamine by aromatic amino acid decarboxylase (AADC). Synthesized dopamine is stored in tubulovesicular structures that are part of the ER; these structures are the primary site of VMAT2, the vesicular monoamine transporter expressed in dopamine soma and proximal dendrites. Dopamine dendrites contain few vesicles, but those present appear to bud from tubulovesicles. Somatodendritic dopamine release is action potential dependent. Release also requires Ca2+ entry via VGCCs, but is amplified by both RyRs and metabotropic glutamate receptor (mGluR)‐dependent activation of IP3Rs that release Ca2+ from intracellular ER stores. Immunohistochemical evidence suggests that a novel constellation of SNARE proteins may be involved in the release, including SNAP‐25, VAMP2, and syntaxin3b. Release from dendrites has also been suggested to involved reversal of the DAT. Released dopamine is taken up and recycled via the DAT.
 1.Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366‐375, 1989.
 2.An S, Zenisek D. Regulation of exocytosis in neurons, neuroendocrine cells. Cur Opin Neurobiol 14: 522‐530, 2004.
 3.Andersson DR, Nissbrandt H, Bergquist F. Partial depletion of dopamine in substantia nigra impairs motor performance without altering striatal dopamine neurotransmission. Eur J Neurosci 24: 617‐624, 2006.
 4.Armstrong WE. Morphological, electrophysiological classification of hypothalamic supraoptic neurons. Prog Neurobiol 47: 291‐339, 1995.
 5.Bains JS, Ferguson AV. Activation of N‐methyl‐D‐aspartate receptors evokes calcium spikes in the dendrites of rat hypothalamic paraventricular nucleus neurons. Neuroscience 90: 885‐891, 1999.
 6.Baraban SC, Tallent MK. Interneuron diversity series: Interneuronal neuropeptides–endogenous regulators of neuronal excitability. Trends Neurosci 27: 135‐142, 2004.
 7.Bayer VE, Pickel VM. Ultrastructural localization of tyrosine hydroxylase in the rat ventral tegmental area: Relationship between immunolabeling density, neuronal associations. J Neurosci 10: 2996‐3013, 1990.
 8.Bealer SL, Armstrong WE, Crowley WR. Oxytocin release in magnocellular nuclei: neurochemical mediators, functional significance during gestation. Am J Physiol 299: R452‐458, 2010.
 9.Beckstead MJ, Ford CP, Phillips PE, Williams JT. Presynaptic regulation of dendrodendritic dopamine transmission. Eur J Neurosci 26: 1479‐1488, 2007.
 10.Beckstead MJ, Grandy DK, Wickman K, Williams JT. Vesicular dopamine release elicits an inhibitory postsynaptic current in midbrain dopamine neurons. Neuron 42: 939‐946, 2004.
 11.Bergquist F, Jonason J, Pileblad E, Nissbrandt H. Effects of local administration of L‐, N‐, P/Q‐type calcium channel blockers on spontaneous dopamine release in the striatum, the substantia nigra: A microdialysis study in rat. J Neurochem 70: 1532‐1540, 1998.
 12.Bergquist F, Ludwig M. Dendritic transmitter release: A comparison of two model systems. J Neuroendocrinol 20: 677‐686, 2008.
 13.Bergquist F, Niazi HS, Nissbrandt H. Evidence for different exocytosis pathways in dendritic, terminal dopamine release in vivo. Brain Res 950: 245‐253, 2002.
 14.Bergquist F, Nissbrandt H. Influence of R‐type (Cav2.3), t‐type (Cav3.1‐3.3) antagonists on nigral somatodendritic dopamine release measured by microdialysis. Neuroscience 120: 757‐764, 2003.
 15.Bergquist F, Shahabi HN, Nissbrandt H. Somatodendritic dopamine release in rat substantia nigra influences motor performance on the accelerating rod. Brain Res 973: 81‐91, 2003.
 16.Birgner C, Nordenankar K, Lundblad M, Mendez JA, Smith C, le Greves M, Galter D, Olson L, Fredriksson A, Trudeau LE, Kullander K, Wallen‐Mackenzie A. VGLUT2 in dopamine neurons is required for psychostimulant‐induced behavioral activation. Proc Natl Acad Sci U S A 107: 389‐394, 2010.
 17.Bjorklund A, Lindvall O. Dopamine in dendrites of substantia nigra neurons: Suggestions for a role in dendritic terminals. Brain Res 83: 531‐537, 1975.
 18.Brimblecombe KR, Gracie CJ, Platt NJ, Cragg SJ. Gating of dopamine transmission by calcium, axonal N‐, Q‐, T‐, L‐type voltage‐gated calcium channels differs between striatal domains. J Physiol 593: 929‐946, 2015.
 19.Brown CH, Bains JS, Ludwig M, Stern JE. Physiological regulation of magnocellular neurosecretory cell activity: Integration of intrinsic, local, afferent mechanisms. J Neuroendocrinol 25: 678‐710, 2013.
 20.Brown CH, Munro G, Johnstone LE, Robson AC, Landgraf R, Russell JA. Oxytocin neurone autoexcitation during morphine withdrawal in anaesthetized rats. Neuroreport 8: 951‐955, 1997.
 21.Brown CH, Scott V, Ludwig M, Leng G, Bourque CW. Somatodendritic dynorphin release: Orchestrating activity patterns of vasopressin neurons. Biochem Soc Trans 35: 1236‐1242, 2007.
 22.Callahan MF, Ludwig M, Tsai KP, Sim LJ, Morris M. Baroreceptor input regulates osmotic control of central vasopressin secretion. Neuroendocrinology 65: 238‐245, 1997.
 23.Cameron DL, Williams JT. Dopamine D1 receptors facilitate transmitter release. Nature 366: 344‐347, 1993.
 24.Carlsson A. Treatment of Parkinson's with L‐DOPA. The early discovery phase, a comment on current problems. J Neural Transm (Vienna) 109: 777‐787, 2002.
 25.Carta M, Bezard E. Contribution of pre‐synaptic mechanisms to L‐DOPA‐induced dyskinesia. Neuroscience 198: 245‐251, 2011.
 26.Chen BT, Avshalumov MV, Rice ME. Modulation of somatodendritic dopamine release by endogenous H(2)O(2): susceptibility in substantia nigra but resistance in VTA. J Neurophysiol 87: 1155‐1158, 2002.
 27.Chen BT, Moran KA, Avshalumov MV, Rice ME. Limited regulation of somatodendritic dopamine release by voltage‐sensitive Ca channels contrasted with strong regulation of axonal dopamine release. J Neurochem 96: 645‐655, 2006.
 28.Chen BT, Patel JC, Moran KA, Rice ME. Differential calcium dependence of axonal versus somatodendritic dopamine release, with characteristics of both in the ventral tegmental area. Front Syst Neurosci 5: 39, 2011.
 29.Chen BT, Rice ME. Novel Ca2+ dependence, time course of somatodendritic dopamine release: Substantia nigra versus striatum. J Neurosci 21: 7841‐7847, 2001.
 30.Chen BT, Rice ME. Synaptic regulation of somatodendritic dopamine release by glutamate, GABA differs between substantia nigra, ventral tegmental area. J Neurochem 81: 158‐169, 2002.
 31.Chen QH, Toney GM. Identification, characterization of two functionally distinct groups of spinal cord‐projecting paraventricular nucleus neurons with sympathetic‐related activity. Neuroscience 118: 797‐807, 2003.
 32.Cheramy A, Leviel V, Glowinski J. Dendritic release of dopamine in the substantia nigra. Nature 289: 537‐542, 1981.
 33.Chevaleyre V, Dayanithi G, Moos FC, Desarmenien MG. Developmental regulation of a local positive autocontrol of supraoptic neurons. J Neurosci 20: 5813‐5819, 2000.
 34.Choi YM, Kim SH, Chung S, Uhm DY, Park MK. Regional interaction of endoplasmic reticulum Ca2+ signals between soma, dendrites through rapid luminal Ca2+ diffusion. J Neurosci 26: 12127‐12136, 2006.
 35.Chuhma N, Mingote S, Moore H, Rayport S. Dopamine neurons control striatal cholinergic neurons via regionally heterogeneous dopamine, glutamate signaling. Neuron 81: 901‐912, 2014.
 36.Chuhma N, Zhang H, Masson J, Zhuang X, Sulzer D, Hen R, Rayport S. Dopamine neurons mediate a fast excitatory signal via their glutamatergic synapses. J Neurosci 24: 972‐981, 2004.
 37.Cook CJ, Devine CE. Antibody‐based electrodes for hormonal, neurotransmitter measurements in vivo. Electronalaysis 10: 1108‐1111, 1998.
 38.Courtney NA, Mamaligas AA, Ford CP. Species differences in somatodendritic dopamine transmission determine D2‐autoreceptor‐mediated inhibition of ventral tegmental area neuron firing. J Neurosci 32: 13520‐13528, 2012.
 39.Cox CL. Complex regulation of dendritic transmitter release from thalamic interneurons. Cur Opin Neurobiol 29C: 126‐132, 2014.
 40.Cragg S, Rice ME, Greenfield SA. Heterogeneity of electrically evoked dopamine release, reuptake in substantia nigra, ventral tegmental area, striatum. J Neurophysiol 77: 863‐873, 1997.
 41.Cragg SJ, Greenfield SA. Differential autoreceptor control of somatodendritic, axon terminal dopamine release in substantia nigra, ventral tegmental area, striatum. J Neurosci 17: 5738‐5746, 1997.
 42.Cragg SJ, Hawkey CR, Greenfield SA. Comparison of serotonin, dopamine release in substantia nigra, ventral tegmental area: Region, species differences. J Neurochem 69: 2378‐2386, 1997.
 43.Cragg SJ, Nicholson C, Kume‐Kick J, Tao L, Rice ME. Dopamine‐mediated volume transmission in midbrain is regulated by distinct extracellular geometry, uptake. J Neurophysiol 85: 1761‐1771, 2001.
 44.Cragg SJ, Rice ME. DAncing past the DAT at a DA synapse. Trends Neurosci 27: 270‐277, 2004.
 45.Crocker AD. The regulation of motor control: An evaluation of the role of dopamine receptors in the substantia nigra. Rev Neurosci 8: 55‐76, 1997.
 46.Crosby KM, Baimoukhametova DV, Bains JS, Pittman QJ. Postsynaptic depolarization enhances GABA drive to dorsomedial hypothalamic neurons through somatodendritic cholecystokinin release. J Neurosci 35: 13160‐13170, 2015.
 47.Crowley WR, Armstrong WE. Neurochemical regulation of oxytocin secretion in lactation. Endocr Rev 13: 33‐65, 1992.
 48.Cui G, Bernier BE, Harnett MT, Morikawa H. Differential regulation of action potential‐, metabotropic glutamate receptor‐induced Ca2+ signals by inositol 1,4,5‐trisphosphate in dopaminergic neurons. J Neurosci 27: 4776‐4785, 2007.
 49.Dawson TM, Snyder SH. Gases as biological messengers: Nitric oxide, carbon monoxide in the brain. J Neurosci 14: 5147‐5159, 1994.
 50.Dayanithi G, Forostyak O, Ueta Y, Verkhratsky A, Toescu EC. Segregation of calcium signalling mechanisms in magnocellular neurones, terminals. Cell Calcium 51: 293‐299, 2012. Kock CP, Burnashev N, Lodder JC, Mansvelder HD, Brussaard AB. NMDA receptors induce somatodendritic secretion in hypothalamic neurones of lactating female rats. J Physiol 561: 53‐64, 2004. Kock CP, Cornelisse LN, Burnashev N, Lodder JC, Timmerman AJ, Couey JJ, Mansvelder HD, Brussaard AB. NMDA receptors trigger neurosecretion of 5‐HT within dorsal raphe nucleus of the rat in the absence of action potential firing. J Physiol 577: 891‐905, 2006. Kock CP, Wierda KD, Bosman LW, Min R, Koksma JJ, Mansvelder HD, Verhage M, Brussaard AB. Somatodendritic secretion in oxytocin neurons is upregulated during the female reproductive cycle. J Neurosci 23: 2726‐2734, 2003.
 54.De Mota N, Reaux‐Le Goazigo A, El Messari S, Chartrel N, Roesch D, Dujardin C, Kordon C, Vaudry H, Moos F, Llorens‐Cortes C. Apelin, a potent diuretic neuropeptide counteracting vasopressin actions through inhibition of vasopressin neuron activity, vasopressin release. Proc Natl Acad Sci U S A 101: 10464‐10469, 2004.
 55.Descarries L, Berube‐Carriere N, Riad M, Bo GD, Mendez JA, Trudeau LE. Glutamate in dopamine neurons: Synaptic versus diffuse transmission. Brain Res Rev 58: 290‐302, 2008.
 56.Deutch AY, Goldstein M, Baldino F, Jr., Roth RH. Telencephalic projections of the A8 dopamine cell group. Ann New York Acad Sci 537: 27‐50, 1988.
 57.Dillon C, Goda Y. The actin cytoskeleton: Integrating form, function at the synapse. Ann Rev Neurosci 28: 25‐55, 2005.
 58.Douglas AJ, Neumann I, Meeren HK, Leng G, Johnstone LE, Munro G, Russell JA. Central endogenous opioid inhibition of supraoptic oxytocin neurons in pregnant rats. J Neurosci 15: 5049‐5057, 1995.
 59.Duguid IC, Pankratov Y, Moss GW, Smart TG. Somatodendritic release of glutamate regulates synaptic inhibition in cerebellar Purkinje cells via autocrine mGluR1 activation. J Neurosci 27: 12464‐12474, 2007.
 60.Elverfors A, Jonason J, Jonason G, Nissbrandt H. Effects of drugs interfering with sodium channels, calcium channels on the release of endogenous dopamine from superfused substantia nigra slices. Synapse 26: 359‐369, 1997.
 61.Elverfors A, Nissbrandt H. Reserpine‐insensitive dopamine release in the substantia nigra? Brain Res 557: 5‐12, 1991.
 62.Engelmann M, Wotjak CT, Neumann I, Ludwig M, Landgraf R. Behavioral consequences of intracerebral vasopressin, oxytocin: Focus on learning, memory. Neurosci Biobehav Rev 20: 341‐358, 1996.
 63.Falkenburger BH, Barstow KL, Mintz IM. Dendrodendritic inhibition through reversal of dopamine transport. Science 293: 2465‐2470, 2001.
 64.Fiorillo CD, Williams JT. Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature 394: 78‐82, 1998.
 65.Fisher TE, Bourque CW. Calcium‐channel subtypes in the somata, axon terminals of magnocellular neurosecretory cells. Trends Neurosci 19: 440‐444, 1996.
 66.Fleming TM, Scott V, Naskar K, Joe N, Brown CH, Stern JE. State‐dependent changes in astrocyte regulation of extrasynaptic NMDA receptor signalling in neurosecretory neurons. J Physiol 589: 3929‐3941, 2011.
 67.Foehring RC, Armstrong WE. Pharmacological dissection of high‐voltage‐activated Ca2+ current types in acutely dissociated rat supraoptic magnocellular neurons. J Neurophysiol 76: 977‐983, 1996.
 68.Ford CP. The role of D2‐autoreceptors in regulating dopamine neuron activity, transmission. Neuroscience 282C: 13‐22, 2014.
 69.Ford CP, Gantz SC, Phillips PE, Williams JT. Control of extracellular dopamine at dendrite, axon terminals. J Neurosci 30: 6975‐6983, 2010.
 70.Fortin GD, Desrosiers CC, Yamaguchi N, Trudeau LE. Basal somatodendritic dopamine release requires snare proteins. J Neurochem 96: 1740‐1749, 2006.
 71.Freund‐Mercier MJ, Stoeckel ME, Klein MJ. Oxytocin receptors on oxytocin neurones: Histoautoradiographic detection in the lactating rat. J Physiol 480: 155‐161, 1994.
 72.Fujihara H, Sasaki K, Mishiro‐Sato E, Ohbuchi T, Dayanithi G, Yamasaki M, Ueta Y, Minamino N. Molecular characterization, biological function of neuroendocrine regulatory peptide‐3 in the rat. Endocrinology 153: 1377‐1386, 2012.
 73.Gantz SC, Bunzow JR, Williams JT. Spontaneous inhibitory synaptic currents mediated by a G protein‐coupled receptor. Neuron 78: 807‐812, 2013.
 74.Geffen LB, Jessell TM, Cuello AC, Iversen LL. Release of dopamine from dendrites in rat substantia nigra. Nature 260: 258‐260, 1976.
 75.Gentet LJ, Williams SR. Dopamine gates action potential backpropagation in midbrain dopaminergic neurons. J Neurosci 27: 1892‐1901, 2007.
 76.Gerfen CR, Surmeier DJ. Modulation of striatal projection systems by dopamine. Ann Rev Neurosci 34: 441‐466, 2011.
 77.Gillard ER, Leon‐Olea M, Mucio‐Ramirez S, Coburn CG, Sanchez‐Islas E, de Leon A, Mussenden H, Bauce LG, Pittman QJ, Curras‐Collazo MC. A novel role for endogenous pituitary adenylate cyclase activating polypeptide in the magnocellular neuroendocrine system. Endocrinology 147: 791‐803, 2006.
 78.Gonon FG. Nonlinear relationship between impulse flow, dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 24: 19‐28, 1988.
 79.Groves PM, Linder JC. Dendro‐dendritic synapses in substantia nigra: Descriptions based on analysis of serial sections. Exp Brain Res 49: 209‐217, 1983.
 80.Haber SN, Fudge JL, McFarland NR. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20: 2369‐2382, 2000.
 81.Hatton GI. Emerging concepts of structure‐function dynamics in adult brain: The hypothalamo‐neurohypophysial system. Prog Neurobiol 34: 437‐504, 1990.
 82.Hausser M, Stuart G, Racca C, Sakmann B. Axonal initiation, active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15: 637‐647, 1995.
 83.Heeringa MJ, Abercrombie ED. Biochemistry of somatodendritic dopamine release in substantia nigra: An in vivo comparison with striatal dopamine release. J Neurochem 65: 192‐200, 1995.
 84.Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, Edwards RH. Vesicular glutamate transport promotes dopamine storage, glutamate corelease in vivo. Neuron 65: 643‐656, 2010.
 85.Hoffman AF, Gerhardt GA. Differences in pharmacological properties of dopamine release between the substantia nigra, striatum: An in vivo electrochemical study. J Pharmacol Exp Ther 289: 455‐463, 1999.
 86.Hu B, Bourque CW. NMDA receptor‐mediated rhythmic bursting activity in rat supraoptic nucleus neurones in vitro. J Physiol 458: 667‐687, 1992.
 87.Ingram CD, Kavadas V, Thomas MR, Threapleton JD. Endogenous opioid control of somatodendritic oxytocin release from the hypothalamic supraoptic, paraventricular nuclei in vitro. Neurosci Res 25: 17‐24, 1996.
 88.Insel TR. The challenge of translation in social neuroscience: A review of oxytocin, vasopressin, affiliative behavior. Neuron 65: 768‐779, 2010.
 89.Iremonger KJ, Wamsteeker Cusulin JI, Bains JS. Changing the tune: Plasticity, adaptation of retrograde signals. Trends Neurosci 36: 471‐479, 2013.
 90.Isaacson JS. Mechanisms governing dendritic gamma‐aminobutyric acid (GABA) release in the rat olfactory bulb. Proc Natl Acad Sci U S A 98: 337‐342, 2001.
 91.Jaffe EH, Marty A, Schulte A, Chow RH. Extrasynaptic vesicular transmitter release from the somata of substantia nigra neurons in rat midbrain slices. J Neurosci 18: 3548‐3553, 1998.
 92.Jhamandas JH, Lind RW, Renaud LP. Angiotensin II may mediate excitatory neurotransmission from the subfornical organ to the hypothalamic supraoptic nucleus: An anatomical, electrophysiological study in the rat. Brain Res 487: 52‐61, 1989.
 93.John CE, Budygin EA, Mateo Y, Jones SR. Neurochemical characterization of the release, uptake of dopamine in ventral tegmental area, serotonin in substantia nigra of the mouse. J Neurochem 96: 267‐282, 2006.
 94.Joux N, Chevaleyre V, Alonso G, Boissin‐Agasse L, Moos FC, Desarmenien MG, Hussy N. High voltage‐activated Ca2+ currents in rat supraoptic neurones: Biophysical properties, expression of the various channel alpha1 subunits. J Neuroendocrinol 13: 638‐649, 2001.
 95.Juraska JM, Wilson CJ, Groves PM. The substantia nigra of the rat: A Golgi study. J Comp Neurol 172: 585‐600, 1977.
 96.Jurgutis P, Shuang R, Fletcher A, Stuenkel EL. Characterization, distribution of SNARE proteins at neuroendocrine nerve endings. Neuroendocrinology 64: 379‐392, 1996.
 97.Kalivas PW, Duffy P. A comparison of axonal, somatodendritic dopamine release using in vivo dialysis. J Neurochem 56: 961‐967, 1991.
 98.Kendrick KM. Microdialysis measurement of in vivo neuropeptide release. J Neurosci Meth 34: 35‐46, 1990.
 99.Kennedy MJ, Ehlers MD. Mechanisms, function of dendritic exocytosis. Neuron 69: 856‐875, 2011.
 100.Kim JI, Ganesan S, Luo SX, Wu YW, Park E, Huang EJ, Chen L, Ding JB. Aldehyde dehydrogenase 1a1 mediates a GABA synthesis pathway in midbrain dopaminergic neurons. Science 350: 102‐106, 2015.
 101.Kim Y, Park MK, Chung S. Voltage‐operated Ca2+ channels regulate dopamine release from somata of dopamine neurons in the substantia nigra pars compacta. Biochem Biophys Res Commun 373: 665‐669, 2008.
 102.Kim Y, Park MK, Chung S. Regulation of somatodendritic dopamine release by corticotropin‐releasing factor via the inhibition of voltage‐operated Ca2+ channels. Neurosci Lett 465: 31‐35, 2009.
 103.Knobloch HS, Charlet A, Hoffmann LC, Eliava M, Khrulev S, Cetin AH, Osten P, Schwarz MK, Seeburg PH, Stoop R, Grinevich V. Evoked axonal oxytocin release in the central amygdala attenuates fear response. Neuron 73: 553‐566, 2012.
 104.Kombian SB, Mouginot D, Pittman QJ. Dendritically released peptides act as retrograde modulators of afferent excitation in the supraoptic nucleus in vitro. Neuron 19: 903‐912, 1997.
 105.Komori Y, Tanaka M, Kuba M, Ishii M, Abe M, Kitamura N, Verkhratsky A, Shibuya I, Dayanithi G. Ca(2+) homeostasis, Ca(2+) signalling, somatodendritic vasopressin release in adult rat supraoptic nucleus neurones. Cell Calcium 48: 324‐332, 2010.
 106.Koos T, Tecuapetla F, Tepper JM. Glutamatergic signaling by midbrain dopaminergic neurons: Recent insights from optogenetic, molecular, behavioral studies. Cur Opin Neurobiol 21: 393‐401, 2011.
 107.Lambert RC, Dayanithi G, Moos FC, Richard P. A rise in the intracellular Ca2+ concentration of isolated rat supraoptic cells in response to oxytocin. J Physiol 478: 275‐287, 1994.
 108.Lambert RC, Moos FC, Richard P. Action of endogenous oxytocin within the paraventricular or supraoptic nuclei: A powerful link in the regulation of the bursting pattern of oxytocin neurons during the milk‐ejection reflex in rats. Neuroscience 57: 1027‐1038, 1993.
 109.Landgraf R, Kuba M, Holsboer F, Wotjak CT. Release of vasopressin, oxytocin within the brain, into blood: Microdialysis, antisense targeting. In: Neurohypophysis: Recent Progress of Vasopressin, Oxytocin Research edited by Saito T, Kurokawa K, and Yoshida S. Amsterdam: Elesevier, 1995, pp. 243‐256.
 110.Landgraf R, Neumann I, Russell JA, Pittman QJ. Push‐pull perfusion, microdialysis studies of central oxytocin, vasopressin release in freely moving rats during pregnancy, parturition, lactation. Ann New York Acad Sci 652: 326‐339, 1992.
 111.Landgraf R, Neumann ID. Vasopressin, oxytocin release within the brain: A dynamic concept of multiple, variable modes of neuropeptide communication. Front Neuroendocrinol 25: 150‐176, 2004.
 112.Landry M, Vila‐Porcile E, Hokfelt T, Calas A. Differential routing of coexisting neuropeptides in vasopressin neurons. Eur J Neurosci 17: 579‐589, 2003.
 113.Le Meur K, Galante M, Angulo MC, Audinat E. Tonic activation of NMDA receptors by ambient glutamate of non‐synaptic origin in the rat hippocampus. J Physiol 580: 373‐383, 2007.
 114.Leng G, Brown CH, Russell JA. Physiological pathways regulating the activity of magnocellular neurosecretory cells. Prog Neurobiol 57: 625‐655, 1999.
 115.Leng G, Ludwig M. Jacques Benoit Lecture. Information processing in the hypothalamus: peptides, analogue computation. J Neuroendocrinol 18: 379‐392, 2006.
 116.Leng G, Ludwig M. Neurotransmitters, peptides: Whispered secrets, public announcements. J Physiol 586: 5625‐5632, 2008.
 117.Leszczyszyn DJ, Jankowski JA, Viveros OH, Diliberto EJ, Jr., Near JA, Wightman RM. Nicotinic receptor‐mediated catecholamine secretion from individual chromaffin cells. Chemical evidence for exocytosis. J Biol Chem 265: 14736‐14737, 1990.
 118.Leviel V. The reverse transport of DA, what physiological significance? Neurochem Int 38: 83‐106, 2001.
 119.Ludwig M. Dendritic Neurotransmitter Release. New York: Springer, 2005.
 120.Ludwig M. Dendritic release of vasopressin, oxytocin. J Neuroendocrinol 10: 881‐895, 1998.
 121.Ludwig M, Bull PM, Tobin VA, Sabatier N, Landgraf R, Dayanithi G, Leng G. Regulation of activity‐dependent dendritic vasopressin release from rat supraoptic neurones. J Physiol 564: 515‐522, 2005.
 122.Ludwig M, Callahan MF, Landgraf R, Johnson AK, Morris M. Neural input modulates osmotically stimulated release of vasopressin into the supraoptic nucleus. Am J Physiol 270: E787‐E792, 1996.
 123.Ludwig M, Callahan MF, Morris M. Effects of tetrodotoxin on osmotically stimulated central, peripheral vasopressin, oxytocin release. Neuroendocrinology 62: 619‐627, 1995.
 124.Ludwig M, Callahan MF, Neumann I, Landgraf R, Morris M. Systemic osmotic stimulation increases vasopressin, oxytocin release within the supraoptic nucleus. J Neuroendocrinol 6: 369‐373, 1994.
 125.Ludwig M, Johnstone LE, Neumann I, Landgraf R, Russell JA. Direct hypertonic stimulation of the rat supraoptic nucleus increases c‐fos expressionin glial cells rather than magnocellular neurones. Cell Tissue Res 287: 79‐90, 1997.
 126.Ludwig M, Leng G. Autoinhibition of supraoptic nucleus vasopressin neurons in vivo: A combined retrodialysis/electrophysiological study in rats. Eur J Neurosci 9: 2532‐2540, 1997.
 127.Ludwig M, Leng G. Dendritic peptide release, peptide‐dependent behaviours. Nat Rev Neurosci 7: 126‐136, 2006.
 128.Ludwig M, Pittman QJ. Talking back: Dendritic neurotransmitter release. Trends Neurosci 26: 255‐261, 2003.
 129.Ludwig M, Sabatier N, Bull PM, Landgraf R, Dayanithi G, Leng G. Intracellular calcium stores regulate activity‐dependent neuropeptide release from dendrites. Nature 418: 85‐89, 2002.
 130.Ludwig M, Williams K, Callahan MF, Morris M. Salt loading abolishes osmotically stimulated vasopressin release within the supraoptic nucleus. Neurosci Lett 215: 1‐4, 1996.
 131.Mabrouk OS, Kennedy RT. Simultaneous oxytocin, arg‐vasopressin measurements in microdialysates using capillary liquid chromatography‐mass spectrometry. J Neurosci Meth 209: 127‐133, 2012.
 132.Maletic‐Savatic M, Koothan T, Malinow R. Calcium‐evoked dendritic exocytosis in cultured hippocampal neurons. Part II: Mediation by calcium/calmodulin‐dependent protein kinase II. J Neurosci 18: 6814‐6821, 1998.
 133.Maletic‐Savatic M, Malinow R. Calcium‐evoked dendritic exocytosis in cultured hippocampal neurons. Part I: Trans‐Golgi network‐derived organelles undergo regulated exocytosis. J Neurosci 18: 6803‐6813, 1998.
 134.Mallet N, Pogosyan A, Sharott A, Csicsvari J, Bolam JP, Brown P, Magill PJ. Disrupted dopamine transmission, the emergence of exaggerated beta oscillations in subthalamic nucleus, cerebral cortex. J Neurosci 28: 4795‐4806, 2008.
 135.Mansvelder HD, Kits KS. Calcium channels, the release of large dense core vesicles from neuroendocrine cells: Spatial organization, functional coupling. Prog Neurobiol 62: 427‐441, 2000.
 136.Martin TF. Tuning exocytosis for speed: Fast, slow modes. Biochim Biophys Acta 1641: 157‐165, 2003.
 137.Mason WT. Supraoptic neurones of rat hypothalamus are osmosensitive. Nature 287: 154‐157, 1980.
 138.Mason WT, Hatton GI, Ho YW, Chapman C, Robinson IC. Central release of oxytocin, vasopressin, neurophysin by magnocellular neurone depolarization: Evidence in slices of guinea pig, rat hypothalamus. Neuroendocrinology 42: 311‐322, 1986.
 139.Matsuda W, Furuta T, Nakamura KC, Hioki H, Fujiyama F, Arai R, Kaneko T. Single nigrostriatal dopaminergic neurons form widely spread, highly dense axonal arborizations in the neostriatum. J Neurosci 29: 444‐453, 2009.
 140.Matsutani S, Yamamoto N. Postnatal development of dendritic spines on olfactory bulb granule cells in rats. J Comp Neurol 473: 553‐561, 2004.
 141.Mebel DM, Wong JC, Dong YJ, Borgland SL. Insulin in the ventral tegmental area reduces hedonic feeding, suppresses dopamine concentration via increased reuptake. Eur J Neurosci 36: 2336‐2346, 2012.
 142.Meinrenken CJ, Borst JG, Sakmann B. Local routes revisited: The space, time dependence of the Ca2+ signal for phasic transmitter release at the rat calyx of Held. J Physiol 547: 665‐689, 2003.
 143.Mendez JA, Bourque MJ, Fasano C, Kortleven C, Trudeau LE. Somatodendritic dopamine release requires synaptotagmin 4, 7, the participation of voltage‐gated calcium channels. J Biol Chem 286: 23928‐23937, 2011.
 144.Mens WB, Witter A, van Wimersma Greidanus TB. Penetration of neurohypophyseal hormones from plasma into cerebrospinal fluid (CSF): Half‐times of disappearance of these neuropeptides from CSF. Brain Res 262: 143‐149, 1983.
 145.Mercer L, del Fiacco M, Cuello AC. The smooth endoplasmic reticulum as a possible storage site for dendritic dopamine in substantia nigra neurones. Experientia 35: 101‐103, 1979.
 146.Millar J, Stamford JA, Kruk ZL, Wightman RM. Electrochemical, pharmacological, electrophysiological evidence of rapid dopamine release, removal in the rat caudate nucleus following electrical stimulation of the median forebrain bundle. Eur J Pharmacol 109: 341‐348, 1985.
 147.Miyata S, Hatton GI. Activity‐related, dynamic neuron‐glial interactions in the hypothalamo‐neurohypophysial system. Microscopy Res Tech 56: 143‐157, 2002.
 148.Miyata S, Khan AM, Hatton GI. Colocalization of calretinin, calbindin‐D28k with oxytocin, vasopressin in rat supraoptic nucleus neurons: A quantitative study. Brain Res 785: 178‐182, 1998.
 149.Miyazaki T, Lacey MG. Presynaptic inhibition by dopamine of a discrete component of GABA release in rat substantia nigra pars reticulata. J Physiol 513: 805‐817, 1998.
 150.Moos F, Poulain DA, Rodriguez F, Guerne Y, Vincent JD, Richard P. Release of oxytocin within the supraoptic nucleus during the milk ejection reflex in rats. Exp Brain Res 76: 593‐602, 1989.
 151.Morgan A. Exocytosis. Essays Biochem 30: 77‐95, 1995.
 152.Moriguchi A, Ferrario CM, Brosnihan KB, Ganten D, Morris M. Differential regulation of central vasopressin in transgenic rats harboring the mouse Ren‐2 gene. Am J Physiol 267: R786‐791, 1994.
 153.Morikawa H, Khodakhah K, Williams JT. Two intracellular pathways mediate metabotropic glutamate receptor‐induced Ca2+ mobilization in dopamine neurons. J Neurosci 23: 149‐157, 2003.
 154.Morikawa H, Paladini CA. Dynamic regulation of midbrain dopamine neuron activity: Intrinsic, synaptic, plasticity mechanisms. Neuroscience 198: 95‐111, 2011.
 155.Morris JF, Ludwig M. Magnocellular dendrites: Prototypic receiver/transmitters. J Neuroendocrinol 16: 403‐408, 2004.
 156.Morris JF, Pow DV. New anatomical insights into the inputs, outputs from hypothalamic magnocellular neurons. Ann New York Acad Sci 689: 16‐33, 1993.
 157.Morris JF, Pow DV. Widespread release of peptides in the central nervous system: Quantitation of tannic acid‐captured exocytoses. Anat Record 231: 437‐445, 1991.
 158.Morris JF, Pow DV, Sokol HW, Ward A. Dendritic release of peptides from magnocellular neurons in normal rats, Brattleboro rats, mice with hereditary nephrogenic diabetes insipidus. In: Vasopressin, edited by Gross P, Richter D, and Roberston GL. Paris: John Libbey Eurotext, 1993, pp. 171‐182.
 159.Morris M, Alexander N. Baroreceptor influences on oxytocin, vasopressin secretion. Hypertension 13: 110‐114, 1989.
 160.Morris M, Barnard RR, Jr., Sain LE. Osmotic mechanisms regulating cerebrospinal fluid vasopressin, oxytocin in the conscious rat. Neuroendocrinology 39: 377‐383, 1984.
 161.Murase T, Kondo K, Otake K, Oiso Y. Pituitary adenylate cyclase‐activating polypeptide stimulates arginine vasopressin release in conscious rats. Neuroendocrinology 57: 1092‐1096, 1993.
 162.Naskar K, Stern JE. A functional coupling between extrasynaptic NMDA receptors, A‐type K+ channels under astrocyte control regulates hypothalamic neurosecretory neuronal activity. J Physiol 592: 2813‐2827, 2014.
 163.Neumann I, Douglas AJ, Pittman QJ, Russell JA, Landgraf R. Oxytocin released within the supraoptic nucleus of the rat brain by positive feedback action is involved in parturition‐related events. J Neuroendocrinol 8: 227‐233, 1996.
 164.Neumann I, Koehler E, Landgraf R, Summy‐Long J. An oxytocin receptor antagonist infused into the supraoptic nucleus attenuates intranuclear, peripheral release of oxytocin during suckling in conscious rats. Endocrinology 134: 141‐148, 1994.
 165.Neumann I, Landgraf R, Takahashi Y, Pittman QJ, Russell JA. Stimulation of oxytocin release within the supraoptic nucleus, into blood by CCK‐8. Am J Physiol 267: R1626‐R1631, 1994.
 166.Neumann I, Ludwig M, Engelmann M, Pittman QJ, Landgraf R. Simultaneous microdialysis in blood, brain: Oxytocin, vasopressin release in response to central, peripheral osmotic stimulation, suckling in the rat. Neuroendocrinology 58: 637‐645, 1993.
 167.Neumann I, Russell JA, Landgraf R. Oxytocin, vasopressin release within the supraoptic, paraventricular nuclei of pregnant, parturient, lactating rats: A microdialysis study. Neuroscience 53: 65‐75, 1993.
 168.Neumann ID, Landgraf R. Balance of brain oxytocin, vasopressin: Implications for anxiety, depression, social behaviors. Trends Neurosci 35: 649‐659, 2012.
 169.Nieoullon A, Cheramy A, Glowinski J. Release of dopamine in vivo from cat substantia nigra. Nature 266: 375‐377, 1977.
 170.Nirenberg MJ, Chan J, Liu Y, Edwards RH, Pickel VM. Ultrastructural localization of the vesicular monoamine transporter‐2 in midbrain dopaminergic neurons: Potential sites for somatodendritic storage, release of dopamine. J Neurosci 16: 4135‐4145, 1996.
 171.Nirenberg MJ, Chan J, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM. Immunogold localization of the dopamine transporter: An ultrastructural study of the rat ventral tegmental area. J Neurosci 17: 5255‐5262, 1997.
 172.Nirenberg MJ, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM. The dopamine transporter is localized to dendritic, axonal plasma membranes of nigrostriatal dopaminergic neurons. J Neurosci 16: 436‐447, 1996.
 173.Nissen R, Hu B, Renaud LP. Regulation of spontaneous phasic firing of rat supraoptic vasopressin neurones in vivo by glutamate receptors. J Physiol 484: 415‐424, 1995.
 174.Nissen R, Renaud LP. GABA receptor mediation of median preoptic nucleus‐evoked inhibition of supraoptic neurosecretory neurones in rat. J Physiol 479: 207‐216, 1994.
 175.Oliet SH, Baimoukhametova DV, Piet R, Bains JS. Retrograde regulation of GABA transmission by the tonic release of oxytocin, endocannabinoids governs postsynaptic firing. J Neurosci 27: 1325‐1333, 2007.
 176.Oliet SH, Bourque CW. Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature 364: 341‐343, 1993.
 177.Opazo F, Schulz JB, Falkenburger BH. PKC links Gq‐coupled receptors to DAT‐mediated dopamine release. J Neurochem 114: 587‐596, 2010.
 178.Ota M, Crofton JT, Festavan G, Share L. Central carbachol stimulates vasopressin release into interstitial fluid adjacent to the paraventricular nucleus. Brain Res 592: 249‐254, 1992.
 179.Ota M, Crofton JT, Share L. Hemorrhage‐induced vasopressin release in the paraventricular nucleus measured by in vivo microdialysis. Brain Res 658: 49‐54, 1994.
 180.Ovsepian SV, Dolly JO. Dendritic SNAREs add a new twist to the old neuron theory. Proc Natl Acad Sci U S A 108: 19113‐19120, 2011.
 181.Palmiter RD. Dopamine signaling as a neural correlate of consciousness. Neuroscience 198: 213‐220, 2011.
 182.Paquet M, Tremblay M, Soghomonian JJ, Smith Y. AMPA, NMDA glutamate receptor subunits in midbrain dopaminergic neurons in the squirrel monkey: An immunohistochemical, in situ hybridization study. J Neurosci 17: 1377‐1396, 1997.
 183.Patel JC, Rice ME. Monitoring axonal, somatodendritic dopamine release using fast‐scan cyclic voltammetry in brain slices. Meth Mol Biol 964: 243‐273, 2013.
 184.Patel JC, Witkovsky P, Avshalumov MV, Rice ME. Mobilization of calcium from intracellular stores facilitates somatodendritic dopamine release. J Neurosci 29: 6568‐6579, 2009.
 185.Pickel VM, Nirenberg MJ, Milner TA. Ultrastructural view of central catecholaminergic transmission: Immunocytochemical localization of synthesizing enzymes, transporters, receptors. J Neurocytol 25: 843‐856, 1996.
 186.Potapenko ES, Biancardi VC, Florschutz RM, Ryu PD, Stern JE. Inhibitory‐excitatory synaptic balance is shifted toward increased excitation in magnocellular neurosecretory cells of heart failure rats. J Neurophysiol 106: 1545‐1557, 2011.
 187.Potapenko ES, Biancardi VC, Zhou Y, Stern JE. Astrocytes modulate a postsynaptic NMDA‐GABAA‐receptor crosstalk in hypothalamic neurosecretory neurons. J Neurosci 33: 631‐640, 2013.
 188.Pothos EN, Davila V, Sulzer D. Presynaptic recording of quanta from midbrain dopamine neurons, modulation of the quantal size. J Neurosci 18: 4106‐4118, 1998.
 189.Pow DV, Morris JF. Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis. Neuroscience 32: 435‐439, 1989.
 190.Prior IA, Clague MJ. Glutamate uptake occurs at an early stage of synaptic vesicle recycling. Curr Biol 7: 353‐356, 1997.
 191.Pucak ML, Grace AA. Evidence that systemically administered dopamine antagonists activate dopamine neuron firing primarily by blockade of somatodendritic autoreceptors. J Pharmacol Exp Ther 271: 1181‐1192, 1994.
 192.Radnikow G, Misgeld U. Dopamine D1 receptors facilitate GABAA synaptic currents in the rat substantia nigra pars reticulata. J Neurosci 18: 2009‐2016, 1998.
 193.Redgrave P, Vautrelle N, Reynolds JN. Functional properties of the basal ganglia's re‐entrant loop architecture: Selection, reinforcement. Neuroscience 198: 138‐151, 2011.
 194.Rice ME. Distinct regional differences in dopamine‐mediated volume transmission. Prog Brain Res 125: 277‐290, 2000.
 195.Rice ME, Cragg SJ. Dopamine spillover after quantal release: Rethinking dopamine transmission in the nigrostriatal pathway. Brain Res Rev 58: 303‐313, 2008.
 196.Rice ME, Cragg SJ, Greenfield SA. Characteristics of electrically evoked somatodendritic dopamine release in substantia nigra, ventral tegmental area in vitro. J Neurophysiol 77: 853‐862, 1997.
 197.Rice ME, Patel JC, Cragg SJ. Dopamine release in the basal ganglia. Neuroscience 198: 112‐137, 2011.
 198.Rice ME, Richards CD, Nedergaard S, Hounsgaard J, Nicholson C, Greenfield SA. Direct monitoring of dopamine, 5‐HT release in substantia nigra, ventral tegmental area in vitro. Exp Brain Res 100: 395‐406, 1994.
 199.Robertson GS, Damsma G, Fibiger HC. Characterization of dopamine release in the substantia nigra by in vivo microdialysis in freely moving rats. J Neurosci 11: 2209‐2216, 1991.
 200.Robertson GS, Robertson HA. Evidence that L‐dopa‐induced rotational behavior is dependent on both striatal, nigral mechanisms. J Neurosci 9: 3326‐3331, 1989.
 201.Rossoni E, Feng J, Tirozzi B, Brown D, Leng G, Moos F. Emergent synchronous bursting of oxytocin neuronal network. PLoS Comp Biol 4: e1000123, 2008.
 202.Russell JA, Leng G, Douglas AJ. The magnocellular oxytocin system, the fount of maternity: Adaptations in pregnancy. Front Neuroendocrinol 24: 27‐61, 2003.
 203.Russell JA, Neumann I, Landgraf R. Oxytocin, vasopressin release in discrete brain areas after naloxone in morphine‐tolerant, ‐dependent anesthetized rats: Push‐pull perfusion study. J Neurosci 12: 1024‐1032, 1992.
 204.Sabatier N, Caquineau C, Dayanithi G, Bull P, Douglas AJ, Guan XM, Jiang M, Van der Ploeg L, Leng G. Alpha‐melanocyte‐stimulating hormone stimulates oxytocin release from the dendrites of hypothalamic neurons while inhibiting oxytocin release from their terminals in the neurohypophysis. J Neurosci 23: 10351‐10358, 2003.
 205.Sabatier N, Richard P, Dayanithi G. L‐, N‐, T‐ but neither P‐ nor Q‐type Ca2+ channels control vasopressin‐induced Ca2+ influx in magnocellular vasopressin neurones isolated from the rat supraoptic nucleus. J Physiol 503: 253‐268, 1997.
 206.Sabatier N, Shibuya I, Dayanithi G. Intracellular calcium increase, somatodendritic vasopressin release by vasopressin receptor agonists in the rat supraoptic nucleus: Involvement of multiple intracellular transduction signals. J Neuroendocrinol 16: 221‐236, 2004.
 207.Sah P, Hestrin S, Nicoll RA. Tonic activation of NMDA receptors by ambient glutamate enhances excitability of neurons. Science 246: 815‐818, 1989.
 208.Salio C, Lossi L, Ferrini F, Merighi A. Neuropeptides as synaptic transmitters. Cell Tissue Res 326: 583‐598, 2006.
 209.Salvatore MF, Pruett BS. Dichotomy of tyrosine hydroxylase, dopamine regulation between somatodendritic, terminal field areas of nigrostriatal, mesoaccumbens pathways. PloS One 7: e29867, 2012.
 210.Santiago M, Machado A, Cano J. Fast sodium channel dependency of the somatodendritic release of dopamine in the rat's brain. Neurosci Lett 148: 145‐147, 1992.
 211.Santiago M, Westerink BH. Characterization, pharmacological responsiveness of dopamine release recorded by microdialysis in the substantia nigra of conscious rats. J Neurochem 57: 738‐747, 1991.
 212.Schoffelmeer AN, Drukarch B, De Vries TJ, Hogenboom F, Schetters D, Pattij T. Insulin modulates cocaine‐sensitive monoamine transporter function, impulsive behavior. J Neurosci 31: 1284‐1291, 2011.
 213.Sesack SR, Aoki C, Pickel VM. Ultrastructural localization of D2 receptor‐like immunoreactivity in midbrain dopamine neurons, their striatal targets. J Neurosci 14: 88‐106, 1994.
 214.Shaw FD, Morris JF. Calcium localization in the rat neurohypophysis. Nature 287: 56‐58, 1980.
 215.Shibuya I, Noguchi J, Tanaka K, Harayama N, Inoue U, Kabashima N, Ueta Y, Hattori Y, Yamashita H. PACAP increases the cytosolic Ca2+ concentration, stimulates somatodendritic vasopressin release in rat supraoptic neurons. J Neuroendocrinol 10: 31‐42, 1998.
 216.Simmons ML, Terman GW, Gibbs SM, Chavkin C. L‐type calcium channels mediate dynorphin neuropeptide release from dendrites but not axons of hippocampal granule cells. Neuron 14: 1265‐1272, 1995.
 217.Sladek CD. Regulation of vasopressin release by neurotransmitters, neuropeptides, osmotic stimuli. Prog Brain Res 60: 71‐90, 1983.
 218.Son SJ, Filosa JA, Potapenko ES, Biancardi VC, Zheng H, Patel KP, Tobin VA, Ludwig M, Stern JE. Dendritic peptide release mediates interpopulation crosstalk between neurosecretory, preautonomic networks. Neuron 78: 1036‐1049, 2013.
 219.Staal RG, Mosharov EV, Sulzer D. Dopamine neurons release transmitter via a flickering fusion pore. Nature Neurosci 7: 341‐346, 2004.
 220.Stern JE. Neuroendocrine‐autonomic integration in the PVN: Novel roles for dendritically released neuropeptides. J Neuroendocrinol 27: 487‐497, 2015.
 221.Stern JE, Armstrong WE. Reorganization of the dendritic trees of oxytocin, vasopressin neurons of the rat supraoptic nucleus during lactation. J Neurosci 18: 841‐853, 1998.
 222.Stern JE, Potapenko ES. Enhanced NMDA receptor‐mediated intracellular calcium signaling in magnocellular neurosecretory neurons in heart failure rats. Am J Physiol 305: R414‐R422, 2013.
 223.Stocker SD, Keith KJ, Toney GM. Acute inhibition of the hypothalamic paraventricular nucleus decreases renal sympathetic nerve activity, arterial blood pressure in water‐deprived rats. Am J Physiol 286: R719‐R725, 2004.
 224.Stoop R. Neuromodulation by oxytocin, vasopressin. Neuron 76: 142‐159, 2012.
 225.Straub C, Tritsch NX, Hagan NA, Gu C, Sabatini BL. Multiphasic modulation of cholinergic interneurons by nigrostriatal afferents. J Neurosci 34: 8557‐8569, 2014.
 226.Stuart G, Spruston N, Hausser M. Dendrites. Oxford: Oxford University Press, 1999.
 227.Stuart G, Spruston N, Sakmann B, Hausser M. Action potential initiation, backpropagation in neurons of the mammalian CNS. Trends Neurosci 20: 125‐131, 1997.
 228.Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J Neurosci 30: 8229‐8233, 2010.
 229.Sudhof TC. The synaptic vesicle cycle. Ann Rev Neurosci 27: 509‐547, 2004.
 230.Sulzer D, Chen TK, Lau YY, Kristensen H, Rayport S, Ewing A. Amphetamine redistributes dopamine from synaptic vesicles to the cytosol, promotes reverse transport. J Neurosci 15: 4102‐4108, 1995.
 231.Tecuapetla F, Patel JC, Xenias H, English D, Tadros I, Shah F, Berlin J, Deisseroth K, Rice ME, Tepper JM, Koos T. Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J Neurosci 30: 7105‐7110, 2010.
 232.Thompson TL, Moss RL. Estrogen regulation of dopamine release in the nucleus accumbens: Genomic‐, nongenomic‐mediated effects. J Neurochem 62: 1750‐1756, 1994.
 233.Timmerman W, Abercrombie ED. Amphetamine‐induced release of dendritic dopamine in substantia nigra pars reticulata: D1‐mediated behavioral, electrophysiological effects. Synapse 23: 280‐291, 1996.
 234.Tobin V, Leng G, Ludwig M. The involvement of actin, calcium channels, exocytosis proteins in somato‐dendritic oxytocin, vasopressin release. Front Physiol 3: 261, 2012.
 235.Tobin V, Schwab Y, Lelos N, Onaka T, Pittman QJ, Ludwig M. Expression of exocytosis proteins in rat supraoptic nucleus neurones. J Neuroendocrinol 24: 629‐641, 2012.
 236.Tobin VA, Douglas AJ, Leng G, Ludwig M. The involvement of voltage‐operated calcium channels in somato‐dendritic oxytocin release. PloS One 6: e25366, 2011.
 237.Tobin VA, Hurst G, Norrie L, Dal Rio FP, Bull PM, Ludwig M. Thapsigargin‐induced mobilization of dendritic dense‐cored vesicles in rat supraoptic neurons. Eur J Neurosci 19: 2909‐2912, 2004.
 238.Tobin VA, Ludwig M. The role of the actin cytoskeleton in oxytocin, vasopressin release from rat supraoptic nucleus neurons. J Physiol 582: 1337‐1348, 2007.
 239.Trevitt JT, Carlson BB, Nowend K, Salamone JD. Substantia nigra pars reticulata is a highly potent site of action for the behavioral effects of the D1 antagonist SCH 23390 in the rat. Psychopharmacology 156: 32‐41, 2001.
 240.Tritsch NX, Ding JB, Sabatini BL. Dopaminergic neurons inhibit striatal output through non‐canonical release of GABA. Nature 490: 262‐266, 2012.
 241.Trueta C, De‐Miguel FF. Extrasynaptic exocytosis, its mechanisms: A source of molecules mediating volume transmission in the nervous system. Front Physiol 3: 319, 2012.
 242.Trueta C, Sanchez‐Armass S, Morales MA, De‐Miguel FF. Calcium‐induced calcium release contributes to somatic secretion of serotonin in leech Retzius neurons. J Neurobiol 61: 309‐316, 2004.
 243.Verbalis JG, McCann MJ, McHale CM, Stricker EM. Oxytocin secretion in response to cholecystokinin, food: Differentiation of nausea from satiety. Science 232: 1417‐1419, 1986.
 244.Verkhratsky A. Physiology, pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 85: 201‐279, 2005.
 245.Vitale ML, Seward EP, Trifaro JM. Chromaffin cell cortical actin network dynamics control the size of the release‐ready vesicle pool, the initial rate of exocytosis. Neuron 14: 353‐363, 1995.
 246.Voorn P, Vanderschuren LJ, Groenewegen HJ, Robbins TW, Pennartz CM. Putting a spin on the dorsal‐ventral divide of the striatum. Trends Neurosci 27: 468‐474, 2004.
 247.Wang D, Fisher TE. Expression of CaV 2.2, splice variants of CaV 2.1 in oxytocin‐, vasopressin‐releasing supraoptic neurones. J Neuroendocrinol 26: 100‐110, 2014.
 248.Wang YF, Hatton GI. Mechanisms underlying oxytocin‐induced excitation of supraoptic neurons: Prostaglandin mediation of actin polymerization. J Neurophysiol 95: 3933‐3947, 2006.
 249.Wassef M, Berod A, Sotelo C. Dopaminergic dendrites in the pars reticulata of the rat substantia nigra, their striatal input. Combined immunocytochemical localization of tyrosine hydroxylase, anterograde degeneration. Neuroscience 6: 2125‐2139, 1981.
 250.Watson SJ, Akil H, Fischli W, Goldstein A, Zimmerman E, Nilaver G, van Wimersma Greidanus TB. Dynorphin, vasopressin: Common localization in magnocellular neurons. Science 216: 85‐87, 1982.
 251.Wichmann T, Dostrovsky JO. Pathological basal ganglia activity in movement disorders. Neuroscience 198: 232‐244, 2011.
 252.Widmer H, Ludwig M, Bancel F, Leng G, Dayanithi G. Neurosteroid regulation of oxytocin, vasopressin release from the rat supraoptic nucleus. J Physiol 548: 233‐244, 2003.
 253.Wilson CJ, Groves PM, Fifkova E. Monoaminergic synapses, including dendro‐dendritic synapses in the rat substantia nigra. Exp Brain Res 30: 161‐174, 1977.
 254.Witkovsky P, Patel JC, Lee CR, Rice ME. Immunocytochemical identification of proteins involved in dopamine release from the somatodendritic compartment of nigral dopaminergic neurons. Neuroscience 164: 488‐496, 2009.
 255.Wotjak CT, Ganster J, Kohl G, Holsboer F, Landgraf R, Engelmann M. Dissociated central, peripheral release of vasopressin, but not oxytocin, in response to repeated swim stress: New insights into the secretory capacities of peptidergic neurons. Neuroscience 85: 1209‐1222, 1998.
 256.Wotjak CT, Landgraf R, Engelmann M. Listening to neuropeptides by microdialysis: Echoes, new sounds? Pharmacol Biochem Behav 90: 125‐134, 2008.
 257.Wotjak CT, Ludwig M, Ebner K, Russell JA, Singewald N, Landgraf R, Engelmann M. Vasopressin from hypothalamic magnocellular neurons has opposite actions at the adenohypophysis, in the supraoptic nucleus on ACTH secretion. Eur J Neurosci 16: 477‐485, 2002.
 258.Wotjak CT, Ludwig M, Landgraf R. Vasopressin facilitates its own release within the rat supraoptic nucleus in vivo. Neuroreport 5: 1181‐1184, 1994.
 259.Xu J, Mashimo T, Sudhof TC. Synaptotagmin‐1, ‐2, ‐9: Ca(2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54: 567‐581, 2007.
 260.Yung KK. Localization of ionotropic, metabotropic glutamate receptors in distinct neuronal elements of the rat substantia nigra. Neurochem Inter 33: 313‐326, 1998.
 261.Yung KK, Bolam JP, Smith AD, Hersch SM, Ciliax BJ, Levey AI. Immunocytochemical localization of D1, D2 dopamine receptors in the basal ganglia of the rat: Light, electron microscopy. Neuroscience 65: 709‐730, 1995.
 262.Zhang K, Patel KP. Effect of nitric oxide within the paraventricular nucleus on renal sympathetic nerve discharge: Role of GABA. Am J Physiol 275: R728‐R734, 1998.
 263.Zhang Z, Bhalla A, Dean C, Chapman ER, Jackson MB. Synaptotagmin IV: A multifunctional regulator of peptidergic nerve terminals. Nature Neurosci 12: 163‐171, 2009.
 264.Zhang ZW, Kang JI, Vaucher E. Axonal varicosity density as an index of local neuronal interactions. PloS One 6: e22543, 2011.
 265.Zhou FW, Jin Y, Matta SG, Xu M, Zhou FM. An ultra‐short dopamine pathway regulates basal ganglia output. J Neurosci 29: 10424‐10435, 2009.
 266.Zilberter Y, Harkany T, Holmgren CD. Dendritic release of retrograde messengers controls synaptic transmission in local neocortical networks. Neuroscientist 11: 334‐344, 2005.

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Mike Ludwig, David Apps, John Menzies, Jyoti C. Patel, Margaret E. Rice. Dendritic Release of Neurotransmitters. Compr Physiol 2016, 7: 235-252. doi: 10.1002/cphy.c160007