PKC-mediated GABAergic enhancement of dopaminergic responses: Implication for short-term potentiation at a dual-transmitter synapse

Journal of Neurophysiology

Volumn 112, Issue 1, 2014, Pages 22-29

  Svensson, Erik ^a   Proekt, Alex ^a   Jing, Jian ^a   Weiss, Klaudiusz R ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Buccal ganglia; Classical transmitters; Co transmission; Neuromodulation; Synaptic plasticity

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; DOPAMINE; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; PROTEIN KINASE C; SEROTONIN 3 RECEPTOR; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR;

ANIMAL EXPERIMENT; APLYSIA; ARTICLE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC TRANSMISSION; ELECTRIC CURRENT; ENZYME ACTIVATION; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; MOLECULAR MECHANICS; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC TRANSMISSION; ANIMAL; DOPAMINERGIC NERVE CELL; DRUG EFFECTS; METABOLISM; PHYSIOLOGY;

ANIMALS; APLYSIA; DOPAMINE; DOPAMINERGIC NEURONS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA-B RECEPTOR AGONISTS; GABA-B RECEPTOR ANTAGONISTS; GABAERGIC NEURONS; GAMMA-AMINOBUTYRIC ACID; NEURONAL PLASTICITY; PROTEIN KINASE C; SYNAPSES;

EID: 84903626406     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00794.2013     Document Type: Article

References (63)

1. Antonov I, Kandel ER, Hawkins RD. Presynaptic and postsynaptic mechanisms of synaptic plasticity and metaplasticity during intermediate-term memory formation in Aplysia. J Neurosci 30: 5781-5791, 2010.
2. Barbas D, Zappulla JP, Angers S, Bouvier M, Mohamed HA, Byrne JH, Castellucci VF, DesGroseillers L. An aplysia dopamine1-like receptor: molecular and functional characterization. J Neurochem 96: 414-427, 2006.
3. Barreiro-Iglesias A, Villar-Cerviño V, Anadón R, Rodicio MC. Dopamine and Y-aminobutyric acid are colocalized in restricted groups of neurons in the sea lamprey brain: insights into the early evolution of neurotransmitter colocalization in vertebrates. J Anat 215: 601-610, 2009.
4. Braha O, Dale N, Hochner B, Klein M, Abrams TW, Kandel ER. Second messengers involved in the two processes of presynaptic facilitation that contribute to sensitization and dishabituation in Aplysia sensory neurons. Proc Natl Acad Sci USA 87: 2040-2044, 1990.
5. 2+ current of the sensory neurons in Aplysia. J Neurosci 13: 1839-1851, 1993.
6. Bray JG, Mynlieff M. Involvement of protein kinase C and protein kinase A in the enhancement of L-type calcium current by GABAB receptor activation in neonatal hippocampus. Neuroscience 179: 62-72, 2011.
7. Brenowitz S, David J, Trussell L. Enhancement of synaptic efficacy by presynaptic GABA(B) receptors. Neuron 20: 135-141, 1998.
8. Brunelli M, Castellucci V, Kandel ER. Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science 194: 1178-1181, 1976.
9. Chitwood RA, Li Q, Glanzman DL. Serotonin facilitates AMPA-type responses in isolated siphon motor neurons of Aplysia in culture. J Physiol 534: 501-510, 2001.
10. Christie AE, Stein W, Quinlan JE, Beenhakker MP, Marder E, Nusbaum MP. Actions of a histaminergic/peptidergic projection neuron on rhythmic motor patterns in the stomatogastric nervous system of the crab Cancer borealis. J Comp Neurol 469: 153-169, 2004.
11. Collingridge GL, Kehl SJ, McLennan H. Excitatory amino acids in synaptic transmission in the Schaffer collateral-commissural pathway of the rat hippocampus. J Physiol 334: 33-46, 1983.
12. 3 and GABAA receptors. Mol Membr Biol 25: 293-301, 2008.
13. Cropper EC, Evans CG, Hurwitz I, Jing J, Proekt A, Romero A, Rosen SC. Feeding neuronal networks in the mollusk Aplysia. Neurosignals 13: 70-86, 2004.
14. Dacks AM, Weiss KR. Release of a single neurotransmitter from an identified interneuron coherently affects motor output on multiple time scales. J Neurophysiol 109: 2327-2334, 2013.
15. Descarries L, Bérubé-Carrière N, Riad M, Bo GD, Mendez JA, Trudeau LE. Glutamate in dopamine neurons: synaptic versus diffuse transmission. Brain Res Rev 58: 290-302, 2008.
16. Díaz-Ríos M, Miller MW. Rapid dopaminergic signaling by interneurons that contain markers for catecholamines and GABA in the feeding circuitry of Aplysia. J Neurophysiol 93: 2142-2156, 2005.
17. Díaz-Ríos M, Oyola E, Miller MW. Colocalization of gamma-aminobutyric acid-like immunoreactivity and catecholamines in the feeding network of Aplysia californica. J Comp Neurol 445: 29-46, 2002.
18. Dubin AE, Huvar R, D'Andrea MR, Pyati J, Zhu JY, Joy KC, Wilson SJ, Galindo JE, Glass CA, Luo L, Jackson MR, Lovenberg TW, Erlander MG. The pharmacological and functional characteristics of the serotonin 5-HT(3A) receptor are specifically modified by a 5-HT(3B) receptor subunit. J Biol Chem 274: 30799-30810, 1999.
19. Due MR, Jing J, Weiss KR. Dopaminergic contributions to modulatory functions of a dual-transmitter interneuron in Aplysia. Neurosci Lett 358: 53-57, 2004.
20. 3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J Neurosci 22: 7389-7397, 2002.
21. Fisher SA, Fischer TM, Carew TJ. Multiple overlapping processes underlying short-term synaptic enhancement. Trends Neurosci 20: 170-177, 1997.
22. Fox LE, Lloyd PE. Evidence that post-tetanic potentiation is mediated by neuropeptide release in Aplysia. J Neurophysiol 86: 2845-2855, 2001.
23. Gutovitz S, Birmingham JT, Luther JA, Simon DJ, Marder E. GABA enhances transmission at an excitatory glutamatergic synapse. J Neurosci 21: 5935-5943, 2001.
24. Henley JM, Barker EA, Glebov OO. Routes, destinations and delays: recent advances in AMPA receptor trafficking. Trends Neurosci 34: 258-268, 2011.
25. Hirasawa H, Betensky RA, Raviola E. Corelease of dopamine and GABA by a retinal dopaminergic neuron. J Neurosci 32: 13281-13291, 2012.
26. + current in the pleural sensory neurons of Aplysia by serotonin and cAMP: implications for spike broadening. Proc Natl Acad Sci USA 89: 11476-11480, 1992.
27. Hubbard L, Quastel DM, Llinas R. Electrophysiological Analysis of Synaptic Transmission. Baltimore, MD: William and Wilkins, 1969.
28. Jin I, Hawkins RD. Presynaptic and postsynaptic mechanisms of a novel form of homosynaptic potentiation at Aplysia sensory-motor neuron synapses. J Neurosci 23: 7288-7297, 2003.
29. Jing J, Weiss KR. Neural mechanisms of motor program switching in Aplysia. J Neurosci 21: 7349-7362, 2001.
30. Katz PS, Frost WN. Intrinsic neuromodulation: altering neuronal circuits from within. Trends Neurosci 19: 54-61, 1996.
31. Katz PS, Harris-Warrick RM. Neuromodulation of the crab pyloric central pattern generator by serotonergic/cholinergic proprioceptive afferents. J Neurosci 10: 1495-1512, 1990.
32. Katz PS, Harris-Warrick RM. Serotonergic/cholinergic muscle receptor cells in the crab stomatogastric nervous system. II. Rapid nicotinic and prolonged modulatory effects on neurons in the stomatogastric ganglion. J Neurophysiol 62: 571-581, 1989.
33. Kiehn O, Harris-Warrick RM. Serotonergic stretch receptors induce plateau properties in a crustacean motor neuron by a dual-conductance mechanism. J Neurophysiol 68: 485-495, 1992.
34. Klein M. Differential cyclic AMP dependence of facilitation at Aplysia sensorimotor synapses as a function of prior stimulation: augmentation versus restoration of transmitter release. J Neurosci 13: 3793-3801, 1993.
35. Koh HY, Vilim FS, Jing J, Weiss KR. Two neuropeptides colocalized in a command-like neuron use distinct mechanisms to enhance its fast synaptic connection. J Neurophysiol 90: 2074-2079, 2003.
36. Koh HY, Weiss KR. Peptidergic contribution to posttetanic potentiation at a central synapse of Aplysia. J Neurophysiol 94: 1281-1286, 2005.
37. Kwiatkowski MA, Gabranski ER, Huber KE, Chapline MC, Christie AE, Dickinson PS. Coordination of distinct but interacting rhythmic motor programs by a modulatory projection neuron using different co-transmitters in different ganglia. J Exp Biol 216: 1827-1836, 2013.
38. Liu S, Plachez C, Shao Z, Puche A, Shipley MT. Olfactory bulb short axon cell release of GABA and dopamine produces a temporally biphasic inhibition-excitation response in external tufted cells. J Neurosci 33: 2916-2926, 2013.
39. Lloyd PE, Willows AO. Multiple transmitter neurons in Tritonia. II. Control of gut motility. J Neurobiol 19: 55-67, 1988.
40. Maher BJ, Westbrook GL. Co-transmission of dopamine and GABA in periglomerular cells. J Neurophysiol 99: 1559-1564, 2008.
41. Malenka RC. Synaptic plasticity and AMPA receptor trafficking. Ann NY Acad Sci 1003: 1-11, 2003.
42. Manseau F, Sossin WS, Castellucci VF. Long-term changes in excitability induced by protein kinase C activation in Aplysia sensory neurons. J Neurophysiol 79: 1210-1218, 1998.
43. Morgan PT, Perrins R, Lloyd PE, Weiss KR. Intrinsic and extrinsic modulation of a single central pattern generating circuit. J Neurophysiol 84: 1186-1193, 2000.
44. 3 receptors. Eur J Pharmacol 127: 271-274, 1986.
45. Nusbaum MP, Blitz DM, Swensen AM, Wood D, Marder E. The roles of co-transmission in neuronal network modulation. Trends Neurosci 24: 146-154, 2001.
46. 3 receptors. Synapse 50: 303-313, 2003.
47. Proekt A, Brezina V, Weiss KR. Dynamical basis of intentions and expectations in a simple neuronal network. Proc Natl Acad Sci USA 101: 9447-9452, 2004.
48. Proekt A, Jing J, Weiss KR. Multiple contributions of an input-representing neuron to the dynamics of the Aplysia feeding network. J Neurophysiol 97: 3046-3056, 2007.
49. Roberts AC, Glanzman DL. Learning in Aplysia: looking at synaptic plasticity from both sides. Trends Neurosci 26: 662-670, 2003.
50. Rodicio MC, Villar-Cerviño V, Barreiro-Iglesias A, Anadón R. Colocalization of dopamine and GABA in spinal cord neurons in the sea lamprey. Brain Res Bull 76: 45-49, 2008.
51. Sámano C, Cifuentes F, Morales MA. Neurotransmitter segregation: functional and plastic implications. Prog Neurobiol 97: 277-287, 2012.
52. Shen W, Slaughter MM. Metabotropic GABA receptors facilitate L-type and inhibit N-type calcium channels in single salamander retinal neurons. J Physiol 516: 711-718, 1999.
53. Stein W, DeLong ND, Wood DE, Nusbaum MP. Divergent co-transmitter actions underlie motor pattern activation by a modulatory projection neuron. Eur J Neurosci 26: 1148-1165, 2007.
54. Stensrud MJ, Puchades M, Gundersen V. GABA is localized in dopaminergic synaptic vesicles in the rodent striatum. Brain Struct Funct. First published July 2013; doi:10.1007/s00429-013-0609-4.
55. 3 receptors in rat amygdala. Neuron 8: 199-203, 1992.
56. Svensson E, Grillner S, Parker D. Gating and braking of short-and long-term modulatory effects by interactions between co-localized neuromodulators. J Neurosci 21: 5984-5992, 2001.
57. Teyke T, Rosen SC, Weiss KR, Kupfermann I. Dopaminergic neuron B20 generates rhythmic neuronal activity in the feeding motor circuitry of Aplysia. Brain Res 630: 226-237, 1993.
58. Tremblay E, Ben-Ari Y, Roisin MP. Different GABAB-mediated effects on protein kinase C activity and immunoreactivity in neonatal and adult rat hippocampal slices. J Neurochem 65: 863-870, 1995.
59. Triller A, Choquet D. Surface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move! Trends Neurosci 28: 133-139, 2005.
60. Tritsch NX, Ding JB, Sabatini BL. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490: 262-266, 2012.
61. Villareal G, Li Q, Cai D, Fink AE, Lim T, Bougie JK, Sossin WS, Glanzman DL. Role of protein kinase C in the induction and maintenance of serotonin-dependent enhancement of the glutamate response in isolated siphon motor neurons of Aplysia californica. J Neurosci 29: 5100-5107, 2009.
62. Willows AO, Lloyd PE, Masinovsky BP. Multiple transmitter neurons in Tritonia. III. Modulation of central pattern generator controlling feeding. J Neurobiol 19: 69-86, 1988.
63. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405, 2002.