Short-term synaptic plasticity compensates for variability in number of motor neurons at a neuromuscular junction

Journal of Neuroscience

Volumn 32, Issue 45, 2012, Pages 16007-16017

  Daur, Nelly ^a   Bryan, Ayanna S ^a   Garcia, Veronica J ^a   Bucher, Dirk ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; DEPOLARIZATION; ELECTROPHYSIOLOGY; EVOKED MUSCLE RESPONSE; EXCITATORY JUNCTION POTENTIAL; FEMALE; HOMARUS AMERICANUS; HOMEOSTASIS; INTRACELLULAR RECORDING; MALE; MICROPHOTOGRAPHY; MOTONEURON; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PYLORIC NERVE CELL; SPIKE WAVE;

ACTION POTENTIALS; ANIMALS; AXONS; ELECTRIC STIMULATION; MOTOR NEURONS; MUSCLE CONTRACTION; MUSCLES; NEPHROPIDAE; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; PYLORUS; SYNAPTIC TRANSMISSION;

EID: 84868594482     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2584-12.2012     Document Type: Article

References (72)

1. Abbott LF, Regehr WG (2004) Synaptic computation. Nature 431:796-803.
2. Atwood HL (1976) Organization and synaptic physiology of crustacean neuromuscular systems. Prog Neurobiol 7:291-391.
3. Atwood HL, Govind CK, Jahromi SS (1977) Excitatory synapsesofblue crab gastric mill muscles. Cell Tissue Res 177:145-158.
4. Atwood HL, Govind CK, Kwan I (1978) Nonhomogeneous excitatory synapses of a crab stomach muscle. J Neurobiol 9:17-28.
5. Blitz DM, Foster KA, Regehr WG (2004) Short-term synaptic plasticity: a comparison of two synapses. Nat Rev Neurosci 5:630-640.
6. Branco T, Staras K, Darcy KJ, Goda Y (2008) Local dendritic activity sets release probability at hippocampal synapses. Neuron 59:475-485.
7. Bucher D (2009) Neuronal homeostasis: does form follow function or vice versa? Curr Biol 19:R64-R67.
8. Bucher D, Prinz AA, Marder E (2005) Animal-to-animal variability in motor pattern production in adults and during growth. J Neurosci 25:1611-1619.
9. Bucher D, Taylor AL, Marder E (2006) Central pattern generating neurons simultaneously express fast and slow rhythmic activities in the stomato-gastric ganglion. J Neurophysiol 95:3617-3632.
10. Bucher D, Johnson CD, Marder E (2007) Neuronal morphology and neu-ropil structure in the stomatogastric ganglion of the lobster, Homarus americanus. J Comp Neurol 501:185-205.
11. Burrows M (1996) The neurobiologyofaninsect brain. Oxford: Oxford UP.
12. Chen C, Blitz DM, Regehr WG (2002) Contributions of receptor desensiti-zation and saturationtoplasticityatthe retinogeniculate synapse. Neuron 33:779-788.
13. Davis GW (2006) Homeostatic control of neural activity: from phenomenology to molecular design. Annu Rev Neurosci 29:307-323.
14. Davis GW, Bezprozvanny I (2001) Maintaining the stability of neural function: a homeostatic hypothesis. Annu Rev Physiol 63:847-869.
15. Davis GW, Murphey RK (1994) Long-term regulation of short-term transmitter release properties: retrograde signaling and synaptic development. Trends Neurosci 17:9-13.
16. Davis GW, DiAntonio A, Petersen SA, Goodman CS (1998) Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron 20:305-315.
17. Dittman JS, Kreitzer AC, Regehr WG (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neuro-sci 20:1374-1385.
18. Foster KA, Kreitzer AC, Regehr WG (2002) Interaction of postsynaptic receptor saturation with presynaptic mechanisms produces a reliable synapse. Neuron 36:1115-1126.
19. Foster KA, Crowley JJ, Regehr WG (2005) The influence of multivesicular release and postsynaptic receptor saturation on transmission at granule cell to Purkinje cell synapses. J Neurosci 25:11655-11665.
20. Frank CA, Pielage J, Davis GW (2009) A presynaptic homeostatic signaling system composed of the Eph receptor, ephexin, Cdc42, and CaV2.1 calcium channels. Neuron 61:556-569.
21. Golowasch J, Casey M, Abbott LF, Marder E (1999a) Network stability from activity-dependent regulation ofneuronal conductances. Neural Comput 11:1079-1096.
22. Golowasch J, Abbott LF, Marder E (1999b) Activity-dependent regulation of potassium currents in an identified neuron of the stomatogastric ganglion of the crab Cancer borealis. J Neurosci 19:RC33(1-5).
23. Goodman C (1974) Anatomy of locust ocellar interneurons: constancy and variability. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 95: 185-201.
24. Govind CK, Atwood HL (1982) Organization of neuromuscular systems. In: The biology of crustacea: Neurobiology: structure and function. (At-wood HL, Sandeman DC, eds), pp 63-98. New York: Academic.
25. Govind CK, Atwood HL, Maynard DM (1975) Innervation and neuromus-cular physiology of intrinsic foregut muscles in the blue crab and spiny lobster. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 96:185-204.
26. Gundlfinger A, Leibold C, Gebert K, Moisel M, Schmitz D, Kempter R (2007) Differential modulation of short-term synaptic dynamics by long-term potentiation at mouse hippocampal mossy fibre synapses. J Physiol 585: 853-865.
27. Hartline DK, Gassie DV, Sirchia CD (1987) PY cell types in the stomatogas-tric ganglion of Panulirus. In: The crustacean stomatogastric system (Selverston AI, Moulins M, eds), pp 75-77. Berlin: Springer.
28. Hoyle G (1983) Muscles and their neural control. New York: Wiley.
29. Jahromi SS, Govind CK (1976) Ultrastructural diversity in motor units of crustacean stomach muscles. Cell Tissue Res 166:159-166.
30. Jones MV, Westbrook GL (1996) The impact of receptor desensitization on fast synaptic transmission. Trends Neurosci 19:96-101.
31. Kuffler DP, Muller KJ (1974) The properties and connections of supernumerary sensory and motor nerve cells in the central nervous system of an abnormal leech. J Neurobiol 5:331-348.
32. Leibold C, Bendels MH (2009) Learning to discriminate through long-term changes of dynamical synaptic transmission. Neural Comput 21: 3408-3428.
33. Lingle C (1980) The sensitivity of decapod foregut muscles to acetylcholine and glutamate. J Comp Physiol 138:187-199.
34. Liu KS, Gray M, Otto SJ, Fetcho JR, Beattie CE (2003) Mutations in deadly seven/notch1a reveal developmental plasticity in the escape response circuit. J Neurosci 23:8159-8166.
35. Ma PM, Lopez M (2003) Consistency in the number of dopaminergic para-ventricular organ-accompanying neurons in the posterior tuberculum of the zebrafish brain. Brain Res 967:267-272.
36. Maffei A, Turrigiano GG (2008) Multiple modes of network homeostasis in visual cortical layer 2/3. J Neurosci 28:4377-4384.
37. Maffei A, Nelson SB, Turrigiano GG (2004) Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 7:1353-1359.
38. Marder E, Bucher D (2007) Understanding circuit dynamics using the sto-matogastric nervous system of lobsters and crabs. Annu Rev Physiol 69:291-316.
39. Marder E, Goaillard JM (2006) Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7:563-574.
40. Marder E, Prinz AA (2002) Modeling stability in neuron and network function: the role of activity in homeostasis. Bioessays 24:1145-1154.
41. Maynard DM, Dando MR (1974) The structure of the stomatogastric neu-romuscular system in Callinectes sapidus, Homarus americanus and Panu-lirus argus (Decapoda Crustacea). Philos Trans R Soc Lond B 268:161-220.
42. Moulder KL, Jiang X, Taylor AA, Olney JW, Mennerick S (2006) Physiological activity depresses synaptic function through an effectonvesicle priming. J Neurosci 26:6618-6626.
43. Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673-682.
44. Nadim F, Manor Y (2000) The role of short-term synaptic dynamics in motor control. Curr Opin Neurobiol 10:683-690.
45. Nadim F, Manor Y, Kopell N, Marder E (1999) Synaptic depression creates a switch that controls the frequency of an oscillatory circuit. Proc Natl Acad Sci U S A 96:8206-8211.
46. Newcomb JM, Fickbohm DJ, Katz PS (2006) Comparative mapping of serotonin-immunoreactive neurons in the central nervous systems of nudibranch molluscs. J Comp Neurol 499:485-505.
47. Paradis S, Sweeney ST, Davis GW (2001) Homeostatic control of presynap-tic release is triggered by postsynaptic membrane depolarization. Neuron 30:737-749.
48. Pérez-Otaño I, Ehlers MD (2005) Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci 28:229-238.
49. Pozo K, Goda Y (2010) Unraveling mechanisms of homeostatic synaptic plasticity. Neuron 66:337-351.
50. Prinz AA, Billimoria CP, Marder E (2003) Alternative to hand-tuning conductance-based models: construction and analysis of databases of model neurons. J Neurophysiol 90:3998-4015.
51. Prinz AA, Bucher D, Marder E (2004) Similar network activity from disparate circuit parameters. Nat Neurosci 7:1345-1352.
52. Pulver SR, Bucher D, Simon DJ, Marder E (2005) Constant amplitude of postsynaptic responses for single presynaptic action potentials but not bursting input during growth of an identified neuromuscular junction in the lobster, Homarus americanus. J Neurobiol 62:47-61.
53. Regehr WG, Stevens CF (2001) Physiology of synaptic transmission and short-term plasticity. In: Synapses (Cowan WM, Sudhof TC, Stevens CF, eds), pp 135-176. Baltimore: The Johns Hopkins UP.
54. Rogers SM, Krapp HG, Burrows M, Matheson T (2007) Compensatory plasticity at an identified synapse tunes a visuomotor pathway. J Neurosci 27:4621-4633.
55. Sandeman DC (1982) Organization of the central nervous system. In: The biology of crustacea: Neurobiology: structure and function. (Atwood HL, Sandeman DC, eds), pp 1-54. New York: Academic.
56. Schulz DJ, Goaillard JM, Marder E (2006) Variable channel expression in identified single and electrically coupled neuronsindifferent animals. Nat Neurosci 9:356-362.
57. Sen K, Jorge-Rivera JC, Marder E, Abbott LF (1996) Decoding synapses. J Neurosci 16:6307-6318.
58. Soto-Treviño C, Thoroughman KA, Marder E, Abbott LF (2001) Activity-dependent modification of inhibitory synapses in models of rhythmic neural networks. Nat Neurosci 4:297-303.
59. Stein W, Smarandache CR, Nickmann M, Hedrich UB (2006) Functional consequences of activity-dependent synaptic enhancement at a crustacean neuromuscular junction. J Exp Biol 209:1285-1300.
60. Sun YG, Beierlein M (2011) Receptor saturation controls short-term synap-tic plasticity at corticothalamic synapses. J Neurophysiol 105:2319-2329.
61. Thuma JB, Harness PI, Koehnle TJ, Morris LG, Hooper SL (2007) Muscle anatomy is a primary determinant of muscle relaxation dynamics in the lobster (Panulirus interruptus) stomatogastric system. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 193:1101-1113.
62. Turrigiano G (2007) Homeostatic signaling: the positive side of negative feedback. Curr Opin Neurobiol 17:318-324.
63. Turrigiano G (2011) Too many cooks? Intrinsic and synaptic homeostatic mechanisms in cortical circuit refinement. Annu Rev Neurosci 34: 89-103.
64. Turrigiano G, Abbott LF, Marder E (1994) Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264:974-977.
65. TurrigianoGG (2008) The self-tuning neuron: synaptic scalingofexcitatory synapses. Cell 135:422-435.
66. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107.
67. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:892-896.
68. Whitney IE, Raven MA, Ciobanu DC, Poché RA, Ding Q, Elshatory Y, Gan L, Williams RW, Reese BE (2011) Genetic modulation of horizontal cell number in the mouse retina. Proc Natl Acad Sci U S A 108:9697-9702.
69. Williams RW, Herrup K (1988) The control of neuron number. Annu Rev Neurosci 11:423-453.
70. Williams RW, Strom RC, Rice DS, Goldowitz D (1996) Genetic and environmental control of variation in retinal ganglion cell number in mice. J Neurosci 16:7193-7205.
71. Williams RW, Strom RC, Goldowitz D (1998) Natural variation in neuron number in mice is linked to a major quantitative trait locus on Chr 11. J Neurosci 18:138-146.
72. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.