Robust circuit rhythms in small circuits arise from variable circuit components and mechanisms

Current Opinion in Neurobiology

Volumn 31, Issue , 2015, Pages 156-163

  Marder, Eve ^a   Goeritz, Marie L ^a   Otopalik, Adriane G ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLATOSTATIN;

ACTION POTENTIAL; ANATOMICAL VARIATION; BRAIN FUNCTION; CELL DENSITY; CONNECTOME; CRAB; ELECTROENCEPHALOGRAPHY; GENETIC VARIABILITY; LOBSTER; NEUROMODULATION; NONHUMAN; PATTERN GENERATOR; REVIEW; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; SYNAPTIC TRANSMISSION; TEMPERATURE; TEMPERATURE DEPENDENCE; ANIMAL; BIOLOGICAL MODEL; BRAIN; CENTRAL PATTERN GENERATOR; COMPUTER SIMULATION; CYTOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; BRAIN; CENTRAL PATTERN GENERATORS; COMPUTER SIMULATION; MODELS, NEUROLOGICAL;

EID: 84910136850     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2014.10.012     Document Type: Review

References (79)

1. Marder E., Bucher D. Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu Rev Physiol 2007, 69:291-316.
2. Marder E., Calabrese R.L. Principles of rhythmic motor pattern generation. Physiol Rev 1996, 76:687-717.
3. Getting P.A. Emerging principles governing the operation of neural networks. Annu Rev Neurosci 1989, 12:185-204.
4. Selverston A.I., Moulins M. Oscillatory neural networks. Annu Rev Physiol 1985, 47:29-48.
5. Nadim F., Zhao S., Zhou L., Bose A. Inhibitory feedback promotes stability in an oscillatory network. J Neural Eng 2011, 8:065001.
6. Mulloney B., Perkel D.H., Budelli R.W. Motor-pattern production: interaction of chemical and electrical synapses. Brain Res 1981, 229:25-33.
7. Grashow R., Brookings T., Marder E. Reliable neuromodulation from circuits with variable underlying structure. Proc Natl Acad Sci U S A 2009, 106:11742-11746.
8. Lamb D.G., Calabrese R.L. Small is beautiful: models of small neuronal networks. Curr Opin Neurobiol 2012, 22:670-675.
9. Blitz D.M., Nusbaum M.P. Modulation of circuit feedback specifies motor circuit output. J Neurosci 2012, 32:9182-9193.
10. Marder E. Neuromodulation of neuronal circuits: back to the future. Neuron 2012, 76:1-11.
11. Nadim F., Bucher D. Neuromodulation of neurons and synapses. Curr Opin Neurobiol 2014, 29C:48-56.
12. Brezina V. Beyond the wiring diagram: signalling through complex neuromodulator networks. Philos Trans R Soc Lond B Biol Sci 2010, 365:2363-2374.
13. Bargmann C.I. Beyond the connectome: how neuromodulators shape neural circuits. Bioessays 2012, 34:458-465.
14. Dickinson P.S., Mecsas C., Marder E. Neuropeptide fusion of two motor-pattern generator circuits. Nature 1990, 344:155-158.
15. Hooper S.L., Moulins M. Switching of a neuron from one network to another by sensory-induced changes in membrane properties. Science 1989, 244:1587-1589.
16. Weimann J.M., Marder E. Switching neurons are integral members of multiple oscillatory networks. Curr Biol 1994, 4:896-902.
17. Bucher D., Taylor A.L., Marder E. Central pattern generating neurons simultaneously express fast and slow rhythmic activities in the stomatogastric ganglion. J Neurophysiol 2006, 95:3617-3632.
18. Meyrand P., Simmers J., Moulins M. Construction of a pattern-generating circuit with neurons of different networks. Nature 1991, 351:60-63.
19. Goaillard J.M., Taylor A.L., Schulz D.J., Marder E. Functional consequences of animal-to-animal variation in circuit parameters. Nat Neurosci 2009, 12:1424-1430.
20. Schulz D.J., Goaillard J.M., Marder E. Variable channel expression in identified single and electrically coupled neurons in different animals. Nat Neurosci 2006, 9:356-362.
21. Schulz D.J., Goaillard J.M., Marder E. Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression. Proc Natl Acad Sci U S A 2007, 104:13187-13191.
22. Temporal S., Desai M., Khorkova O., Varghese G., Dai A., Schulz D.J., Golowasch J. Neuromodulation independently determines correlated channel expression and conductance levels in motor neurons of the stomatogastric ganglion. J Neurophysiol 2012, 107:718-727.
23. Temporal S., Lett K.M., Schulz D.J. Activity-dependent feedback regulates correlated ion channel mRNA levels in single identified motor neurons. Curr Biol 2014, 24:1899-1904.
24. Norris B.J., Wenning A., Wright T.M., Calabrese R.L. Constancy and variability in the output of a central pattern generator. J Neurosci 2011, 31:4663-4674.
25. Roffman R.C., Norris B.J., Calabrese R.L. Animal-to-animal variability of connection strength in the leech heartbeat central pattern generator. J Neurophysiol 2012, 107:1681-1693.
26. Golowasch J. Ionic current variability and functional stability in the nervous system. Bioscience 2014, 64:570-580.
27. Goodman C.S. Isogenic grasshoppers: genetic variability in the morphology of identified neurons. J Comp Neurol 1978, 182:681-705.
28. Goeritz M.L., Bowers M.R., Slepian B., Marder E. Neuropilar projections of the anterior gastric receptor neuron in the stomatogastric ganglion of the Jonah crab, Cancer borealis. PLoS One 2013, 8:e79306.
29. Thuma J.B., White W.E., Hobbs K.H., Hooper S.L. Pyloric neuron morphology in the stomatogastric ganglion of the lobster, Panulirus interruptus. Brain Behav Evol 2009, 73:26-42.
30. Daur N., Bryan A.S., Garcia V.J., Bucher D. Short-term synaptic plasticity compensates for variability in number of motor neurons at a neuromuscular junction. J Neurosci 2012, 32:16007-16017.
31. Goldman M.S., Golowasch J., Marder E., Abbott L.F. Global structure, robustness, and modulation of neuronal models. J Neurosci 2001, 21:5229-5238.
32. Tobin A.E., Cruz-Bermudez N.D., Marder E., Schulz D.J. Correlations in ion channel mRNA in rhythmically active neurons. PLoS One 2009, 4:e6742.
33. Ransdell J.L., Nair S.S., Schulz D.J. Rapid homeostatic plasticity of intrinsic excitability in a central pattern generator network stabilizes functional neural network output. J Neurosci 2012, 32:9649-9658.
34. Ransdell J.L., Nair S.S., Schulz D.J. Neurons within the same network independently achieve conserved output by differentially balancing variable conductance magnitudes. J Neurosci 2013, 33:9950-9956.
35. Zhao S.B., Golowasch J. Ionic current correlations underlie the global tuning of large numbers of neuronal activity attributes. J Neurosci 2012, 32:13380-13388.
36. Calabrese R.L., Norris B.J., Wenning A., Wright T.M. Coping with variability in small neuronal networks. Integr Comp Biol 2011, 51:845-855.
37. Prinz A.A., Bucher D., Marder E. Similar network activity from disparate circuit parameters. Nat Neurosci 2004, 7:1345-1352.
38. Taylor A.L., Goaillard J.M., Marder E. How multiple conductances determine electrophysiological properties in a multicompartment model. J Neurosci 2009, 29:5573-5586.
39. Lamb D.G., Calabrese R.L. Correlated conductance parameters in leech heart motor neurons contribute to motor pattern formation. PLoS One 2013, 8:e79267.
40. Marder E., Taylor A.L. Multiple models to capture the variability in biological neurons and networks. Nat Neurosci 2011, 14:133-138.
41. Hudson A.E., Prinz A.A. Conductance ratios and cellular identity. PLoS Comput Biol 2010, 6:e1000838.
42. Caplan J.S., Williams A.H., Marder E. Many parameter sets in a multicompartment model oscillator are robust to temperature perturbations. J Neurosci 2014, 34:4963-4975.
43. Soofi W., Archila S., Prinz A.A. Co-variation of ionic conductances supports phase maintenance in stomatogastric neurons. J Comput Neurosci 2012, 33:77-95.
44. Grashow R., Brookings T., Marder E. Compensation for variable intrinsic neuronal excitability by circuit-synaptic interactions. J Neurosci 2010, 30:9145-9156.
45. O'Leary T., Williams A.H., Caplan J.S., Marder E. Correlations in ion channel expression emerge from homeostatic tuning rules. Proc Natl Acad Sci U S A 2013, 110:E2645-E2654.
46. O'Leary T., Williams A.H., Franci A., Marder E. Cell types, network homeostasis, and pathological compensation from a biologically plausible ion channel expression model. Neuron 2014, 82:809-821.
47. Krenz W.D., Parker A.R., Rodgers E.W., Baro D.J. Dopaminergic tone persistently regulates voltage-gated ion current densities through the D1R-PKA axis, RNA polymerase II transcription, RNAi, mTORC1, and translation. Front Cell Neurosci 2014, 8:39.
48. Krenz W.D., Hooper R.M., Parker A.R., Prinz A.A., Baro D.J. Activation of high and low affinity dopamine receptors generates a closed loop that maintains a conductance ratio and its activity correlate. Front Neural Circuits 2013, 7:169.
49. Sakurai A., Tamvacakis A.N., Katz P.S. Hidden synaptic differences in a neural circuit underlie differential behavioral susceptibility to a neural injury. elife 2014, 3:e02598.
50. Robertson R.M., Money T.G. Temperature and neuronal circuit function: compensation, tuning and tolerance. Curr Opin Neurobiol 2012, 22:724-734.
51. Rinberg A., Taylor A.L., Marder E. The effects of temperature on the stability of a neuronal oscillator. PLoS Comput Biol 2013, 9:e1002857.
52. Soofi W., Goeritz M.L., Kispersky T.J., Prinz A.A., Marder E., Stein W. Phase maintenance in a rhythmic motor pattern during temperature changes in vivo. J Neurophysiol 2014, 111:2603-2613.
53. Tang L.S., Goeritz M.L., Caplan J.S., Taylor A.L., Fisek M., Marder E. Precise temperature compensation of phase in a rhythmic motor pattern. PLoS Biol 2010, 8:e1000469.
54. Tang L.S., Taylor A.L., Rinberg A., Marder E. Robustness of a rhythmic circuit to short- and long-term temperature changes. J Neurosci 2012, 32:10075-10085.
55. Dacks A.M., Weiss K.R. Latent modulation: a basis for non-disruptive promotion of two incompatible behaviors by a single network state. J Neurosci 2013, 33:3786-3798.
56. Nusbaum M.P., Marder E. A modulatory proctolin-containing neuron (MPN) II. State-dependent modulation of rhythmic motor activity. J Neurosci 1989, 9:1600-1607.
57. Marder E., O'Leary T., Shruti S. Neuromodulation of circuits with variable parameters: single neurons and small circuits reveal principles of state-dependent and robust neuromodulation. Annu Rev Neurosci 2014, 37:329-346.
58. Spitzer N., Cymbalyuk G., Zhang H., Edwards D.H., Baro D.J. Serotonin transduction cascades mediate variable changes in pyloric network cycle frequency in response to the same modulatory challenge. J Neurophysiol 2008, 99:2844-2863.
59. Wiwatpanit T., Powers B., Dickinson P.S. Inter-animal variability in the effects of C-type allatostatin on the cardiac neuromuscular system in the lobster Homarus americanus. J Exp Biol 2012, 215:2308-2318.
60. Williams A.H., Calkins A., O'Leary T., Symonds R., Marder E., Dickinson P.S. The neuromuscular transform of the lobster cardiac system explains the opposing effects of a neuromodulator on muscle output. J Neurosci 2013, 33:16565-16575.
61. Rodgers E.W., Fu J.J., Krenz W.D., Baro D.J. Tonic nanomolar dopamine enables an activity-dependent phase recovery mechanism that persistently alters the maximal conductance of the hyperpolarization-activated current in a rhythmically active neuron. J Neurosci 2011, 31:16387-16397.
62. Rodgers E.W., Krenz W.D., Baro D.J. Tonic dopamine induces persistent changes in the transient potassium current through translational regulation. J Neurosci 2011, 31:13046-13056.
63. Hamilton J.L., Edwards C.R., Holt S.R., Worden M.K. Temperature dependent modulation of lobster neuromuscular properties by serotonin. J Exp Biol 2007, 210:1025-1035.
64. Thuma J.B., Hobbs K.H., Burstein H.J., Seiter N.S., Hooper S.L. Temperature sensitivity of the pyloric neuromuscular system and its modulation by dopamine. PLoS One 2013, 8:e67930.
65. Hill E.S., Vasireddi S.K., Bruno A.M., Wang J., Frost W.N. Variable neuronal participation in stereotypic motor programs. PLoS One 2012, 7.
66. Wu J.Y., Cohen L.B., Falk C.X. Neuronal activity during different behaviors in Aplysia: a distributed organization?. Science 1994, 263:820-823.
67. Zochowski M., Cohen L.B., Fuhrmann G., Kleinfeld D. Distributed and partially separate pools of neurons are correlated with two different components of the gill-withdrawal reflex in Aplysia. J Neurosci 2000, 20:8485-8492.
68. Gutierrez G.J., O'Leary T., Marder E. Multiple mechanisms switch an electrically coupled, synaptically inhibited neuron between competing rhythmic oscillators. Neuron 2013, 77:845-858.
69. Gutierrez G.J., Marder E. Rectifying electrical synapses can affect the influence of synaptic modulation on output pattern robustness. J Neurosci 2013, 33:13238-13248.
70. Rodriguez J.C., Blitz D.M., Nusbaum M.P. Convergent rhythm generation from divergent cellular mechanisms. J Neurosci 2013, 33:18047-18064.
71. Wenning A., Norris B.J., Doloc-Mihu A., Calabrese R.L. Variation in motor output and motor performance in a centrally generated motor pattern. J Neurophysiol 2014, 112:95-109.
72. Diehl F., White R.S., Stein W., Nusbaum M.P. Motor circuit-specific burst patterns drive different muscle and behavior patterns. J Neurosci 2013, 33:12013-12029.
73. Kristan W.B., Calabrese R.L., Friesen W.O. Neuronal control of leech behavior. Prog Neurobiol 2005, 76:279-327.
74. Lamb D.G., Calabrese R.L. Neural circuits controlling behavior and autonomic functions in medicinal leeches. Neural Syst Circuits 2011, 1:13.
75. Grillner S., Wallen P. Cellular bases of a vertebrate locomotor system-steering, intersegmental and segmental co-ordination and sensory control. Brain Res Brain Res Rev 2002, 40:92-106.
76. Gjorgjieva J., Berni J., Evers J.F., Eglen S.J. Neural circuits for peristaltic wave propagation in crawling Drosophila larvae: analysis and modeling. Front Comput Neurosci 2013, 7:24.
77. Gjorgjieva J., Biron D., Haspel G. Neurobiology of Caenorhabditis elegans Locomotion: where do we stand?. Bioscience 2014, 64:476-486.
78. Smarandache-Wellmann C., Weller C., Mulloney B. Mechanisms of coordination in distributed neural circuits: decoding and integration of coordinating information. J Neurosci 2014, 34:793-803.
79. Zhang C., Guy R.D., Mulloney B., Zhang Q., Lewis T.J. Neural mechanism of optimal limb coordination in crustacean swimming. Proc Natl Acad Sci U S A 2014.