Multiple mechanisms switch an electrically coupled, synaptically inhibited neuron between competing rhythmic oscillators

Neuron

Volumn 77, Issue 5, 2013, Pages 845-858

  Gutierrez, Gabrielle J ^a   O'Leary, Timothy ^a   Marder, Eve ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTIC METHOD; ARTICLE; BRAIN NERVE CELL; CELL ACTIVITY; CELL FUNCTION; COORDINATION; ELECTRICAL SYNAPSE; GENETIC MANIPULATION; INHIBITORY SYNAPSE; MOLECULAR DYNAMICS; MULTIPLE MECHANISM SWITCH; NERVE CELL NETWORK; OPTOGENETICS; OSCILLATION; OSCILLATOR; PARAMETERSCAPE; PRIORITY JOURNAL; RHYTHMIC OSCILLATION; STRENGTH; SYNAPSE; SYNAPTIC INHIBITION; ALGORITHM; BIOLOGICAL MODEL; COMPUTER SIMULATION; ELECTROPHYSIOLOGY; INNERVATION; KINETICS; MEMBRANE POTENTIAL; NERVE CELL; NERVE TRACT; PERIODICITY; PHYSIOLOGY; SENSORY GATING; TONGUE;

ALGORITHMS; COMPUTER SIMULATION; ELECTROPHYSIOLOGICAL PHENOMENA; KINETICS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NERVE NET; NEURAL PATHWAYS; NEURONS; PERIODICITY; SENSORY GATING; SYNAPSES; TONGUE;

MLCS; MLOWN;

EID: 84876453272     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.01.016     Document Type: Article

References (75)

1. Ainsworth, M., Lee, S., Cunningham, M.O., Roopun, A.K., Traub, R.D., Kopell, N.J., and Whittington, M.A. (2011). Dual g rhythm generators control interlaminar synchrony in auditory cortex. J. Neurosci. 31, 17040-17051.
2. Bargmann, C.I. (2012). Beyond the connectome: how neuromodulators shape neural circuits. Bioessays 34, 458-465.
3. Bem, T., and Rinzel, J. (2004). Short duty cycle destabilizes a half-center oscillator, but gap junctions can restabilize the anti-phase pattern. J. Neurophysiol. 91, 693-703.
4. Bem, T., Le Feuvre, Y., Rinzel, J., and Meyrand, P. (2005). Electrical coupling induces bistability of rhythms in networks of inhibitory spiking neurons. Eur. J. Neurosci. 22, 2661-2668.
5. Bennett, M.V. (2000a). Electrical synapses, a personal perspective (or history). Brain Res. Brain Res. Rev. 32, 16-28.
6. Bennett, M.V. (2000b). Seeing is relieving: electrical synapses between visualized neurons. Nat. Neurosci. 3, 7-9.
7. Bennett, M.V., and Zukin, R.S. (2004). Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 41, 495-511.
8. Berke, J.D. (2009). Fast oscillations in cortical-striatal networks switch frequency following rewarding events and stimulant drugs. Eur. J. Neurosci. 30, 848-859.
9. Briggman, K.L., and Kristan, W.B. (2008). Multifunctional pattern-generating circuits. Annu. Rev. Neurosci. 31, 271-294.
10. Bucher, D., Taylor, A.L., and Marder, E. (2006). Central pattern generating neurons simultaneously express fast and slow rhythmic activities in the stomatogastric ganglion. J. Neurophysiol. 95, 3617-3632.
11. Büschges, A., Ludwar, B.Ch., Bucher, D., Schmidt, J., and DiCaprio, R.A. (2004). Synaptic drive contributing to rhythmic activation of motoneurons in the deafferented stick insect walking system. Eur. J. Neurosci. 19, 1856-1862.
12. Clapp, W.C., Rubens, M.T., Sabharwal, J., and Gazzaley, A. (2011). Deficit in switching between functional brain networks underlies the impact of multitasking on working memory in older adults. Proc. Natl. Acad. Sci. USA 108, 7212-7217.
13. Connors, B.W., and Long, M.A. (2004). Electrical synapses in the mammalian brain. Annu. Rev. Neurosci. 27, 393-418.
14. Connors, B.W., Benardo, L.S., and Prince, D.A. (1983). Coupling between neurons of the developing rat neocortex. J. Neurosci. 3, 773-782.
15. Connors, B.W., Zolnik, T.A., and Lee, S.C. (2010). Enhanced functions of electrical junctions. Neuron 67, 354-356.
16. Dickinson, P.S., Mecsas, C., and Marder, E. (1990). Neuropeptide fusion of two motor-pattern generator circuits. Nature 344, 155-158.
17. Diester, I., Kaufman, M.T., Mogri, M., Pashaie, R., Goo, W., Yizhar, O., Ramakrishnan, C., Deisseroth, K., and Shenoy, K.V. (2011). An optogenetic toolbox designed for primates. Nat. Neurosci. 14, 387-397.
18. Fenno, L., Yizhar, O., and Deisseroth, K. (2011). The development and application of optogenetics. Annu. Rev. Neurosci. 34, 389-412.
19. Griffith, L.C. (2012). Identifying behavioral circuits in Drosophila melanogaster: moving targets in a flying insect. Curr. Opin. Neurobiol. 22, 609-614.
20. Grillner, S. (2006). Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52, 751-766.
21. Haas, J.S., and Landisman, C.E. (2011). State-dependent modulation of gap junction signaling by the persistent sodium current. Front. Cell. Neurosci. 5, 31.
22. Haas, J.S., and Landisman, C.E. (2012). Bursts modify electrical synaptic strength. Brain Res. 1487, 140-149.
23. Haas, J.S., Zavala, B., and Landisman, C.E. (2011). Activity-dependent longterm depression of electrical synapses. Science 334, 389-393.
24. Heerebout, B.T., and Phaf, R.H. (2010). Good vibrations switch attention: an affective function for network oscillations in evolutionary simulations. Cogn. Affect. Behav. Neurosci. 10, 217-229.
25. Hooper, S.L., and Moulins, M. (1989). Switching of a neuron from one network to another by sensory-induced changes in membrane properties. Science 244, 1587-1589.
26. Hooper, S.L., and Moulins, M. (1990). Cellular and synaptic mechanisms responsible for a long-lasting restructuring of the lobster pyloric network. J. Neurophysiol. 64, 1574-1589.
27. Hooper, S.L., Moulins, M., and Nonnotte, L. (1990). Sensory input induces long-lasting changes in the output of the lobster pyloric network. J. Neurophysiol. 64, 1555-1573.
28. Izhikevich, E.M. (2007). Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting (Cambridge, MA: MIT Press).
29. Katz, P.S., and Harris-Warrick, R.M. (1991). Recruitment of crab gastric mill neurons into the pyloric motor pattern by mechanosensory afferent stimulation. J. Neurophysiol. 65, 1442-1451.
30. Kepler, T.B., Marder, E., and Abbott, L.F. (1990). The effect of electrical coupling on the frequency of model neuronal oscillators. Science 248, 83-85.
31. Kopell, N., and Ermentrout, B. (2004). Chemical and electrical synapses perform complementary roles in the synchronization of interneuronal networks. Proc. Natl. Acad. Sci. USA 101, 15482-15487.
32. Kopell, N., Abbott, L.F., and Soto-Trevino, C. (1998). On the behavior of a neural oscillator electrically coupled to a bistable element. Physica D 121, 367-395.
33. Lamb, D.G., and Calabrese, R.L. (2011). Neural circuits controlling behavior and autonomic functions in medicinal leeches. Neural Syst. Circuits 1, 13.
34. Lamb, D.G., and Calabrese, R.L. (2012). Small is beautiful: models of small neuronal networks. Curr. Opin. Neurobiol. 22, 670-675.
35. Landisman, C.E., and Connors, B.W. (2005). Long-term modulation of electrical synapses in the mammalian thalamus. Science 310, 1809-1813.
36. Macosko, E.Z., Pokala, N., Feinberg, E.H., Chalasani, S.H., Butcher, R.A., Clardy, J., and Bargmann, C.I. (2009). A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458, 1171-1175.
37. Manor, Y., Rinzel, J., Segev, I., and Yarom, Y. (1997). Low-amplitude oscillations in the inferior olive: a model based on electrical coupling of neurons with heterogeneous channel densities. J. Neurophysiol. 77, 2736-2752.
38. Marder, E. (1984). Roles for electrical coupling in neural circuits as revealed by selective neuronal deletions. J. Exp. Biol. 112, 147-167.
39. Marder, E. (1998). Electrical synapses: beyond speed and synchrony to computation. Curr. Biol. 8, R795-R797.
40. Marder, E. (2011). Variability, compensation, and modulation in neurons and circuits. Proc. Natl. Acad. Sci. USA 108(Suppl 3), 15542-15548.
41. Marder, E., and Bucher, D. (2001). Central pattern generators and the control of rhythmic movements. Curr. Biol. 11, R986-R996.
42. Marder, E., and Bucher, D. (2007). Understanding circuit dynamics using the stomatogastric nervous system of lobsters and crabs. Annu. Rev. Physiol. 69, 291-316.
43. Marder, E., and Calabrese, R.L. (1996). Principles of rhythmic motor pattern generation. Physiol. Rev. 76, 687-717.
44. Mayeri, E. (1973). Functional organization of the cardiac ganglion of the lobster, Homarus americanus. J. Gen. Physiol. 62, 448-472.
45. Meyrand, P., Simmers, J., and Moulins, M. (1991). Construction of a patterngenerating circuit with neurons of different networks. Nature 351, 60-63.
46. Meyrand, P., Simmers, J., and Moulins, M. (1994). Dynamic construction of a neural network from multiple pattern generators in the lobster stomatogastric nervous system. J. Neurosci. 14, 630-644.
47. Miller, J.P., and Selverston, A. (1979). Rapid killing of single neurons by irradiation of intracellularly injected dye. Science 206, 702-704.
48. Miller, J.P., and Selverston, A.I. (1982a). Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. II. Oscillatory properties of pyloric neurons. J. Neurophysiol. 48, 1378-1391.
49. Miller, J.P., and Selverston, A.I. (1982b). Mechanisms underlying pattern generation in lobster stomatogastric ganglion as determined by selective inactivation of identified neurons. IV. Network properties of pyloric system. J. Neurophysiol. 48, 1416-1432.
50. Morris, C., and Lecar, H. (1981). Voltage oscillations in the barnacle giant muscle fiber. Biophys. J. 35, 193-213.
51. Mulloney, B. (2003). During fictive locomotion, graded synaptic currents drive bursts of impulses in swimmeret motor neurons. J. Neurosci. 23, 5953-5962.
52. Mulloney, B., Perkel, D.H., and Budelli, R.W. (1981). Motor-pattern production: interaction of chemical and electrical synapses. Brain Res. 229, 25-33.
53. Pearson, K.G., Reye, D.N., Parsons, D.W., and Bicker, G. (1985). Flight-initiating interneurons in the locust. J. Neurophysiol. 53, 910-925.
54. Pereda, A.E., Curti, S., Hoge, G., Cachope, R., Flores, C.E., and Rash, J.E. (2013). Gap junction-mediated electrical transmission: regulatory mechanisms and plasticity. Biochim. Biophys. Acta 1828, 134-146.
55. Prinz, A.A., Bucher, D., and Marder, E. (2004). Similar network activity from disparate circuit parameters. Nat. Neurosci. 7, 1345-1352.
56. Pulver, S.R., Pashkovski, S.L., Hornstein, N.J., Garrity, P.A., and Griffith, L.C. (2009). Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J. Neurophysiol. 101, 3075-3088.
57. Ramirez, J.M., Tryba, A.K., and Peña, F. (2004). Pacemaker neurons and neuronal networks: an integrative view. Curr. Opin. Neurobiol. 14, 665-674.
58. Roopun, A.K., Kramer, M.A., Carracedo, L.M., Kaiser, M., Davies, C.H., Traub, R.D., Kopell, N.J., and Whittington, M.A. (2008). Temporal interactions between cortical rhythms. Front. Neurosci. 2, 145-154.
59. Russell, D.F. (1985). Pattern and reset analysis of the gastric mill rhythm in a spiny lobster, Panulirus interruptus. J. Exp. Biol. 114, 71-98.
60. Selverston, A.I. (2010). Invertebrate central pattern generator circuits. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 2329-2345.
61. Sherman, A., and Rinzel, J. (1992). Rhythmogenic effects of weak electrotonic coupling in neuronal models. Proc. Natl. Acad. Sci. USA 89, 2471-2474.
62. Skinner, F.K., Turrigiano, G.G., and Marder, E. (1993). Frequency and burst duration in oscillating neurons and two-cell networks. Biol. Cybern. 69, 375-383.
63. Soto-Treviño, C., Rabbah, P., Marder, E., and Nadim, F. (2005). Computational model of electrically coupled, intrinsically distinct pacemaker neurons. J. Neurophysiol. 94, 590-604.
64. Tang, L.S., Taylor, A.L., Rinberg, A., and Marder, E. (2012). Robustness of a rhythmic circuit to short- and long-term temperature changes. J. Neurosci. 32, 10075-10085.
65. Traub, R.D. (1995). Model of synchronized population bursts in electrically coupled interneurons containing active dendritic conductances. J. Comput. Neurosci. 2, 283-289.
66. Traub, R.D., Whittington, M.A., Stanford, I.M., and Jefferys, J.G. (1996). A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383, 621-624.
67. Traub, R.D., Cunningham, M.O., and Whittington, M.A. (2011). Chemical synaptic and gap junctional interactions between principal neurons: partners in epileptogenesis. Neural Netw. 24, 515-525.
68. Turrigiano, G., LeMasson, G., and Marder, E. (1995). Selective regulation of current densities underlies spontaneous changes in the activity of cultured neurons. J. Neurosci. 15, 3640-3652.
69. Vervaeke, K., Lorincz, A., Gleeson, P., Farinella, M., Nusser, Z., and Silver, R.A. (2010). Rapid desynchronization of an electrically coupled interneuron network with sparse excitatory synaptic input. Neuron 67, 435-451.
70. Wang, X.J. (1999). Fast burst firing and short-term synaptic plasticity: a model of neocortical chattering neurons. Neuroscience 89, 347-362.
71. Wang, X.J. (2010). Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 90, 1195-1268.
72. Weimann, J.M., and Marder, E. (1994). Switching neurons are integral members of multiple oscillatory networks. Curr. Biol. 4, 896-902.
73. Weimann, J.M., Meyrand, P., and Marder, E. (1991). Neurons that form multiple pattern generators: identification and multiple activity patterns of gastric/pyloric neurons in the crab stomatogastric system. J. Neurophysiol. 65, 111-122.
74. Yizhar, O., Fenno, L.E., Davidson, T.J., Mogri, M., and Deisseroth, K. (2011). Optogenetics in neural systems. Neuron 71, 9-34.
75. Zhang, F., Gradinaru, V., Adamantidis, A.R., Durand, R., Airan, R.D., de Lecea, L., and Deisseroth, K. (2010). Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures. Nat. Protoc. 5, 439-456.