Ionic current variability and functional stability in the nervous system

BioScience

Volumn 64, Issue 7, 2014, Pages 570-580

  Golowasch, Jorge ^a  

^a NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

animal physiology; conductances; homeostasis; neurobiology; variability

Indexed keywords

EID: 84904192639     PISSN: 00063568     EISSN: 15253244     Source Type: Journal    
DOI: 10.1093/biosci/biu070     Document Type: Review

References (63)

1. Amendola J, Woodhouse A, Martin-Eauclaire M-F, Goaillard J-M. 2012. Ca2+/cAMP-sensitive covariation of IA and IH voltage dependences tunes rebound firing in dopaminergic neurons. Journal of Neuroscience 32: 2166-2181.
2. Aradi I, Soltesz I. 2002. Modulation of network behaviour by changes in variance in interneuronal properties. Journal of Physiology 538: 227-251. (Pubitemid 35190052)
3. Aradi I, Santhakumar V, Chen K, Soltesz I. 2002. Postsynaptic effects of GABAergic synaptic diversity: Regulation of neuronal excitability by changes in IPSC variance. Neuropharmacology 43: 511-522. (Pubitemid 35279563)
4. Ball JM, Franklin CC, Tobin A-E, Schulz DJ, Nair SS. 2010. Coregulation of ion channel conductances preserves output in a computational model of a crustacean cardiac motor neuron. Journal of Neuroscience 30: 8637-8649.
5. Bergquist S, Dickman DK, Davis GW. 2010. A hierarchy of cell intrinsic and target-derived homeostatic signaling. Neuron 66: 220-234.
6. Bucher D, Prinz AA, Marder E. 2005. Animal-to-animal variability in motor pattern production in adults and during growth. Journal of Neuroscience 25: 1611-1619. (Pubitemid 40282592)
7. Burdakov D. 2005. Gain control by concerted changes in IA and IH conductances. Neural Computation 17: 991-995. (Pubitemid 40551610)
8. Cohen AH, Ermentrout GB, Kiemel T, Kopell N, Sigvardt KA, Williams TL. 1992. Modelling of intersegmental coordination in the lamprey central pattern generator for locomotion. Trends in Neurosciences 15: 434-438.
9. Davis GW. 2006. Homeostatic control of neural activity: From phenomenology to molecular design. Annual Review of Neuroscience 29: 307-323. (Pubitemid 44476848)
10. Desai NS, Rutherford LC, Turrigiano GG. 1999. Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nature Neuroscience 2: 515-520. (Pubitemid 30491231)
11. Dicaprio R, Jordan G, Hampton T. 1997. Maintenance of motor pattern phase relationships in the ventilatory system of the crab. Journal of Experimental Biology 200: 963-974. (Pubitemid 27161904)
12. Echegoyen J, Neu A, Graber KD, Soltesz I. 2007. Homeostatic plasticity studied using in vivo hippocampal activity-blockade: Synaptic scaling, intrinsic plasticity and age-dependence. PLOS ONE 2 (art. e700).
13. Etheredge JA, Murchison D, Abbott LC, Griffith WH. 2007. Functional compensation by other voltage-gated Ca2+ channels in mouse basal forebrain neurons with CaV2.1 mutations. Brain Research 1140: 105-119. (Pubitemid 46357641)
14. Goaillard J-M, Taylor AL, Schulz DJ, Marder E. 2009. Functional consequences of animal-to-animal variation in circuit parameters. Nature Neuroscience 12: 1424-1430.
15. Golowasch J, Goldman MS, Abbott LF, Marder E. 2002. Failure of averaging in the construction of a conductance-based neuron model. Journal of Neurophysiology 87: 1129-1131. (Pubitemid 34670875)
16. Grashow R, Brookings T, Marder E. 2010. Compensation for variable intrinsic neuronal excitability by circuit-synaptic interactions. Journal of Neuroscience 30: 9145-9156.
17. Greenberg I, Manor Y. 2005. Synaptic depression in conjunction with A-current channels promote phase constancy in a rhythmic network. Journal of Neurophysiology 93: 656-677.
18. Guo W, Jung WE, Marionneau C, Aimond F, Xu H, Yamada KA, Schwarz TL, Demolombe S, Nerbonne JM. 2005. Targeted deletion of Kv4.2 eliminates Ito,f and results in electrical and molecular remodeling, with no evidence of ventricular hypertrophy or myocardial dysfunction. Circulation Research 97: 1342-1350.
19. Haedo RJ, Golowasch J. 2006. Ionic mechanism underlying recovery of rhythmic activity in adult isolated neurons. Journal of Neurophysiology 96: 1860-1876. (Pubitemid 44527442)
20. Howard AL, Neu A, Morgan RJ, Echegoyen JC, Soltesz I. 2007. Opposing modifications in intrinsic currents and synaptic inputs in post-traumatic mossy cells: Evidence for single-cell homeostasis in a hyperexcitable network. Journal of Neurophysiology 97: 2394-2409. (Pubitemid 46411169)
21. Hudson AE, Prinz AA. 2010. Conductance ratios and cellular identity. PLOS Computational Biology 6 (art. e1000838).
22. Khorkova O, Golowasch J. 2007. Neuromodulators, not activity, control coordinated expression of ionic currents. Journal of Neuroscience 27: 8709-8718. (Pubitemid 47254253)
23. Lamb DG, Calabrese RL. 2013. Correlated conductance parameters in leech heart motor neurons contribute to motor pattern formation. PLOS ONE 8 (art. e79267).
24. Leao RM, Li S, Doiron B, Tzounopoulos T. 2012. Diverse levels of an inwardly rectifying potassium conductance generate heterogeneous neuronal behavior in a population of dorsal cochlear nucleus pyramidal neurons. Journal of Neurophysiology 107: 3008-3019.
25. Li J, Baccei ML. 2011. Pacemaker neurons within newborn spinal pain circuits. Journal of Neuroscience 31: 9010-9022.
26. Lien CC, Jonas P. 2003. Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. Journal of Neuroscience 23: 2058-2068. (Pubitemid 36368893)
27. Liss B, Franz O, Sewing S, Bruns R, Neuhoff H, Roeper J. 2001. Tuning pacemaker frequency of individual dopaminergic neurons by Kv4.3L and KChip3.1 transcription. EMBO Journal 20: 5715-5724. (Pubitemid 33010048)
28. Liu Z, Golowasch J, Marder E, Abbott LF. 1998. A model neuron with activity-dependent conductances regulated by multiple calcium sensors. Journal of Neuroscience 18: 2309-2320. (Pubitemid 28141780)
29. Luther JA, Robie AA, Yarotsky J, Reina C, Marder E, Golowasch J. 2003. Episodic bouts of activity accompany recovery of rhythmic output by a neuromodulator-and activity-deprived adult neural network. Journal of Neurophysiology 90: 2720-2730. (Pubitemid 37266536)
30. MacLean JN, Zhang Y, Johnson BR, Harris-Warrick RM. 2003. Activity-independent homeostasis in rhythmically active neurons. Neuron 37: 109-120. (Pubitemid 36106438)
31. MacLean JN, Zhang Y, Goeritz ML, Casey R, Oliva R, Guckenheimer J, Harris-Warrick RM. 2005. Activity-independent coregulation of IA and Ih in rhythmically active neurons. Journal of Neurophysiology 94: 3601-3617. (Pubitemid 41504794)
32. Manor Y, Bose A, Booth V, Nadim F. 2003. Contribution of synaptic depression to phase maintenance in a model rhythmic network. Journal of Neurophysiology 90: 3513-3528. (Pubitemid 37430041)
33. McAnelly ML, Zakon HH. 2000. Coregulation of voltage-dependent kinetics of Na+ and K+ currents in electric organ. Journal of Neuroscience 20: 3408-3414. (Pubitemid 30263156)
34. Mulloney B, Smarandache-Wellmann C. 2012. Neurobiology of the crustacean swimmeret system. Progress in Neurobiology 96: 242-267.
35. Nerbonne JM, Gerber BR, Norris A, Burkhalter A. 2008. Electrical remodelling maintains firing properties in cortical pyramidal neurons lacking KCND2-encoded A-type K+ currents. The Journal of Physiology 586: 1565-1579. (Pubitemid 351404961)
36. Norris BJ, Wenning A, Wright TM, Calabrese RL. 2011. Constancy and variability in the output of a central pattern generator. Journal of Neuroscience 31: 4663-4674.
37. Nusser Z. 2009. Variability in the subcellular distribution of ion channels increases neuronal diversity. Trends in Neurosciences 32: 267-274.
38. OLeary T, Williams AH, Caplan JS, Marder E. 2013. Correlations in ion channel expression emerge from homeostatic tuning rules. Proceedings of the National Academy of Sciences 110: E2645-2654.
39. Olypher AV, Calabrese RL. 2007. Using constraints on neuronal activity to reveal compensatory changes in neuronal parameters. Journal of Neurophysiology 98: 3749-3758.
40. Prinz AA, Bucher D, Marder E. 2004. Similar network activity from disparate circuit parameters. Nature Neuroscience 7: 1345-1352. (Pubitemid 41057757)
41. Ransdell JL, Nair SS, Schulz DJ. 2012. Rapid homeostatic plasticity of intrinsic excitability in a central pattern generator network stabilizes functional neural network output. Journal of Neuroscience 32: 9649-9658.
42. Ransdell JL, Nair SS, Schulz DJ.. 2013. Neurons within the same network independently achieve conserved output by differentially balancing variable conductance magnitudes. Journal of Neuroscience 33: 9950-9956.
43. Roffman RC, Norris BJ, Calabrese RL. 2012. Animal-to-animal variability of connection strength in the leech heartbeat central pattern generator. Journal of Neurophysiology 107: 1681-1693.
44. Santhakumar V, Soltesz I. 2004. Plasticity of interneuronal species diversity and parameter variance in neurological diseases. Trends in Neurosciences 27: 504-510. (Pubitemid 38951044)
45. Schulz DJ, Goaillard J-M, Marder E. 2006. Variable channel expression in identified single and electrically coupled neurons in different animals. Nature Neuroscience 9: 356-362. (Pubitemid 43290965)
46. Schulz DJ, Goaillard J-M, Marder E.. 2007. Quantitative expression profiling of identified neurons reveals cell-specific constraints on highly variable levels of gene expression. Proceedings of the National Academy of Sciences 104: 13187-13191. (Pubitemid 351737614)
47. Soofi W, Archila S, Prinz AA. 2012. Co-variation of ionic conductances supports phase maintenance in stomatogastric neurons. Journal of Computational Neuroscience 33: 77-95.
48. Swensen AM, Bean BP. 2005. Robustness of burst firing in dissociated purkinje neurons with acute or long-term reductions in sodium conductance. Journal of Neuroscience 25: 3509-3520.
49. Taylor AL, Hickey TJ, Prinz AA, Marder E. 2006. Structure and visualization of high-dimensional conductance spaces. Journal of Neurophysiology 96: 891-905. (Pubitemid 44155224)
50. Taylor AL, Goaillard J-M, Marder E. 2009. How multiple conductances determine electrophysiological properties in a multicompartment model. Journal of Neuroscience 29: 5573-5586.
51. Temporal S, Desai M, Khorkova O, Varghese G, Dai A, Schulz DJ, Golowasch J. 2012. Neuromodulation independently determines correlated channel expression and conductance levels in motor neurons of the stomatogastric ganglion. Journal of Neurophysiology 107: 718-727.
52. Thoby-Brisson M, Simmers J. 1998. Neuromodulatory inputs maintain expression of a lobster motor pattern-generating network in a modulation-dependent state: Evidence from long-term decentralization in vitro. Journal of Neuroscience 18: 2212-2225. (Pubitemid 28141425)
53. Tobin A-E, Cruz-Bermdez ND, Marder E, Schulz DJ. 2009. Correlations in ion channel mRNA in rhythmically active neurons. PLOS ONE 4 (art. e6742).
54. Toledo-Rodriguez M, Blumenfeld B, Wu C, Luo J, Attali B, Goodman P, Markram H. 2004. Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. Cerebral Cortex 14: 1310-1327. (Pubitemid 39507282)
55. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB. 1998. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391: 892-896. (Pubitemid 28157666)
56. Unal CT, Golowasch JP, Zaborszky L. 2012. Adult mouse basal forebrain harbors two distinct cholinergic populations defined by their electrophysiology. Frontiers in Behavioral Neuroscience 6: 21.
57. Vähäsöyrinki M, Niven JE, Hardie RC, Weckstrom M, Juusola M. 2006. Robustness of neural coding in Drosophila photoreceptors in the absence of slow delayed rectifier K+ channels. Journal of Neuroscience 26: 2652-2660. (Pubitemid 43357848)
58. Van Welie I, van Hooft JA, Wadman WJ. 2004. Homeostatic scaling of neuronal excitability by synaptic modulation of somatic hyperpolarization- activated Ih channels. Proceedings of the National Academy of Sciences 101: 5123-5128. (Pubitemid 38469213)
59. Williams AH, Kwiatkowski MA, Mortimer AL, Marder E, Zeeman ML, Dickinson PS. 2013. Animal-to-animal variability in the phasing of the crustacean cardiac motor pattern: An experimental and computational analysis. Journal of Neurophysiology 109: 2451-2465.
60. Wu YC, Fettiplace R. 1996. A developmental model for generating frequency maps in the reptilian and avian cochleas. Biophysical Journal 70: 2557-2570. (Pubitemid 26000956)
61. Zakon H, McAnelly L, Smith GT, Dunlap K, Lopreato G, Oestreich J, Few WP. 1999. Plasticity of the electric organ discharge: Implications for the regulation of ionic currents. Journal of Experimental Biology 202: 1409-1416. (Pubitemid 29285345)
62. Zhao S, Golowasch J. 2012. Ionic current correlations underlie the global tuning of large numbers of neuronal activity attributes. Journal of Neuroscience 32: 13380-13388.
63. Zhao S, Golowasch J, Nadim F. 2010. Pacemaker neuron and network oscillations depend on a neuromodulator-regulated linear current. Frontiers in Behavioral Neuroscience 4: 21.