Do Cortical Circuits Need Protecting from Themselves?

Trends in Neurosciences

Volumn 39, Issue 8, 2016, Pages 502-511

  Trevelyan, Andrew J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN CORTEX; BRAIN FUNCTION; HOMEOSTASIS; HUMAN; INTERNEURON; NERVE CELL EXCITABILITY; NERVE CELL INHIBITION; NERVE CELL NETWORK; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; REVIEW; SEIZURE; ANIMAL; NERVE TRACT; NEUROPROTECTION; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CEREBRAL CORTEX; HUMANS; INTERNEURONS; NEURAL PATHWAYS; NEUROPROTECTION; SEIZURES;

EID: 84991228037     PISSN: 01662236     EISSN: 1878108X     Source Type: Journal    
DOI: 10.1016/j.tins.2016.06.002     Document Type: Review

References (96)

1. 1 Beggs, J.M., The criticality hypothesis: how local cortical networks might optimize information processing. Philos. Trans. A Math. Phys. Eng. Sci. 366 (2008), 329–343.
2. 2 Buzsáki, G., Rhythms of the Brain. 2006, Oxford University Press.
3. 3 Bi, G.Q., Rubin, J., Timing in synaptic plasticity: from detection to integration. Trends Neurosci. 28 (2005), 222–228.
4. 4 Markram, H., et al. A history of spike-timing-dependent plasticity. Front. Synaptic Neurosci., 3, 2011, 4.
5. 5 Abbott, L.F., Nelson, S.B., Synaptic plasticity: taming the beast. Nat. Neurosci. 3 Suppl. (2000), 1178–1183.
6. 6 Cossell, L., et al. Functional organization of excitatory synaptic strength in primary visual cortex. Nature 518 (2015), 399–403.
7. 7 Husain, A.M., Evoked potentials overview. Ebersole, J.S., (eds.) Current Practice of Clinical EEG (4th edn), 2014, Lippincott Williams & Wilkins, 442–487.
8. 8 Italiano, D., et al. Genetics of reflex seizures and epilepsies in humans and animals. Epilepsy Res. 121 (2016), 47–54.
9. 9 Stephani, U., et al. Genetics of photosensitivity (photoparoxysmal response): a review. Epilepsia 45:Suppl. 1 (2004), 19–23.
10. 10 Tian, G.F., et al. An astrocytic basis of epilepsy. Nat. Med. 11 (2005), 973–981.
11. 11 Gomez-Gonzalo, M., et al. An excitatory loop with astrocytes contributes to drive neurons to seizure threshold. PLoS Biol., 8, 2010, e1000352.
12. 12 Robel, S., Sontheimer, H., Glia as drivers of abnormal neuronal activity. Nat. Neurosci. 19 (2016), 28–33.
13. 13 Freund, T.F., Buzsaki, G., Interneurons of the hippocampus. Hippocampus 6 (1996), 347–470.
14. 14 Cobb, S.R., et al. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378 (1995), 75–78.
15. 15 Deuchars, J., Thomson, A.M., Innervation of burst firing spiny interneurons by pyramidal cells in deep layers of rat somatomotor cortex: paired intracellular recordings with biocytin filling. Neuroscience 69 (1995), 739–755.
16. 16 Le Bon-Jego, M., Yuste, R., Persistently active, pacemaker-like neurons in neocortex. Front. Neurosci. 1 (2007), 123–129.
17. 17 McCormick, D.A., Huguenard, J.R., A model of the electrophysiological properties of thalamocortical relay neurons. J. Neurophysiol. 68 (1992), 1384–1400.
18. 18 Clopath, C., et al. Connectivity reflects coding: a model of voltage-based STDP with homeostasis. Nat. Neurosci. 13 (2010), 344–352.
19. 19 Ko, H., et al. The emergence of functional microcircuits in visual cortex. Nature 496 (2013), 96–100.
20. 20 Lien, A.D., Scanziani, M., Tuned thalamic excitation is amplified by visual cortical circuits. Nat. Neurosci. 16 (2013), 1315–1323.
21. 21 Li, Y.T., et al. Linear transformation of thalamocortical input by intracortical excitation. Nat. Neurosci. 16 (2013), 1324–1330.
22. 22 Lee, W.C., et al. Anatomy and function of an excitatory network in the visual cortex. Nature 532 (2016), 370–374.
23. 23 Reinhold, K., et al. Distinct recurrent versus afferent dynamics in cortical visual processing. Nat. Neurosci. 18 (2015), 1789–1797.
24. 24 Buzsaki, G., Mizuseki, K., The log-dynamic brain: how skewed distributions affect network operations. Nat. Rev. Neurosci. 15 (2014), 264–278.
25. 25 Somogyi, P., Klausberger, T., Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. 562 (2005), 9–26.
26. 26 Pfeffer, C.K., et al. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat. Neurosci. 16 (2013), 1068–1076.
27. 27 Jiang, X., et al. Principles of connectivity among morphologically defined cell types in adult neocortex. Science, 350, 2015, aac9462.
28. 28 Klausberger, T., Somogyi, P., Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321 (2008), 53–57.
29. 29 Buzsaki, G., Wang, X.J., Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35 (2012), 203–225.
30. 30 Traub, R.D., et al. Fast Oscillations in Cortical Circuits. 1999, MIT Press.
31. 31 Niell, C.M., Stryker, M.P., Highly selective receptive fields in mouse visual cortex. J. Neurosci. 28 (2008), 7520–7536.
32. 2+ imaging in transgenic mice. J. Neurosci. 27 (2007), 2145–2149.
33. 33 Liu, B.H., et al. Visual receptive field structure of cortical inhibitory neurons revealed by two-photon imaging guided recording. J. Neurosci. 29 (2009), 10520–10532.
34. 34 Kerlin, A.M., et al. Broadly tuned response properties of diverse inhibitory neuron subtypes in mouse visual cortex. Neuron 67 (2010), 858–871.
35. 35 Wilson, N.R., et al. Division and subtraction by distinct cortical inhibitory networks in vivo. Nature 488 (2012), 343–348.
36. 36 Atallah, B.V., et al. Parvalbumin-expressing interneurons linearly transform cortical responses to visual stimuli. Neuron 73 (2012), 159–170.
37. 37 Ferster, D., Miller, K.D., Neural mechanisms of orientation selectivity in the visual cortex. Annu. Rev. Neurosci. 23 (2000), 441–471.
38. 38 Bock, D.D., et al. Network anatomy and in vivo physiology of visual cortical neurons. Nature 471 (2011), 177–182.
39. 39 Hofer, S.B., et al. Differential connectivity and response dynamics of excitatory and inhibitory neurons in visual cortex. Nat. Neurosci. 14 (2011), 1045–1052.
40. 40 Miles, R., et al. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16 (1996), 815–823.
41. 41 Inan, M., et al. Dense and overlapping innervation of pyramidal neurons by chandelier cells. J. Neurosci. 33 (2013), 1907–1914.
42. 42 Hubel, D.H., Wiesel, T.N., Ferrier Lecture. Functional architecture of macaque monkey visual cortex. Proc. Biol. Sci 198 (1977), 1–59.
43. 43 Hilgetag, C.C., et al. The primate connectome in context: Principles of connections of the cortical visual system. Neuroimage. 134 (2016), 685–702.
44. 44 Schiller, J., et al. NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature 404 (2000), 285–289.
45. 45 Hoffman, K.L., et al. The upshot of up states in the neocortex: from slow oscillations to memory formation. J. Neurosci. 27 (2007), 11838–11841.
46. 46 Raimondo, J.V., et al. Ion dynamics during seizures. Front. Cell. Neurosci., 9, 2015, 419.
47. − in hippocampal CA3 neurons. J. Neurophysiol. 61 (1989), 512–523.
48. 48 Thompson, S.M., Gahwiler, B.H., Activity-dependent disinhibition. I. Repetitive stimulation reduces IPSP driving force and conductance in the hippocampus in vitro. J. Neurophysiol. 61 (1989), 501–511.
49. 49 Kaila, K., Voipio, J., Postsynaptic fall in intracellular pH induced by GABA-activated bicarbonate conductance. Nature 330 (1987), 163–165.
50. 50 Trevelyan, A.J., The direct relationship between inhibitory currents and local field potentials. J. Neurosci. 29 (2009), 15299–15307.
51. 51 Kaila, K., et al. Cation–chloride cotransporters in neuronal development, plasticity and disease. Nat. Rev. Neurosci. 15 (2014), 637–654.
52. 52 Ellender, T.J., et al. Excitatory effects of parvalbumin-expressing interneurons maintain hippocampal epileptiform activity via synchronous afterdischarges. J. Neurosci. 34 (2014), 15208–15222.
53. 53 Fujiwara-Tsukamoto, Y., et al. Prototypic seizure activity driven by mature hippocampal fast-spiking interneurons. J. Neurosci. 30 (2010), 13679–13689.
54. − cotransporter KCC2 promotes GABAergic excitation in the mature rat hippocampus. J. Physiol. 588 (2010), 1527–1540.
55. 55 Kaila, K., et al. GABA actions and ionic plasticity in epilepsy. Curr. Opin. Neurobiol. 26 (2014), 34–41.
56. 56 Miles, R., Wong, R.K., Single neurones can initiate synchronized population discharge in the hippocampus. Nature 306 (1983), 371–373.
57. 57 Hauser, W.A., et al. Incidence of epilepsy and unprovoked seizures in Rochester, Minnesota: 1935-1984. Epilepsia 34 (1993), 453–468.
58. 58 Isaacson, J.S., Scanziani, M., How inhibition shapes cortical activity. Neuron 72 (2011), 231–243.
59. 59 Moore, C.I., et al. Neocortical interneurons: from diversity, strength. Cell 142 (2010), 189–193.
60. 60 Trevelyan, A.J., et al. Modular propagation of epileptiform activity: evidence for an inhibitory veto in neocortex. J. Neurosci. 26 (2006), 12447–12455.
61. 61 Megias, M., et al. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102 (2001), 527–540.
62. 62 Pouille, F., et al. The contribution of synaptic location to inhibitory gain control in pyramidal cells. Physiol. Rep., 1, 2013, e00067.
63. 63 Gulyas, A.I., et al. Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J. Neurosci. 19 (1999), 10082–10097.
64. 64 Asinof, S.K., et al. Independent neuronal origin of seizures and behavioral comorbidities in an animal model of a severe childhood genetic epileptic encephalopathy. PLoS Genet., 11, 2015, e1005347.
65. 65 Rossignol, E., et al. CaV 2.1 ablation in cortical interneurons selectively impairs fast-spiking basket cells and causes generalized seizures. Ann. Neurol. 74 (2013), 209–222.
66. 66 Ogiwara, I., et al. Nav1.1 localizes to axons of parvalbumin-positive inhibitory interneurons: a circuit basis for epileptic seizures in mice carrying an Scn1a gene mutation. J. Neurosci. 27 (2007), 5903–5914.
67. 2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12 (1994), 1281–1289.
68. 68 Pouille, F., Scanziani, M., Routing of spike series by dynamic circuits in the hippocampus. Nature 429 (2004), 717–723.
69. 69 Sessolo, M., et al. Parvalbumin-positive inhibitory interneurons oppose propagation but favor generation of focal epileptiform activity. J. Neurosci. 35 (2015), 9544–9557.
70. 70 Lovett-Barron, M., et al. Regulation of neuronal input transformations by tunable dendritic inhibition. Nat. Neurosci. 15 (2012), 423–430.
71. 71 Gigout, S., et al. Effects of gap junction blockers on human neocortical synchronization. Neurobiol. Dis. 22 (2006), 496–508.
72. B antagonists. Neuropharmacology 43 (2002), 563–572.
73. 73 Trevelyan, A.J., et al. The source of afterdischarge activity in neocortical tonic-clonic epilepsy. J. Neurosci. 27 (2007), 13513–13519.
74. 74 Smith, E.H., et al. The ictal wavefront is the spatiotemporal source of discharges during spontaneous human seizures. Nat. Commun., 7, 2016, 11098.
75. 75 Ziburkus, J., et al. Interneuron and pyramidal cell interplay during in vitro seizure-like events. J. Neurophysiol. 95 (2006), 3948–3954.
76. 76 Alfonsa, H., et al. The contribution of raised intraneuronal chloride to epileptic network activity. J. Neurosci. 35 (2015), 7715–7726.
77. 77 Netoff, T.I., Schiff, S.J., Decreased neuronal synchronization during experimental seizures. J. Neurosci. 22 (2002), 7297–7307.
78. 78 Shouse, M.N., Quigg, M.S., Chronbiology. Engel, J., Pedley, T.A., (eds.) Epilepsy: A Comprehensive Textbook, 2nd, 2008, Lippincott Williams & Wilkins, 1961–1974.
79. 79 Ewell, L.A., et al. Brain state is a major factor in preseizure hippocampal network activity and influences success of seizure intervention. J. Neurosci. 35 (2015), 15635–15648.
80. 80 Cook, M.J., et al. Prediction of seizure likelihood with a long-term, implanted seizure advisory system in patients with drug-resistant epilepsy: a first-in-man study. Lancet Neurol. 12 (2013), 563–571.
81. 81 Liu, X., et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484 (2012), 381–385.
82. 82 Morgan, J.I., et al. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237 (1987), 192–197.
83. 83 Trevelyan, A.J., et al. The information content of physiological and epileptic brain activity. J. Physiol. 591 (2013), 799–805.
84. 84 Schevon, C.A., et al. Evidence of an inhibitory restraint of seizure activity in humans. Nat. Commun., 3, 2012, 1060.
85. 85 Shew, W.L., et al. Neuronal avalanches imply maximum dynamic range in cortical networks at criticality. J. Neurosci. 29 (2009), 15595–15600.
86. 86 Meisel, C., et al. Failure of adaptive self-organized criticality during epileptic seizure attacks. PLoS Comput. Biol., 8, 2012, e1002312.
87. 87 Beggs, J.M., Plenz, D., Neuronal avalanches in neocortical circuits. J. Neurosci. 23 (2003), 11167–11177.
88. 88 Trevelyan, A.J., Schevon, C.A., How inhibition influences seizure propagation. Neuropharmacology 69 (2013), 45–54.
89. 89 Prince, D.A., Wilder, B.J., Control mechanisms in cortical epileptogenic foci “Surround” inhibition. Arch. Neurol. 16 (1967), 194–202.
90. 90 Dichter, M., Spencer, W.A., Penicillin-induced interictal discharges from the cat hippocampus. II. Mechanisms underlying origin and restriction. J. Neurophysiol. 32 (1969), 663–687.
91. 91 Schwartz, T.H., Bonhoeffer, T., In vivo optical mapping of epileptic foci and surround inhibition in ferret cerebral cortex. Nat. Med. 7 (2001), 1063–1067.
92. 92 Timofeev, I., et al. The role of chloride-dependent inhibition and the activity of fast-spiking neurons during cortical spike-wave electrographic seizures. Neuroscience 114 (2002), 1115–1132.
93. 93 Cammarota, M., et al. Fast spiking interneuron control of seizure propagation in a cortical slice model of focal epilepsy. J. Physiol. 591 (2013), 807–822.
94. 94 Trevelyan, A.J., et al. Feedforward inhibition contributes to the control of epileptiform propagation speed. J. Neurosci. 27 (2007), 3383–3387.
95. 95 Weiss, S.A., et al. Seizure localization using ictal phase-locked high gamma: a retrospective surgical outcome study. Neurology 84 (2015), 2320–2328.
96. 96 Merricks, E.M., et al. Single unit action potentials in humans and the effect of seizure activity. Brain 138 (2015), 2891–2906.