LTS and FS inhibitory interneurons, short-term synaptic plasticity, and cortical circuit dynamics

PLoS Computational Biology

Volumn 7, Issue 10, 2011, Pages

  Hayut, Itai ^a   Fanselow, Erika E ^b,c   Connors, Barry W ^b   Golomb, David ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b BROWN UNIVERSITY   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; TIMING CIRCUITS;

CIRCUIT DYNAMICS; FAST SPIKING; FAST SPIKING CELLS; FIRING RATES; HIGH RATE; INHIBITORY INTERNEURONS; LOW THRESHOLDS; SHORT-TERM SYNAPTIC PLASTICITY; SPIKING CELLS; SPIKING NEURONES;

NEURONS;

ARTICLE; CELL ACTIVITY; CELL COUNT; CELL POPULATION; CELL PROTECTION; CELL SHAPE; CELL TYPE; CONTROLLED STUDY; CYTOARCHITECTURE; FACILITATION; FAST SPIKE NEURON; INTERNEURON; LOW THRESHOLD SPIKE NEURON; MATHEMATICAL MODEL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NEUROMODULATION; OSCILLATION; STEADY STATE; ABSENCE; ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; BRAIN CORTEX; ELECTROSTIMULATION; HUMAN; PATHOPHYSIOLOGY; PHYSIOLOGY; RAT; THALAMUS;

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS;

ACTION POTENTIALS; ANIMALS; CEREBRAL CORTEX; COMPUTATIONAL BIOLOGY; ELECTRIC STIMULATION; EPILEPSY, ABSENCE; HUMANS; INTERNEURONS; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; RATS; THALAMUS;

EID: 80055065460     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002248     Document Type: Article

References (86)

1. Amitai Y, Gibson JR, Beierlein M, Patrick SL, Ho AM, et al. (2002) The spatial dimensions of electrically coupled networks of interneurons in the neocortex. J Neurosci 22: 4142-4152.
2. Kawaguchi Y, Kubota Y, (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7: 476-486.
3. Wang Y, Toledo-Rodriguez M, Gupta A, Wu C, Silberberg G, et al. (2004) Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol 561: 65-90.
4. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, et al. (2004) Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807.
5. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, et al. (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9: 557-568.
6. Oliva AA Jr, Jiang M, Lam T, Smith KL, Swann JW, (2000) Novel hippocampal interneuronal subtypes identified using transgenic mice that express green fluorescent protein in GABAergic interneurons. J Neurosci 20: 3354-3368.
7. Fanselow EE, Richardson KA, Connors BW, (2008) Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100: 2640-2652.
8. Fanselow EE, Connors BW, (2010) The roles of somatostatin-expressing (GIN) and fast-spiking inhibitory interneurons in UP-DOWN states of mouse neocortex. J Neurophysiol 104: 596-606.
9. Beierlein M, Gibson JR, Connors BW, (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90: 2987-3000.
10. Gibson JR, Beierlein M, Connors BW, (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402: 75-79.
11. Thomson AM, Deuchars J, West DC, (1993) Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation. Neuroscience 54: 347-360.
12. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, et al. (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1: 279-285.
13. Markram H, Wang Y, Tsodyks M, (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 95: 5323-5328.
14. Deans MR, Gibson JR, Sellitto C, Connors BW, Paul DL, (2001) Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36. Neuron 31: 477-485.
15. Cruikshank SJ, Urabe H, Nurmikko AV, Connors BW, (2010) Pathway-specific feedforward circuits between thalamus and neocortex revealed by selective optical stimulation of axons. Neuron 65: 230-245.
16. Tan Z, Hu H, Huang ZJ, Agmon A, (2008) Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc Natl Acad Sci U S A 105: 2187-2192.
17. Gentet LJ, Avermann M, Matyas F, Staiger JF, Petersen CC, (2010) Membrane potential dynamics of GABAergic neurons in the barrel cortex of behaving mice. Neuron 65: 422-435.
18. Silberberg G, Markram H, (2007) Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53: 735-746.
19. Kapfer C, Glickfeld LL, Atallah BV, Scanziani M, (2007) Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 10: 743-753.
20. Berger TK, Silberberg G, Perin R, Markram H, (2010) Brief bursts self-inhibit and correlate the pyramidal network. PLoS Biol 8: e1000473.
21. Buckmaster PS, Jongen-Relo AL, (1999) Highly specific neuron loss preserves lateral inhibitory circuits in the dentate gyrus of kainate-induced epileptic rats. J Neurosci 19: 9519-9529.
22. Cossart R, Dinocourt C, Hirsch JC, Merchan-Perez A, De Felipe J, et al. (2001) Dendritic but not somatic GABAergic inhibition is decreased in experimental epilepsy. Nat Neurosci 4: 52-62.
23. Lee CK, Huguenard JR, (2011) Martinotti cells: community organizers. Neuron 69: 1042-1045.
24. Tsodyks M, Uziel A, Markram H, (2000) Synchrony generation in recurrent networks with frequency-dependent synapses. J Neurosci 20: RC50.
25. Loebel A, Tsodyks M, (2002) Computation by ensemble synchronization in recurrent networks with synaptic depression. J Comput Neurosci 13: 111-124.
26. Holcman D, Tsodyks M, (2006) The emergence of Up and Down states in cortical networks. PLoS Comput Biol 2: e23.
27. Melamed O, Barak O, Silberberg G, Markram H, Tsodyks M, (2008) Slow oscillations in neural networks with facilitating synapses. J Comput Neurosci 25: 308-316.
28. Wilson HR, Cowan JD, (1972) Excitatory and inhibitory interactions in localized populations of model neurons. Biophys J 12: 1-24.
29. Shriki O, Hansel D, Sompolinsky H, (2003) Rate models for conductance-based cortical neuronal networks. Neural Comput 15: 1809-1841.
30. Golomb D, Ahissar E, Kleinfeld D, (2006) Coding of stimulus frequency by latency in thalamic networks through the interplay of GABAB-mediated feedback and stimulus shape. J Neurophysiol 95: 1735-1750.
31. Tsodyks M, Pawelzik K, Markram H, (1998) Neural networks with dynamic synapses. Neural Comput 10: 821-835.
32. Barak O, Tsodyks M, (2007) Persistent activity in neural networks with dynamic synapses. PLoS Comput Biol 3: e35.
33. Rinzel J, Frankel P, (1992) Activity patterns of a slow synapse network predicted by explicitly averaging spike dynamics. Neural Comput 4: 534-545.
34. Ermentrout B, (1994) Reduction of conductance-based models with slow synapses to neural nets. Neural Comput 6: 679-695.
35. Viaene AN, Petrof I, Sherman SM, (2011) Synaptic properties of thalamic input to layers 2/3 and 4 of primary somatosensory and auditory cortices. J Neurophysiol 105: 279-292.
36. Cruikshank SJ, Lewis TJ, Connors BW, (2007) Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 10: 462-468.
37. Golomb D, Wang XJ, Rinzel J, (1994) Synchronization properties of spindle oscillations in a thalamic reticular nucleus model. J Neurophysiol 72: 1109-1126.
38. Tsodyks MV, Markram H, (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94: 719-723.
39. Hansel D, Sompolinsky H, (1998) Modeling feature selectivity in local cortical circuits. In: Koch C, Segev I, editors. Methods in Neuronal Modeling: From Ions to Networks Cambridge MIT Press pp. 499-567.
40. Ermentrout B, (1998) Linearization of F-I curves by adaptation. Neural Comput 10: 1721-1729.
41. Wang XJ, (1999) Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. J Neurosci 19: 9587-9603.
42. Steriade M, Contreras D, (1998) Spike-wave complexes and fast components of cortically generated seizures. I. Role of neocortex and thalamus. J Neurophysiol 80: 1439-1455.
43. Crunelli V, Leresche N, (2002) Childhood absence epilepsy: genes, channels, neurons and networks. Nat Rev Neurosci 3: 371-382.
44. Engel J, Pedley TA, (2008) Epilepsy: a comprehensive textbook Philadelphia, PA Lippincott Williams & Wilkins.
45. Krauss GL, Fisher RS, (2007) The Johns Hopkins atlas of digital EEG: an interactive training guide Baltimore The Johns Hopkins University Press.
46. Bal T, von Krosigk M, McCormick DA, (1995) Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. J Physiol 483 (Pt 3): 641-663.
47. Wang Y, Gupta A, Toledo-Rodriguez M, Wu CZ, Markram H, (2002) Anatomical, physiological, molecular and circuit properties of nest basket cells in the developing somatosensory cortex. Cereb Cortex 12: 395-410.
48. Pinto DJ, Brumberg JC, Simons DJ, (2000) Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 83: 1158-1166.
49. Swadlow HA, (2003) Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13: 25-32.
50. Strogatz SH, (1994) Nonlinear Dynamics and Chaos, with Applications to Physics, Biology, Chemistry and Engineering Reading Addison-Wesley.
51. Rinzel J, Ermentrout GB, (1998) Analysis of neural excitability and oscillations. In: Koch C, Segev I, editors. Methods in Neuronal Modeling: From Ions to Networks. 2nd ed Cambridge MIT Press pp. 251-291.
52. Izhikevich EM, (2007) Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting Cambridge, MA MIT Press.
53. Bertram R, Butte MJ, Kiemel T, Sherman A, (1995) Topological and phenomenological classification of bursting oscillations. Bull Math Biol 57: 413-439.
54. Golomb D, Yue C, Yaari Y, (2006) Contribution of persistent Na+ current and M-type K+ current to somatic bursting in CA1 pyramidal cells: combined experimental and modeling study. J Neurophysiol 96: 1912-1926.
55. Golomb D, Donner K, Shacham L, Shlosberg D, Amitai Y, et al. (2007) Mechanisms of firing patterns in fast-spiking cortical interneurons. PLoS Comput Biol 3: e156.
56. Holt GR, Koch C, (1997) Shunting inhibition does not have a divisive effect on firing rates. Neural Comput 9: 1001-1013.
57. Chance FS, Abbott LF, Reyes AD, (2002) Gain modulation from background synaptic input. Neuron 35: 773-782.
58. Hansel D, Mato G, (2003) Asynchronous states and the emergence of synchrony in large networks of interacting excitatory and inhibitory neurons. Neural Comput 15: 1-56.
59. Dayan P, Abbott LF, (2005) Theoretical Neuroscience- Computational and Mathematical Modeling of Neural Systems Cambridge, MA The MIT Press.
60. Steriade M, Nunez A, Amzica F, (1993) A novel slow (<1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J Neurosci 13: 3252-3265.
61. Contreras D, Timofeev I, Steriade M, (1996) Mechanisms of long-lasting hyperpolarizations underlying slow sleep oscillations in cat corticothalamic networks. J Physiol 494 (Pt 1): 251-264.
62. Lampl I, Reichova I, Ferster D, (1999) Synchronous membrane potential fluctuations in neurons of the cat visual cortex. Neuron 22: 361-374.
63. Petersen CC, Hahn TT, Mehta M, Grinvald A, Sakmann B, (2003) Interaction of sensory responses with spontaneous depolarization in layer 2/3 barrel cortex. Proc Natl Acad Sci U S A 100: 13638-13643.
64. Sanchez-Vives MV, McCormick DA, (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3: 1027-1034.
65. Compte A, Sanchez-Vives MV, McCormick DA, Wang XJ, (2003) Cellular and network mechanisms of slow oscillatory activity (<1 Hz) and wave propagations in a cortical network model. J Neurophysiol 89: 2707-2725.
66. Golanov EV, Reis DJ, (1996) Contribution of oxygen-sensitive neurons of the rostral ventrolateral medulla to hypoxic cerebral vasodilatation in the rat. J Physiol 495 (Pt 1): 201-216.
67. Drew PJ, Duyn JH, Golanov E, Kleinfeld D, (2008) Finding coherence in spontaneous oscillations. Nat Neurosci 11: 991-993.
68. Tsodyks M, Kenet T, Grinvald A, Arieli A, (1999) Linking spontaneous activity of single cortical neurons and the underlying functional architecture. Science 286: 1943-1946.
69. Ecker AS, Berens P, Keliris GA, Bethge M, Logothetis NK, et al. (2010) Decorrelated neuronal firing in cortical microcircuits. Science 327: 584-587.
70. Renart A, de la Rocha J, Bartho P, Hollender L, Parga N, et al. (2010) The asynchronous state in cortical circuits. Science 327: 587-590.
71. Murayama M, Perez-Garci E, Nevian T, Bock T, Senn W, et al. (2009) Dendritic encoding of sensory stimuli controlled by deep cortical interneurons. Nature 457: 1137-1141.
72. Borgers C, Kopell N, (2003) Synchronization in networks of excitatory and inhibitory neurons with sparse, random connectivity. Neural Comput 15: 509-538.
73. Vierling-Claassen D, Cardin JA, Moore CI, Jones SR, (2010) Computational modeling of distinct neocortical oscillations driven by cell-type selective optogenetic drive: separable resonant circuits controlled by low-threshold spiking and fast-spiking interneurons. Front Hum Neurosci 4: 198.
74. Lewis DA, Hashimoto T, Volk DW, (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6: 312-324.
75. Patrick SL, Connors BW, Landisman CE, (2006) Developmental changes in somatostatin-positive interneurons in a freeze-lesion model of epilepsy. Epilepsy Res 70: 161-171.
76. Berg RW, Kleinfeld D, (2003) Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. J Neurophysiol 89: 104-117.
77. Golomb D, Kleinfeld D, Reid RC, Shapley RM, Shraiman BI, (1994) On temporal codes and the spatiotemporal response of neurons in the lateral geniculate nucleus. J Neurophysiol 72: 2990-3003.
78. Zucker RS, Regehr WG, (2002) Short-term synaptic plasticity. Annu Rev Physiol 64: 355-405.
79. Fuhrmann G, Cowan A, Segev I, Tsodyks M, Stricker C, (2004) Multiple mechanisms govern the dynamics of depression at neocortical synapses of young rats. J Physiol 557: 415-438.
80. Neher E, Sakaba T, (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59: 861-872.
81. Connors BW, (1984) Initiation of synchronized neuronal bursting in neocortex. Nature 310: 685-687.
82. Telfeian AE, Connors BW, (1998) Layer-specific pathways for the horizontal propagation of epileptiform discharges in neocortex. Epilepsia 39: 700-708.
83. Wang Y, Markram H, Goodman PH, Berger TK, Ma J, et al. (2006) Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat Neurosci 9: 534-542.
84. Galarreta M, Hestrin S, (1998) Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci 1: 587-594.
85. Fanselow EE, Connors BW, (2006) Somatostatin-expressing inhibitory interneurons of the neocortex are potently and selectively activated under a wide range of conditions. Soc Neurosco Abstr 31: 796.718.
86. Ermentrout B, (2002) Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students (software, environment, tools) Philadelphia Society for Industrial and Applied Mathematics.