Selective functional interactions between excitatory and inhibitory cortical neurons and differential contribution to persistent activity of the slow oscillation

Journal of Neuroscience

Volumn 32, Issue 35, 2012, Pages 12165-12179

  Tahvildari, Babak ^a   Wölfel, Markus ^a   Duque, Alvaro ^a   McCormick, David A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROPEPTIDE Y; SEROTONIN 3A RECEPTOR; SOMATOSTATIN; VASOACTIVE INTESTINAL POLYPEPTIDE;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ENTORHINAL CORTEX; FEMALE; HYPERPOLARIZATION; INTERNEURON; MALE; MEMBRANE POTENTIAL; MOUSE; NERVE CELL NETWORK; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SPIKE; STELLATE CELL; SYNAPTIC POTENTIAL; TRANSGENIC MOUSE;

ANIMALS; BIOLOGICAL CLOCKS; CEREBRAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; HUMANS; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; NEURONS; ORGAN CULTURE TECHNIQUES; REACTION TIME;

EID: 84865461224     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1181-12.2012     Document Type: Article

References (68)

1. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, Feld-meyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, et al. (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557-568.
2. Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90:2987-3000.
3. Canto CB, Wouterlood FG, Witter MP (2008) What does the anatomical organization of the entorhinal cortex tell us? Neural Plast 2008:381243.
4. 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.
5. Connors BW, Prince DA (1982) Effects of local anesthetic QX-314 on the membrane properties of hippocampal pyramidal neurons. J Pharmacol Exp Ther 220:476-481.
6. Cunningham MO, Pervouchine DD, Racca C, Kopell NJ, Davies CH, Jones RS, Traub RD, Whittington MA (2006) Neuronal metabolism governs cortical network response state. Proc Natl Acad SciU S A 103:5597-5601.
7. DeFelipe J (2002) Cortical interneurons: from Cajal to 2001. Prog Brain Res 136:215-238.
8. Destexhe A, Hughes SW, Rudolph M, Crunelli V (2007) Are corticothalamic "up" states fragments of wakefulness? Trends Neurosci 30:334-342.
9. Dzhala V, Valeeva G, Glykys J, Khazipov R, Staley K (2012) Traumatic al-terations in GABA signaling disrupt hippocampal network activity in the developing brain. J Neurosci 32:4017-4031.
10. 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.
11. Fanselow EE, Richardson KA, Connors BW (2008) Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100:2640-2652.
12. Fino E, Yuste R (2011) Dense inhibitory connectivity in neocortex. Neuron 69:1188-1203.
13. Galarreta M, Hestrin S (1999) A network of fast-spiking cells in the neocor-tex connected by electrical synapses. Nature 402:72-75.
14. 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.
15. Gentet LJ, Kremer Y, Taniguchi H, Huang ZJ, Staiger JF, Petersen CC (2012) Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci 15:607-612.
16. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
17. Gonchar Y, Wang Q, Burkhalter A (2007) Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immuno-staining. Front Neuroanat 1:3.
18. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N (2003) Agene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925.
19. Haider B, McCormick DA (2009) Rapid neocortical dynamics: cellular and network mechanisms. Neuron 62:171-189.
20. Haider B, Duque A, Hasenstaub AR, McCormick DA (2006) Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J Neurosci 26:4535-4545.
21. Hájos N, Ellender TJ, Zemankovics R, Mann EO, Exley R, Cragg SJ, Freund TF, Paulsen O (2009) Maintaining network activity in submerged hip-pocampal slices: importance of oxygen supply. Eur J Neurosci 29:319-327.
22. Halabisky B, Shen F, Huguenard JR, Prince DA (2006) Electrophysiological classification of somatostatin-positive interneurons in mouse sensorimo-tor cortex. J Neurophysiol 96:834-845.
23. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA (2005) Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 47:423-435.
24. Jones RS, Bühl EH (1993) Basket-like interneurones in layer II of the ento-rhinal cortex exhibit a powerful NMDA-mediated synaptic excitation. Neurosci Lett 149:35-39.
25. Jones RS, Heinemann U (1988) Synaptic and intrinsic responses of medical entorhinal cortical cells in normal and magnesium-free medium in vitro. J Neurophysiol 59:1476-1496.
26. Kapfer C, Glickfield LL, Atallah BV, Scanziani M (2007) Supralinear increase of recurrent inhibition during sparse activity inthe somatosensory cortex. Nat Neurosci 10:743-753.
27. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
28. Kawaguchi Y, Katsumaru H, Kosaka T, Heizmann CW, Hama K (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res 416:369-374.
29. Klausberger T, Magill PJ, Márton LF, Roberts JD, Cobden PM, Buzsáki G, Somogyi P (2003) Brain-state- and cell-type-specific firing of hip-pocampal interneurons in vivo. Nature 421:844-848.
30. Klink R, Alonso A (1997) Morphological characteristics of layer II projection neurons in the rat medial entorhinal cortex. Hippocampus 7:571-583.
31. Kubota Y, Shigematsu N, Karube F, Sekigawa A, Kato S, Yamaguchi N, Hirai Y, Morishima M, Kawaguchi Y (2011) Selective coexpression of multiple chemical markers defines discrete populations of neocortical GABAe-rgic neurons. Cereb Cortex 21:1803-1817.
32. Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B (2010) The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci 30:16796-16808.
33. Levy RB, Reyes AD (2012) Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex. J Neurosci 32:5609-5619.
34. Lopes da Silva FH, Witter MP, Boeijinga PH, Lohman AH (1990) Anatomic organization and physiology of the limbic cortex. Physiol Rev 70:453-511.
35. Mainen ZF, Sejnowski TJ (1995) Reliability of spike timing in neocortical neurons. Science 268:1503-1506.
36. Marin-Padilla M (1969) Origin of the pericellular baskets of the pyramidal cells of the human motor cortex: a Golgi study. Brain Res 14:633-646.
37. McCormick DA, Connors BW, Lighthall JW, Prince DA (1985) Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54:782-806.
38. McCormick DA, Shu Y, Hasenstaub A, Sanchez-Vives M, Badoual M, Bal T (2003) Persistent cortical activity: mechanisms of generation and effects on neuronal excitability. Cereb Cortex 13:1219-1231.
39. McGarry LM, Packer AM, Fino E, Nikolenko V, Sippy T, Yuste R (2010) Quantitative classification of somatostatin-positive neocortical interneu-rons identifies three interneuron subtypes. Front Neural Circuits 4:12.
40. Miettinen M, Koivisto E, Riekkinen P, Miettinen R (1996) Coexistence of parvalbumin and GABA in nonpyramidal neurons of the rat entorhinal cortex. Brain Res 706:113-122.
41. Nathan T, Jensen MS, Lambert JD (1990) The slow inhibitory postsynaptic potential in rat hippocampal CA1 neurones is blocked by intracellular injection of QX-314. Neurosci Lett 110:309-313.
42. 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.
43. Packer AM, Yuste R (2011) Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition? J Neurosci 31:13260-13271.
44. 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 USA 100:13638-13643.
45. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1:279-285.
46. Rudy B, Fishell G, Lee S, Hjerling-Leffler J (2011) Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 71:45-61.
47. Sanchez-Vives MV, McCormick DA (2000) Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat Neurosci 3:1027-1034.
48. Schwindt PC, Spain WJ, Foehring RC, Chubb MC, Crill WE (1988) Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J Neurophysiol 59:450-467.
49. Shadlen MN, Newsome WT (1994) Noise, neural codes and cortical organization. Curr Opin Neurobiol 4:569-579.
50. Shu Y, Hasenstaub A, McCormick DA (2003) Turning on and off recurrent balanced cortical activity. Nature 423:288-293.
51. Siddiq A, Miyazaki T, Takagishi Y, Kanou Y, Hayasaka S, Inouye M, Seo H, Murata Y (2001) Expression of ZAKI-4 messenger ribonucleic acid in the brain during rat development and the effect of hypothyroidism. Endocrinology 142:1752-1759.
52. Silberberg G, Markram H (2007) Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53:735-746.
53. 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.
54. Steriade M, Timofeev I, Grenier F (2001) Natural waking and sleep states: a view from inside neocortical neurons. J Neurophysiol 85:1969-1985.
55. Tahvildari B, Alonso A (2005) Morphological and electrophysiological properties of lateral entorhinal cortex layers II and III principal neurons. J Comp Neurol 491:123-140.
56. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Kvitsani D, Fu Y, Lu J, Lin Y, Miyoshi G, Shima Y, Fishell G, Nelson SB, Huang ZJ (2011) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71:995-1013.
57. Thomson AM, Lamy C (2007) Functional maps of neocortical local circuitry. Front Neurosci 1:19-42.
58. Traub RD, Whittington MA, Stanford IM, Jefferys JG (1996) A mechanism for generation of long-range synchronous fast oscillations in the cortex. Nature 383:621-624.
59. Tricoire L, Pelkey KA, Daw MI, Sousa VH, Miyoshi G, Jeffries B, Cauli B, Fishell G, McBain CJ (2010) Common origins of hippocampal Ivy and nitric oxide synthase expressing neurogliaform cells. J Neurosci 30:2165-2176.
60. Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y, Kawaguchi Y (2008) Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 18:315-330.
61. van den Pol AN, Yao Y, Fu LY, Foo K, Huang H, Coppari R, Lowell BB, Broberger C (2009) Neuromedin B and gastrin-releasing peptide excite arcuate nucleus neuropeptide Y neurons in a novel transgenic mouse expressing strong Renilla green fluorescent protein in NPY neurons. J Neurosci 29:4622-4639.
62. Wang XJ (2001) Synaptic reverberation underlying mnemonic persistent activity. Trends Neurosci 24:455-463.
63. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446.
64. Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahip-pocampal region. Prog Neurobiol 33:161-253.
65. Xu X, Roby KD, Callaway EM (2006) Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 499:144-160.
66. Xu X, Roby KD, Callaway EM (2010) Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 518:389-404.
67. Yu Y, Hill AP, McCormick DA (2012) Warm body temperature facilitates energy efficient cortical action potentials. PLoS Comput Biol 8:e1002456.
68. Zhang ET, Hansen AJ, Wieloch T, Lauritzen M (1990) Influence of MK-801 on brain extracellular calcium and potassium activities in severe hypogly-cemia. J Cereb Blood Flow Metab 10:136-139.