Spatial profile of excitatory and inhibitory synaptic connectivity in mouse primary auditory cortex

Journal of Neuroscience

Volumn 32, Issue 16, 2012, Pages 5609-5619

  Levy, Robert B ^a   Reyes, Alex D ^a  

^a NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; INTRACELLULAR RECORDING; MALE; MORPHOMETRICS; MOUSE; NERVE CELL INHIBITION; NERVE CELL MEMBRANE POTENTIAL; NERVE CELL NETWORK; NERVE CELL STIMULATION; NONHUMAN; PRIMARY AUDITORY CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SPIKE; SYNAPSE; THALAMOCORTICAL TRACT; THEORETICAL MODEL;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; AUDITORY CORTEX; AUDITORY PATHWAYS; AXONS; BIOPHYSICS; BRAIN MAPPING; DENDRITES; ELECTRIC STIMULATION; GLUTAMATE DECARBOXYLASE; GREEN FLUORESCENT PROTEINS; INHIBITORY POSTSYNAPTIC POTENTIALS; MICE; MICE, TRANSGENIC; NERVE NET; NEURAL INHIBITION; NEURONS; NORMAL DISTRIBUTION; PATCH-CLAMP TECHNIQUES; SYNAPSES; THALAMUS;

EID: 84859768155     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/jneurosci.5158-11.2012     Document Type: Article

References (80)

1. Bandyopadhyay S, Shamma SA, Kanold PO (2010) Dichotomy of functional organization in the mouse auditory cortex. Nat Neurosci 13:361-368.
2. Barbour B, Isope P (2000) Combining loose cell-attached stimulation and recording. J Neurosci Methods 103:199-208.
3. Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90:2987-3000.
4. Blasdel GG, Lund JS (1983) Termination of afferent axons in macaque striate cortex. J Neurosci 3:1389-1413.
5. Brown SP, Hestrin S (2009) Intracortical circuits of pyramidal neurons reflect their long-range axonal targets. Nature 457:1133-1136.
6. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611.
7. Colonnier M (1964) The tangential organization of the visual cortex. J Anat 98:327-344.
8. Cruikshank SJ, Rose HJ, Metherate R (2002) Auditory thalamocortical synaptic transmission in vitro. J Neurophysiol 87:361-384.
9. de la Rocha J, Marchetti C, Schiff M, Reyes AD (2008) Linking the response properties of cells in auditory cortex with network architecture: co-tuning versus lateral inhibition. J Neurosci 28:9151-9163.
10. Dorrn AL, Yuan K, Barker AJ, Schreiner CE, Froemke RC (2010) Developmental sensory experience balances cortical excitation and inhibition. Nature 465:932-936.
11. Douglas RJ, Koch C, Mahowald M, Martin KA, Suarez HH (1995) Recurrent excitation in neocortical circuits. Science 269:981-985.
12. Ehret G (1976) Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc 1:179-184.
13. 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.
14. Fanselow EE, Richardson KA, Connors BW (2008) Selective, statedependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 100:2640-2652.
15. Fino E, Yuste R (2011) Dense inhibitory connectivity in neocortex. Neuron 69:1188-1203.
16. Goldberg JH, Lacefield CO, Yuste R (2004) Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting. J Physiol 558:465-478.
17. Gupta A, Wang Y, Markram H (2000) Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287:273-278.
18. Hackett TA, Barkat TR, O'Brien BM, Hensch TK, Polley DB (2011) Linking topography to tonotopy in the mouse auditory thalamocortical circuit. J Neurosci 31:2983-2995.
19. Halasy K, Buhl EH, Lörinczi Z, Tamás G, Somogyi P (1996) Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus. Hippocampus 6:306-329.
20. Hellwig B (2000) A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex. Biol Cybern 82:111-121.
21. Holmgren C, Harkany T, Svennenfors B, Zilberter Y (2003) Pyramidal cell communication within local networks in layer 2/3 of rat neocortex. J Physiol 551:139-153.
22. Hromádka T, Deweese MR, Zador AM (2008) Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol 6: e16.
23. Huang CL, Winer JA (2000) Auditory thalamocortical projections in the cat: laminar and areal patterns of input. J Comp Neurol 427:302-331.
24. Hubel DH, Wiesel TN (1977) Ferrier lecture. Functional architecture of macaque monkey visual cortex. Proc R Soc Lond B Biol Sci 198:1-59.
25. Jensen KF, Killackey HP (1987) Terminal arbors of axons projecting to the somatosensory cortex of the adult rat. I. The normal morphology of specific thalamocortical afferents. J Neurosci 7:3529-3543.
26. Kalisman N, Silberberg G, Markram H (2003) Deriving physical connectivity from neuronal morphology. Biological Cybernetics 88:210-218.
27. Kalisman N, Silberberg G, Markram H (2005) The neocortical microcircuit as a tabula rasa. Proc Natl Acad Sci U S A 102:880-885.
28. Kawaguchi Y, Kubota Y (1993) Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin-and calbindinD28kimmunoreactive neurons in layer V of rat frontal cortex. J Neurophysiol 70:387-396.
29. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486.
30. Kirov SA, Sorra KE, Harris KM (1999) Slices have more synapses than perfusion-fixed hippocampus from both young and mature rats. J Neurosci 19:2876-2886.
31. LeVay S (1986) Synaptic organization of claustral and geniculate afferents to the visual cortex of the cat. J Neurosci 6:3564-3575.
32. Levy RB, Reyes AD (2011) Coexistence of lateral and co-tuned inhibitory configurations in cortical networks. PLoS Comput Biol 7:e1002161.
33. Lübke J, Egger V, Sakmann B, Feldmeyer D (2000) Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J Neurosci 20:5300-5311.
34. Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A (2006) Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 26:5069-5082.
35. 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.
36. Markram H, Lübke J, Frotscher M, Roth A, Sakmann B (1997) Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol 500:409-440.
37. 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.
38. McGarry LM, Packer AM, Fino E, Nikolenko V, Sippy T, Yuste R (2010) Quantitative classification of somatostatin-positive neocortical interneurons identifies three interneuron subtypes. Front Neural Circuits 4:12.
39. Metherate R, Aramakis VB (1999) Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. Brain Res Dev Brain Res 115:131-144.
40. Müller-Preuss P, Mitzdorf U (1984) Functional anatomy of the inferior colliculus and the auditory cortex: current source density analyses of clickevoked potentials. Hear Res 16:133-142.
41. Nikolenko V, Fino E, Yuste R (2011) Two-photon mapping of neural circuits. Cold Spring Harb Protoc. doi:10.1101/pdb.top11.
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. Oswald AM, Reyes AD (2008) Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. J Neurophysiol 99:2998-3008.
44. Oswald AM, Reyes AD (2011) Development of inhibitory timescales in auditory cortex. Cereb Cortex 21:1351-1361.
45. Oswald AM, Schiff ML, Reyes AD (2006) Synaptic mechanisms underlying auditory processing. Curr Opin Neurobiol 16:371-376.
46. Oswald AM, Doiron B, Rinzel J, Reyes AD (2009) Spatial profile and differential recruitment of GABAB modulate oscillatory activity in auditory cortex. J Neurosci 29:10321-10334.
47. Otsuka T, Kawaguchi Y (2009) Cortical inhibitory cell types differentially form intralaminar and interlaminar subnetworks with excitatory neurons. J Neurosci 29:10533-10540.
48. Packer AM, Yuste R (2011) Dense, unspecific connectivity of neocortical parvalbumin-positive interneurons: a canonical microcircuit for inhibition? J Neurosci 31:13260-13271.
49. Perin R, Berger TK, Markram H (2011) A synaptic organizing principle for cortical neuronal groups. Proc Natl Acad Sci U S A 108:5419-5424.
50. Peters A, Payne BR (1993) Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex 3:69-78.
51. Peters A, Payne BR, Budd J (1994) A numerical analysis of the geniculocortical input to striate cortex in the monkey. Cereb Cortex 4:215-229.
52. Petersen CC (2007) The functional organization of the barrel cortex. Neuron 56:339-355.
53. Petersen CC, Sakmann B (2000) The excitatory neuronal network of rat layer 4 barrel cortex. J Neurosci 20:7579-7586.
54. Petersen CC, Sakmann B (2001) Functionally independent columns of rat somatosensory barrel cortex revealed with voltage-sensitive dye imaging. J Neurosci 21:8435-8446.
55. 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.
56. Rose HJ, Metherate R (2005) Auditory thalamocortical transmission is reliable and temporally precise. J Neurophysiol 94:2019-2030.
57. 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.
58. Sally SL, Kelly JB (1988) Organization of auditory cortex in the albino rat: sound frequency. J Neurophysiol 59:1627-1638.
59. Schreiner CE, Read HL, Sutter ML (2000) Modular organization of frequency integration in primary auditory cortex. Annu Rev Neurosci 23:501-529.
60. Shapley R, Hawken M, Xing D (2007) The dynamics of visual responses in the primary visual cortex. Prog Brain Res 165:21-32.
61. Shepherd GM, Stepanyants A, Bureau I, Chklovskii D, Svoboda K (2005) Geometric and functional organization of cortical circuits. Nat Neurosci 8:782-790.
62. Sompolinsky H, Shapley R (1997) New perspectives on the mechanisms for orientation selectivity. Curr Opin Neurobiol 7:514-522.
63. Song L, McGee J, Walsh EJ (2006) Frequency-and level-dependent changes in auditory brainstem responses (ABRS) in developing mice. J Acoust Soc Am 119:2242-2257.
64. Stepanyants A, Chklovskii DB (2005) Neurogeometry and potential synaptic connectivity. Trends Neurosci 28:387-394.
65. Stepanyants A, Martinez LM, Ferecskó AS, Kisvárday ZF (2009) The fractions of short-and long-range connections in the visual cortex. Proc Natl Acad Sci U S A 106:3555-3560.
66. Stuart GJ, Dodt HU, Sakmann B (1993) Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Pflügers Arch 423:511-518.
67. Suga N, Simmons JA, Jen PH (1975) Peripheral specialization for fine analysis of doppler-shifted echoes in the auditory system of the "CF-FM" bat Pteronotus parnellii. J Exp Biol 63:161-192.
68. Suga N, Zhang Y, Yan J (1997) Sharpening of frequency tuning by inhibition in the thalamic auditory nucleus of the mustached bat. J Neurophysiol 77:2098-2114.
69. Sun YJ, Wu GK, Liu BH, Li P, Zhou M, Xiao Z, Tao HW, Zhang LI (2010) Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development. Nature 465:927-931.
70. Takesian AE, Kotak VC, Sanes DH (2010) Presynaptic GABA(B) receptors regulate experience-dependent development of inhibitory short-term plasticity. J Neurosci 30:2716-2727.
71. Thomson AM, Deuchars J, West DC (1993) Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation. Neuroscience 54:347-360.
72. Thomson AM, West DC, Deuchars J (1995) Properties of single axon excitatory postsynaptic potentials elicited in spiny interneurons by action potentials in pyramidal neurons in slices of rat neocortex. Neuroscience 69:727-738.
73. Wang Y, Toledo-Rodriguez M, Gupta A, Wu C, Silberberg G, Luo J, Markram H (2004) Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol 561:65-90.
74. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446.
75. White EL (1989) Cortical circuits. Boston: Birkhäuser.
76. Williams SM, Goldman-Rakic PS, Leranth C (1992) The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. J Comp Neurol 320:353-369.
77. Wong WC (1967) The tangential organization of dendrites and axons in three auditory areas of the cat's cerebral cortex. J Anat 101:419-433.
78. Wu GK, Arbuckle R, Liu BH, Tao HW, Zhang LI (2008) Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 58:132-143.
79. Xiang Z, Huguenard JR, Prince DA (1998) Cholinergic switching within neocortical inhibitory networks. Science 281:985-988.
80. Young ED, Brownell WE (1976) Responses to tones and noise of single cells in dorsal cochlear nucleus of unanesthetized cats. J Neurophysiol 39:282-300.