Structural determinants underlying the high efficacy of synaptic transmission and plasticity at synaptic boutons in layer 4 of the adult rat ‘barrel cortex’

Brain Structure and Function

Volumn 220, Issue 6, 2015, Pages 3185-3209

  Rollenhagen, Astrid ^a   Klook, Kerstin ^a,b   Sätzler, Kurt ^c   Qi, Guanxiao ^a   Anstötz, Max ^a   Feldmeyer, Dirk ^a,b,d   Lübke, Joachim H R ^a,b,d  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^c UNIVERSITY OF ULSTER   (United Kingdom)

^d JARA TRANSLATIONAL BRAIN MEDICINE   (Germany)

Author keywords

Barrel cortex; Distinct pools of synaptic vesicles; Layer 4 synaptic boutons; Quantitative 3D reconstructions; Synaptic transmission and plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; ETHINYLESTRADIOL PLUS MEGESTROL ACETATE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONCENTRATION PROCESS; CONTROLLED STUDY; EXCITATORY LAYER 4 NEURON; EXCITATORY POSTSYNAPTIC POTENTIAL; GEOMETRY; IMAGE RECONSTRUCTION; INFORMATION PROCESSING; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; SOMATOSENSORY CORTEX; STRUCTURE ANALYSIS; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC EFFICACY; SYNAPTIC TRANSMISSION; THREE DIMENSIONAL IMAGING; YOUNG ADULT; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN CORTEX; IMAGE PROCESSING; NERVE ENDING; PHYSIOLOGY; PROCEDURES; STRUCTURE ACTIVITY RELATION; ULTRASTRUCTURE; WISTAR RAT;

ANIMALS; CEREBRAL CORTEX; EXCITATORY POSTSYNAPTIC POTENTIALS; IMAGE PROCESSING, COMPUTER-ASSISTED; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 84942373873     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0850-5     Document Type: Article

References (98)

1. Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–246
2. Agmon A, Connors BW (1991) Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41:365–379
3. Ahmed B, Anderson JC, Douglas RJ, Martin KA, Nelson JC (1994) Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J Comp Neurol 341:39–49
4. Ahmed B, Anderson JC, Martin KA, Nelson JC (1997) Map of the synapses onto layer 4 basket cells of the primary visual cortex of the cat. J Comp Neurol 380:230–242
5. Armstrong-James M, Fox K, Das-Gupta A (1992) Flow of excitation within rat barrel cortex on striking a single vibrissa. J Neurophysiol 68:1345–1358
6. Barth AL (2002) Differential plasticity in neocortical networks. Physiol Behav 77:545–550
7. Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90:2987–3000
8. Benshalom G, White E (1986) Quantification of thalamocortical synapses with spiny stellate neurons in layer IV of mouse somatosensory cortex. J Comp Neurol 253:303–314
9. Brückner G, Brauer K, Hartig W, Wolff JR, Rickmann MJ, Derouiche A, Delpech B, Girard N, Oertel WH, Reichenbach A (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8:183–200
10. Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622–1627
11. Constantinople CM, Bruno RM (2013) Deep cortical layers are activated directly by thalamus. Science 340:1591–1594
12. Cragg BG (1972) The development of synapses in cat visual cortex. Invest Ophthalmol 11:377–385
13. Cragg BG (1975) The development of synapses in the visual system of the cat. J Comp Neurol 160:147–166
14. Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105
15. Deller T, Korte M, Chabanis S, Drakew A, Schwegler H, Stefani GG, Zuniga A, Schwarz K, Bonhoeffer T, Zeller R, Frotscher M, Mundel P (2003) Synaptopodin-deficient mice lack a spine apparatus and show deficits in synaptic plasticity. Proc Natl Acad Sci USA 100:10494–10499
16. Egger V, Feldmeyer D, Sakmann B (1999) Coincidence detection and changes of synaptic efficacy in spiny stellate neurons in rat barrel cortex. Nat Neurosci 2:1098–1105
17. Feldmeyer D, Egger V, Lübke J, Sakmann B (1999) Reliable synaptic connections between pairs of excitatory layer 4 neurons within a single ‘barrel’ of developing rat somatosensory cortex. J Physiol 521:169–190
18. Feldmeyer D, Lübke J, Silver RA, Sakmann B (2002) Synaptic connections between layer 4 spiny neuron-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J Physiol 538:803–822
19. Feldmeyer D, Roth A, Sakmann B (2005) Monosynaptic connections between pairs of spiny stellate cells in layer 4 and pyramidal cells in layer 5A indicate that lemniscal and paralemniscal afferent pathways converge in the infragranular somatosensory cortex. J Neurosci 25:3423–3431
20. Feldmeyer D, Brecht M, Helmchen F, Petersen CC, Poulet JF, Staiger JF, Luhmann HJ, Schwarz C (2013) Barrel cortex function. Prog Neurobiol 103:3–27
21. Freche D, Pannasch U, Rouach N, Holcman D (2011) Synapse geometry and receptor dynamics modulate synaptic strength. PLoS One 6:e25122
22. Geinisman Y (1993) Perforated axospinous synapses with multiple, completely partitioned transmission zones: probable structural intermediates in synaptic plasticity. Hippocampus 3:417–433
23. Geinisman Y, de Toledo-Morrell L, Morrell F (1991) Induction of long-term potentiation is associated with an increase in the number of axospinous synapses with segmented postsynaptic densities. Brain Res 566:77–88
24. Gray EG (1959a) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 93:420–433
25. Gray EG (1959b) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183:1592–1593
26. Hallermann S, Pawlu C, Jonas P, Heckmann M (2003) A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc Natl Acad Sci USA 100:8975–8980
27. Harris RM, Woolsey TA (1983) Computer-assisted analyses of barrel neuron axons and their putative synaptic contacts. J Comp Neurol 220:63–79
28. Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009–1031
29. Helmstaedter M, Staiger JF, Sakmann B, Feldmeyer D (2008) Efficient recruitment of layer 2/3 interneurons by layer 4 input in single columns of rat somatosensory cortex. J Neurosci 28:8273–8284
30. Helmstaedter M, Sakmann B, Feldmeyer D (2009) The relation between dendritic geometry, electrical excitability, and axonal projections of L2/3 interneurons in rat barrel cortex. Cereb Cortex 19:938–950
31. Holderith N, Lorincz A, Katona G, Rozsa B, Kulik A, Watanabe M, Nusser Z (2012) Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat Neurosci 15:988–997
32. Holtmaat AJ, Trachtenberg JT, Wilbrecht L, Shepherd GM, Zhang X, Knott GW, Svoboda K (2005) Transient and persistent dendritic spines in the neocortex in vivo. Neuron 45:279–291
33. Houades V, Koulakoff A, Ezan P, Seif I, Giaume C (2008) Gap junction-mediated astrocytic networks in the mouse barrel cortex. J Neurosci 28:5207–5217
34. Jacobs SE, Juliano SL (1995) The impact of basal forebrain lesions on the ability of rats to perform a sensory discrimination task involving barrel cortex. J Neurosci 15:1099–1109
35. Kätzel D, Zemelman BV, Buetfering C, Wolfel M, Miesenbock G (2011) The columnar and laminar organization of inhibitory connections to neocortical excitatory cells. Nat Neurosci 14:100–107
36. Koelbl C, Helmstaedter M, Lübke J, Feldmeyer D (2013) A barrel-related interneuron in layer 4 of rat somatosensory cortex with a high intrabarrel connectivity. Cereb Cortex. doi:10.1093/cercor/bht263
37. Konur S, Yuste R (2004) Imaging the motility of dendritic protrusions and axon terminals: roles in axon sampling and synaptic competition. Mol Cell Neurosci 27:427–440
38. Kumar P, Ohana O (2008) Inter- and intralaminar subcircuits of excitatory and inhibitory neurons in layer 6a of the rat barrel cortex. J Neurophysiol 100:1909–1922
39. Land PW, Kandler K (2002) Somatotopic organization of rat thalamocortical slices. J Neurosci Methods 119:15–21
40. Le Meur K, Mendizabal-Zubiaga J, Grandes P, Audinat E (2012) GABA release by hippocampal astrocytes. Front Comput Neurosci 6:1–10
41. Lee CC, Sherman SM (2008) Synaptic properties of thalamic and intracortical inputs to layer 4 of the first- and higher-order cortical areas in the auditory and somatosensory systems. J Neurophysiol 100:317–326
42. Lübke J, Feldmeyer D (2007) Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct Funct 212:3–17
43. 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
44. Lübke J, Roth A, Feldmeyer D, Sakmann B (2003) Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb Cortex 13:1051–1063
45. Matz J, Gilyan A, Kolar A, McCarvill T, Krueger SR (2010) Rapid structural alterations of the active zone lead to sustained changes in neurotransmitter release. Proc Natl Acad Sci USA 107:8836–8841
46. Meyer HS, Wimmer VC, Hemberger M, Bruno RM, de Kock CP, Frick A, Sakmann B, Helmstaedter M (2010) Cell type-specific thalamic innervation in a column of rat vibrissal cortex. Cereb Cortex 20:2287–2303
47. Meyer HS, Schwarz D, Wimmer VC, Schmitt AC, Kerr JN, Sakmann B, Helmstaedter M (2011) Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A. Proc Natl Acad Sci USA 108:16807–16812
48. Min R, Nevian T (2012) Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat Neurosci 15:746–753
49. Mironov SL (2006) Spontaneous and evoked neuronal activities regulate movements of single neuronal mitochondria. Synapse 59:403–411
50. Mironov SL, Symonchuk N (2006) ER vesicles and mitochondria move and communicate at synapses. J Cell Sci 119:4926–4934
51. Mukherjee K, Yang X, Gerber SH, Kwon HB, Ho A, Castillo PE, Liu X, Südhof TC (2010) Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proc Natl Acad Sci USA 107:6504–6509
52. (+) glial cells receive coordinated excitatory synaptic input. J Gen Physiol 134:115–127
53. Nicol MJ, Walmsley B (2002) Ultrastructural basis of synaptic transmission between endbulbs of Held and bushy cells in the rat cochlear nucleus. J Physiol 539:713–723
54. Nicoletta N, Fenghua C, Gregers W, Maurizio P, Randel NJ (2013) A new efficient method for synaptic vesicle quantification reveals differences between medial prefrontal cortex perforated and non-perforated synapses. J Comp Neurol. doi:10.1002/cne.23482
55. Oliet SH, Piet R, Poulain DA, Theodosis DT (2004) Glial modulation of synaptic transmission: insights from the supraoptic nucleus of the hypothalamus. Glia 47:258–267
56. Pannasch U, Freche D, Dallérac G, Ghézali G, Escartin C, Ezan P, Cohen-Salmon M, Benchenane K, Abudara V, Dufour A, Lübke JHR, Déglon N, Knott G, Holcman D, Rouach N (2014) Connexin 30 sets synaptic strength by controlling astroglial synapse invasion. Nat Neurosci 17:549–558
57. Peters A, Kaiserman-Abramof IR (1969) The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Z Zellforsch Mikrosk Anat 100:487–506
58. Pozzan T, Magalhaes P, Rizzuto R (2000) The comeback of mitochondria to calcium signalling. Cell Calcium 28:279–283
59. Radnikow G, Günter RH, Günter RH, Marx M, Feldmeyer D (2012) Morphofunctional mapping of cortical networks in brain slice preparations using paired electrophysiological recordings. In: Fellin T, Halassa M (eds) Neuromethods: neuronal network analysis. Humana Press, Springer Science and Business Media, LLC 2011, New York, pp 405–431
60. Ramirez A, Pnevmatikakis EA, Merel J, Paninski L, Miller KD, Bruno RM (2014) Spatiotemporal receptive fields of barrel cortex revealed by reverse correlation of synaptic input. Nat Neurosci 17:866–875
61. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
62. Rizzoli SO, Betz WJ (2004) The structural organization of the readily releasable pool of synaptic vesicles. Science 303:2037–2039
63. Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6:57–69
64. Rizzuto R, Bernardi P, Pozzan T (2000) Mitochondria as all-round players of the calcium game. J Physiol 529:37–47
65. Rodríguez-Contreras A, van Hoeve JS, Habets RL, Locher H, Borst JG (2008) Dynamic development of the calyx of Held synapse. Proc Natl Acad Sci USA 105:5603–5608
66. Rollenhagen A, Lübke JHR (2006) The morphology of excitatory central synapses: from structure to function. Cell Tissue Res 326:221–237
67. Rollenhagen A, Sätzler K, Rodriguez EP, Jonas P, Frotscher M, Lübke JHR (2007) Structural determinants of transmission at large hippocampal mossy fiber synapses. J Neurosci 27:10434–10444
68. Rollenhagen A, Klook K, Suchmann C, Kasugai Y, Ferraguti F, Shigemoto R, Lübke JHR (2012) Differential expression and distribution patterns of AMPA and NMDA receptors and their subunits at layer 4 and layer 5 synapses in the rat somatosensory cortex. Soc Neurosci Abstr, 43.12 (online)
69. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197–1207
70. Rowland KC, Irby NK, Spirou GA (2000) Specialized synapse-associated structures within the calyx of Held. J Neurosci 20:9135–9144
71. Sahara Y, Takahashi T (2001) Quantal components of the excitatory postsynaptic currents at a rat central auditory synapse. J Physiol 536:189–197
72. Sätzler K, Söhl LF, Bollmann JH, Borst JG, Frotscher M, Sakmann B, Lübke JHR (2002) Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J Neurosci 22:10567–10579
73. Saviane C, Silver RA (2006) Fast vesicle reloading and a large pool sustain high bandwidth transmission at a central synapse. Nature 439:983–987
74. Schikorski T, Stevens CF (2001) Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391–395
75. Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206–212
76. Schoch S, Gundelfinger ED (2006) Molecular organization of the presynaptic active zone. Cell Tissue Res 326:379–391
77. Schoonover CE, Tapia JC, Schilling VC, Wimmer V, Blazeski R, Zhang W, Mason CA, Bruno RM (2014) Comparative strength and dendritic organization of thalamocortical and corticocortical synapses onto excitatory layer 4 neurons. J Neurosci 34:6746–6758
78. Shapira M, Zhai RG, Dresbach T, Bresler T, Torres VI, Gundelfinger ED, Ziv NE, Garner CC (2003) Unitary assembly of presynaptic active zones from Piccolo-Bassoon transport vesicles. Neuron 38:237–252
79. Sherman SM, Guillery RW (1996) Functional organization of thalamocortical relays. J Neurophysiol 76:1367–1395
80. Silver RA, Lübke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981–1984
81. Simons DJ, Woolsey TA (1984) Morphology of Golgi-Cox-impregnated barrel neurons in rat SmI cortex. J Comp Neurol 230:119–132
82. Somogyi P, Hodgson AJ (1985) Antisera to gamma-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33:249–257
83. Staiger JF, Flagmeyer I, Schubert D, Zilles K, Kötter R, Luhmann HJ (2004) Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. Cereb Cortex 14:690–701
84. Staiger JF, Zuschratter W, Luhmann HJ, Schubert D (2009) Local circuits targeting parvalbumin-containing interneurons in layer IV of rat barrel cortex. Brain Struct Funct 214:1–13
85. Südhof TC (2012) The presynaptic active zone. Neuron 75:11–25
86. Umeda T, Ebihara T, Okabe S (2005) Simultaneous observation of stably associated presynaptic varicosities and postsynaptic spines: morphological alterations of CA3–CA1 synapses in hippocampal slice cultures. Mol Cell Neurosci 28:264–274
87. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, Bellen HJ (2005) Synaptic mitochondria are critical for mobilization of reserve pool vesicles at Drosophila neuromuscular junctions. Neuron 47:365–378
88. von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of held. Nat Rev Neurosci 3:53–64
89. Wanaverbecq N, Bodor AL, Bokor H, Slezia A, Luthi A, Acsady L (2008) Contrasting the functional properties of GABAergic axon terminals with single and multiple synapses in the thalamus. J Neurosci 28:11848–11861
90. Watanabe S, Rost BR, Camacho-Perez M, Davis MW, Sohl-Kielczynski B, Rosenmund C, Jorgensen EM (2013) Ultrafast endocytosis at mouse hippocampal synapses. Nature 504:242–247
91. White EL, Benshalom G, Hersch SM (1984) Thalamocortical and other synapses involving nonspiny multipolar cells of mouse SmI cortex. J Comp Neurol 229:311–320
92. Xu-Friedman MA, Regehr WG (2003) Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses. J Neurosci 23:2182–2192
93. Xu-Friedman MA, Regehr WG (2004) Structural contributions to short-term synaptic plasticity. Physiol Rev 84:69–85
94. Xu-Friedman MA, Harris KM, Regehr WG (2001) Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells. J Neurosci 21:6666–6672
95. Yu C, Derdikman D, Haidarliu S, Ahissar E (2006) Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol 4:e124
96. Zhang ZW, Deschenes M (1997) Intracortical axonal projections of lamina VI cells of the primary somatosensory cortex in the rat: a single-cell labeling study. J Neurosci 17:6365–6379
97. Zhao S, Studer D, Graber W, Nestel S, Frotscher M (2012a) Fine structure of hippocampal mossy fiber synapses following rapid high-pressure freezing. Epilepsia 53(Suppl. 1):4–8
98. Zhao S, Studer D, Chai X, Graber W, Brose N, Nestel S, Young C, Rodriguez EP, Sätzler K, Frotscher M (2012b) Structural plasticity of hippocampal mossy fiber synapses as revealed by high-pressure freezing. J Comp Neurol 520:2340–2351