Skip to main content

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 volume 220, pages 3185–3209 (2015)Cite this article

Abstract

Excitatory layer 4 (L4) neurons in the ‘barrel field’ of the rat somatosensory cortex represent an important component in thalamocortical information processing. However, no detailed information exists concerning the quantitative geometry of synaptic boutons terminating on these neurons. Thus, L4 synaptic boutons were investigated using serial ultrathin sections and subsequent quantitative 3D reconstructions. In particular, parameters representing structural correlates of synaptic transmission and plasticity such as the number, size and distribution of pre- and postsynaptic densities forming the active zone (AZ) and of the three functionally defined pools of synaptic vesicles were analyzed. L4 synaptic boutons varied substantially in shape and size; the majority had a single, but large AZ with opposing pre- and postsynaptic densities that matched perfectly in size and position. More than a third of the examined boutons showed perforations of the postsynaptic density. Synaptic boutons contained on average a total pool of 561 ± 108 vesicles, with ~5 % constituting the putative readily releasable, ~23 % the recycling, and the remainder the reserve pool. These pools are comparably larger than other characterized central synapses. Synaptic complexes were surrounded by a dense network of fine astrocytic processes that reached as far as the synaptic cleft, thus regulating the temporal and spatial glutamate concentration, and thereby shaping the unitary EPSP amplitude. In summary, the geometry and size of AZs, the comparably large readily releasable and recycling pools, together with the tight astrocytic ensheathment, may explain and contribute to the high release probability, efficacy and modulation of synaptic transmission at excitatory L4 synaptic boutons. Moreover, the structural variability as indicated by the geometry of L4 synaptic boutons, the presence of mitochondria and the size and shape of the AZs strongly suggest that synaptic reliability, strength and plasticity is governed and modulated individually at excitatory L4 synaptic boutons.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

References

  • Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–246

    CAS  Article  PubMed  Google Scholar 

  • Agmon A, Connors BW (1991) Thalamocortical responses of mouse somatosensory (barrel) cortex in vitro. Neuroscience 41:365–379

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Barth AL (2002) Differential plasticity in neocortical networks. Physiol Behav 77:545–550

    CAS  Article  PubMed  Google Scholar 

  • Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90:2987–3000

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bruno RM, Sakmann B (2006) Cortex is driven by weak but synchronously active thalamocortical synapses. Science 312:1622–1627

    CAS  Article  PubMed  Google Scholar 

  • Constantinople CM, Bruno RM (2013) Deep cortical layers are activated directly by thalamus. Science 340:1591–1594

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Cragg BG (1972) The development of synapses in cat visual cortex. Invest Ophthalmol 11:377–385

    CAS  PubMed  Google Scholar 

  • Cragg BG (1975) The development of synapses in the visual system of the cat. J Comp Neurol 160:147–166

    CAS  Article  PubMed  Google Scholar 

  • Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105

    CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Freche D, Pannasch U, Rouach N, Holcman D (2011) Synapse geometry and receptor dynamics modulate synaptic strength. PLoS One 6:e25122

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Geinisman Y (1993) Perforated axospinous synapses with multiple, completely partitioned transmission zones: probable structural intermediates in synaptic plasticity. Hippocampus 3:417–433

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Gray EG (1959a) Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 93:420–433

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gray EG (1959b) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183:1592–1593

    CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Harris RM, Woolsey TA (1983) Computer-assisted analyses of barrel neuron axons and their putative synaptic contacts. J Comp Neurol 220:63–79

    CAS  Article  PubMed  Google Scholar 

  • Haydon PG, Carmignoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009–1031

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Land PW, Kandler K (2002) Somatotopic organization of rat thalamocortical slices. J Neurosci Methods 119:15–21

    Article  PubMed  Google Scholar 

  • Le Meur K, Mendizabal-Zubiaga J, Grandes P, Audinat E (2012) GABA release by hippocampal astrocytes. Front Comput Neurosci 6:1–10

    Google Scholar 

  • 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

    PubMed Central  Article  PubMed  Google Scholar 

  • Lübke J, Feldmeyer D (2007) Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex. Brain Struct Funct 212:3–17

    Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Min R, Nevian T (2012) Astrocyte signaling controls spike timing-dependent depression at neocortical synapses. Nat Neurosci 15:746–753

    CAS  Article  PubMed  Google Scholar 

  • Mironov SL (2006) Spontaneous and evoked neuronal activities regulate movements of single neuronal mitochondria. Synapse 59:403–411

    CAS  Article  PubMed  Google Scholar 

  • Mironov SL, Symonchuk N (2006) ER vesicles and mitochondria move and communicate at synapses. J Cell Sci 119:4926–4934

    CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Müller J, Reyes-Haro D, Pivneva T, Nolte C, Schaette R, Lübke J, Kettenmann H (2009) The principal neurons of the medial nucleus of the trapezoid body and NG2(+) glial cells receive coordinated excitatory synaptic input. J Gen Physiol 134:115–127

    PubMed Central  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Pozzan T, Magalhaes P, Rizzuto R (2000) The comeback of mitochondria to calcium signalling. Cell Calcium 28:279–283

    CAS  Article  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Rizzoli SO, Betz WJ (2004) The structural organization of the readily releasable pool of synaptic vesicles. Science 303:2037–2039

    CAS  Article  PubMed  Google Scholar 

  • Rizzoli SO, Betz WJ (2005) Synaptic vesicle pools. Nat Rev Neurosci 6:57–69

    CAS  Article  PubMed  Google Scholar 

  • Rizzuto R, Bernardi P, Pozzan T (2000) Mitochondria as all-round players of the calcium game. J Physiol 529:37–47

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  Article  PubMed  Google Scholar 

  • Rollenhagen A, Lübke JHR (2006) The morphology of excitatory central synapses: from structure to function. Cell Tissue Res 326:221–237

    Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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)

  • Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197–1207

    CAS  Article  PubMed  Google Scholar 

  • Rowland KC, Irby NK, Spirou GA (2000) Specialized synapse-associated structures within the calyx of Held. J Neurosci 20:9135–9144

    CAS  PubMed  Google Scholar 

  • Sahara Y, Takahashi T (2001) Quantal components of the excitatory postsynaptic currents at a rat central auditory synapse. J Physiol 536:189–197

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Saviane C, Silver RA (2006) Fast vesicle reloading and a large pool sustain high bandwidth transmission at a central synapse. Nature 439:983–987

    CAS  Article  PubMed  Google Scholar 

  • Schikorski T, Stevens CF (2001) Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391–395

    CAS  Article  PubMed  Google Scholar 

  • Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206–212

    CAS  Article  PubMed  Google Scholar 

  • Schoch S, Gundelfinger ED (2006) Molecular organization of the presynaptic active zone. Cell Tissue Res 326:379–391

    CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Sherman SM, Guillery RW (1996) Functional organization of thalamocortical relays. J Neurophysiol 76:1367–1395

    CAS  PubMed  Google Scholar 

  • Silver RA, Lübke J, Sakmann B, Feldmeyer D (2003) High-probability uniquantal transmission at excitatory synapses in barrel cortex. Science 302:1981–1984

    CAS  Article  PubMed  Google Scholar 

  • Simons DJ, Woolsey TA (1984) Morphology of Golgi-Cox-impregnated barrel neurons in rat SmI cortex. J Comp Neurol 230:119–132

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Südhof TC (2012) The presynaptic active zone. Neuron 75:11–25

    PubMed Central  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • von Gersdorff H, Borst JG (2002) Short-term plasticity at the calyx of held. Nat Rev Neurosci 3:53–64

    Article  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  Article  PubMed  Google Scholar 

  • Xu-Friedman MA, Regehr WG (2003) Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses. J Neurosci 23:2182–2192

    CAS  PubMed  Google Scholar 

  • Xu-Friedman MA, Regehr WG (2004) Structural contributions to short-term synaptic plasticity. Physiol Rev 84:69–85

    CAS  Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Yu C, Derdikman D, Haidarliu S, Ahissar E (2006) Parallel thalamic pathways for whisking and touch signals in the rat. PLoS Biol 4:e124

    PubMed Central  Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The excellent technical assistance by Eva Nicksch, Brigitte Marshallsay and Ulrike Bandelow is very much appreciated. We would like to thank Dr. Nicola Palomero-Gallagher for critically reading and helpful comments on a pre-final version of the manuscript. This work was supported by the IRTG 1328 (K.K.) and grants of the Deutsche Forschungsgemeinschaft DFG (J.L.). The authors declare no competing financial interests.

Author information

Affiliations

  1. Institute of Neuroscience and Medicine INM-2, Research Centre Jülich GmbH, Leo-Brandt Str., 52425, Jülich, Germany

    Astrid Rollenhagen, Kerstin Klook, Guanxiao Qi, Max Anstötz, Dirk Feldmeyer & Joachim H. R. Lübke

  2. IRTG Graduate School 1328, RWTH/University Hospital, Aachen, Germany

    Kerstin Klook

  3. School of Biomedical Sciences, University of Ulster, Cromore Rd., Londonderry, BT52 1SA, UK

    Kurt Sätzler

  4. Department of Psychiatry, Psychotherapy and Psychosomatics, Medical Faculty, RWTH/University Hospital, Pauwelstr. 30, 52074, Aachen, Germany

    Dirk Feldmeyer & Joachim H. R. Lübke

  5. JARA Translational Brain Medicine, Jülich/Aachen, Germany

    Dirk Feldmeyer & Joachim H. R. Lübke

Authors
  1. Astrid Rollenhagen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kerstin Klook
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kurt Sätzler
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guanxiao Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Max Anstötz
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dirk Feldmeyer
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Joachim H. R. Lübke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joachim H. R. Lübke.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rollenhagen, A., Klook, K., Sätzler, K. et al. Structural determinants underlying the high efficacy of synaptic transmission and plasticity at synaptic boutons in layer 4 of the adult rat ‘barrel cortex’. Brain Struct Funct 220, 3185–3209 (2015). https://doi.org/10.1007/s00429-014-0850-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-014-0850-5

Keywords

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