GRK 1123:  Cellular Mechanisms of Learning and Memory Consolidation in the Hippocampal Formation

• Subject Area: Neurosciences
• Term: from 2005 to 2014
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 462239

• Final Report Year: 2015

Final Report Abstract

Our research training group (RTG) combined innovative approaches in an interdisciplinary fashion to investigate neuronal plasticity as a factor in mechanisms of learning and memory in the hippocampal formation. The hippocampus has long been known to play a key role in the formation of several forms of memory, including episodic and spatial memory. In rodents, hippocampal pyramidal neurons selectively discharge when the animal is in a specific location in space: these neurons are referred to as 'place cells'. Intriguingly, place cells sequentially activated during exploration of space by rodents are subsequently reactivated in the same order during sleep, as if the animal were virtually ‘dreaming’ of the same trajectories. Thus, during exploration a neural assembly is formed which can be reactivated for decision-making and for memory consolidation. This 'replay' occurs during 200 Hz network oscillations known as ‘sharp wave ripples’. The latter, markedly fast timescale is consistent with time windows optimal for induction of long-term potentiation (LTP), the principal candidate as the molecular mechanism of synaptic plasticity underlying memory. Consequently, most studies have focused on synaptic plasticity in the hippocampus, in particular: 1) regulation of transmitter release; 2) mechanisms underlying memory formation and consolidation; 3) homeostatic and heterosynaptic plasticity (and the disturbance of the latter) as a factor in diseases such as temporal lobe epilepsy and Alzheimer’s disease. From the work of the members of the GRK1123 more than 100 papers appeared, many of them in high impact factor journals such as Science, Neuron, and PNAS. A total of 56 funded and associated students were supported by the GRK1123. Approximately 28 students contributed to the success of the second funding period. Many of the GRK1123-funded students found excellent postdoctoral positions in outstanding research groups based at institutions such as Janelia Farm and Cambridge University. The experience of the tutors in the GRK1123 and parallel initiatives led to a successful bid for an Einstein Center, which will be officially publicized in late October 2015. The center will extend the achievements of GRK 1123 by focusing on improved infrastructure for an even more advanced educational platform aimed at a new generation of neuroscientists.

Publications

• (2007) Synaptic plasticity in the temporal lobe and its alterations in a model of MK-801-induced acute schizophreniform psychosis. FU Berlin
  Wöhrl, R.
  
• (2008) Aggregation, structure and pathological effect of the Amyloid-ß peptide. FU Berlin
  Harmeier, A.
  
• (2008) Changing the copy number of transmitter transporters per vesicle - sorting versus expression under regime of day-night cycle. FU Berlin
  Darna, M
  
• (2008) Disruption of dendritic Arc/Arg3.1-translation impairs a unique intermediate phase of hippocampus-dependent memory. FU Berlin
  Mao, Xiaosong
  
• (2008) The effect of C-type natriuretic peptide on metaplasticity in the hippocampus. FU Berlin
  Decker, JM
  
• A novel control software that improves the experimental workflow of scanning photostimulation experiments. 2008, J Neurosci Methods. 175(1):44-57
  Bendels MH, Beed P, Leibold C, Schmitz D, Johenning FW
  
• C-Type natriuretic peptide modulates pre- and postsynaptic properties in hippocampal area CA1 in vitro. 2008, Biochem. Biophys Res Commun. 19;377(3):820-5
  Decker, Jochen Martin; Wojtowicz, Anna; Heinemann, Uwe & Braunewell, Karl-Heinz
  
• Conformational switch of syntaxin-1 controls synaptic vesicle fusion. 2008, Science. 321(5895):1507-10
  Gerber SH, Rah JC, Min SW, Liu X, de Wit H, Dulubova I, Meyer AC, Rizo J, Arancillo M, Hammer RE, Verhage M, Rosenmund C, Südhof TC
  
• Deletion of Go2alpha abolishes cocaine-induced behavioral sensitization by disturbing the striatal dopamine system. 2008, FASEB J. 22(10):3736-46
  Brunk I, Blex C, Sanchis-Segura C, Sternberg J, Perreau-Lenz S, Bilbao A, Hörtnagl H, Baron J, Juranek J, Laube G, Birnbaumer L, Spanagel R, Ahnert-Hilger G
  
• Different motifs regulate trafficking of SorCS1 isoforms. 2008, Traffic, 9(6): 980-94
  Nielsen MS, Keat SJ, Hamati JW, Madsen P, Gutzmann JJ, Engelsberg A, Pedersen KM, Gustafsen C, Nykjaer A, Gliemann J, Hermans-Borgmeyer I, Kuhl D, Petersen CM, Hermey G
  
• (2009) Expression of tumour invasion suppressor gene Visininlike Protein 1 (VILIP-1) and its role in metastasis of squamous cell carcinoma. FU Berlin
  Schönrath née Boeck, K.
  
• (2009) Synaptophysin/Synaptobrevin complex: Characterisation of the Ca2+- dependent cytosolic dissociation of the complex. FU Berlin
  Afube, T.
  
• C-type natriuretic peptide decreases hippocampal network oscillations in adult rats in vitro. 2009, Neuroscience. 164(4):1764-75
  Decker JM, Wójtowicz AM, Ul Haq R, Braunewell KH, Heinemann U, Behrens CJ
  
• Ca2+-dependent regulator of proteins secretion directly promote vesicular monoamine uptake. 2009, J Biol Chem 284:1050- 1056
  Brunk I, Blex C, Speidel D, Brose N, Ahnert-Hilger G
  
• Dendritic compartment and neuronal output mode determine pathway-specific long-term potentiation in the piriform cortex. 2009 Oct 28, J Neurosci.;29(43):13649-61
  Johenning FW, Beed PS, Trimbuch T, Bendels MH, Winterer J, Schmitz D
  
• GluK2-mediated excitability within the superficial layers of the entorhinal cortex. 2009, PLoS One. ;4(5):e5576
  Beed PS, Salmen B, Schmitz D
  
• p53 regulates the self-renewal and differentiation of neural precursors. 2009 Neuroscience.;158(4):1378-89
  Armesilla-Diaz A, Bragado P, Del Valle I, Cuevas E, Lazaro I, Martin C, Cigudosa JC, Silva A
  
• Role of amyloid-beta glycine 33 in oligomerization, toxicity, and neuronal plasticity. 2009, J Neurosci. 10;29(23):7582-90
  Harmeier A, Wozny C, Rost BR, Munter LM, Hua H, Georgiev O, Beyermann M, Hildebrand PW, Weise C, Schaffner W, Schmitz D, Multhaup G
  
• Synaptic PRG-1 modulates excitatory transmission via lipid phosphate-mediated signaling. 2009 Sep 18, Cell.;138(6):1222-35
  Trimbuch T, Beed P, Vogt J, Schuchmann S, Maier N, Kintscher M, Breustedt J, Schuelke M, Streu N, Kieselmann O, Brunk I, Laube G, Strauss U, Battefeld A, Wende H, Birchmeier C, Wiese S, Sendtner M, Kawabe H, Kishimoto-Suga M, Brose N, Baumgart J, Geist B, Aoki J, Savaskan NE, Bräuer AU, Chun J, Ninnemann O, Schmitz D, Nitsch R
  
• The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. 2009 Dec;11, Nat Cell Biol. (12):1411-20
  Rybak A, Fuchs H, Hadian K, Smirnova L, Wulczyn EA, Michel G, Nitsch R, Krappmann D, Wulczyn FG
  
• Time- of-day-dependent sorting of vesicular glutamate transporter to the plasma membrane. 2009, J Biol Chem 284:4300-4307
  Darna M, Schmutz I , Richter K, Höltje M, Yelamanchili SV, Pendyala G, Albrecht U, Ahnert-Hilger G
  
• (2010) Identification of low molecular weight pyroglutamate A{beta} oligomers in Alzheimer disease: a novel tool for therapy and diagnosis. 2010, J Biol Chem. ;285(53):41517-24
  Wirths, Oliver; Erck, Christian; Martens, Henrik; Harmeier, Anja; Geumann, Constanze; Jawhar, Sadim; Kumar, Sathish; Multhaup, Gerd; Walter, Jochen; Ingelsson, Martin; Degerman-Gunnarsson, Malin; Kalimo, Hannu; Huitinga, Inge; Lannfelt, Lars & Bayer, Thomas A.
  
• (2010) Loss of long-term potentiation at the CA1-subiculum synapse in temporal lobe epilepsy. FU Berlin
  Buck, N.
  
• (2010) Microcircuitry in the entorhinal cortex. FU Berlin
  Beed, P.
  
• (2010) Regulation of synaptic vesicle membrane trafficking events at neuronal synapses; FU Berlin (Dissertation)
  Pechstein, A.
  
• (2010) The reaction of spatial active hippocampal CA1-Pyramidal neurons to an exposition into a novel environment and their modulation during sleep. FU Berlin
  Lüdert, T.
  
• Amphetamine regulates NR2B expression in Go2α knockout mice and thereby sustains behavioral sensitization. 2010, J Neurochem. 115(1):234-46
  Brunk I, Sanchis-Segura C, Blex C, Perreau-Lenz S, Bilbao A, Spanagel R, Ahnert-Hilger G
  
• C-type natriuretic peptide modulates bidirectional plasticity in hippocampal area CA1 in vitro. 2010, Neuroscience.169(1):8-22
  Decker JM, Wójtowicz AM, Bartsch JC, Liotta A, Braunewell KH, Heinemann U, Behrens CJ
  
• Detection of input sites in scanning photostimulation data based on spatial correlations. 2010, J Neurosci Methods. 192(2):286-95
  Bendels MH, Beed P, Schmitz D, Johenning FW, Leibold C
  
• Intersectin 1: a versatile actor in the synaptic vesicle cycle. 2010 , Biochemical Society transactions 38:181-186
  Pechstein A, Shupliakov O, Haucke V
  
• MiRNA need a TRIM regulation of miRNA activity by Trim-NHL proteins. 2010, Adv Exp Med Biol. 2010;70
  Wulczyn FG, Cuevas E, Franzoni E, Rybak A
  
• Molecular basis for SH3 domain regulation of F-BAR- mediated membrane deformation. 2010, Proceedings of the National Academy of Sciences of the United States of America 107:8213-8218
  Rao Y, Ma Q, Vahedi-Faridi A, Sundborger A, Pechstein A, Puchkov D, Luo L, Shupliakov O, Saenger W, Haucke V
  
• Neuroligin 1 is dynamically exchanged at postsynaptic sites. 2010, J Neurosci 30:12733–12744
  Schapitz IU, Behrend B, Pechmann Y, Lappe-Siefke C, Kneussel SJ, Wallace KE, Stempel AV, Buck F, Grant SGN, Schweizer M, Schmitz D, Schwarz JR, Holzbaur ELF, Kneussel M
  
• Pyroglutamate Abeta pathology in APP/PS1KI mice, sporadic and familial Alzheimer's disease cases. 2010, J Neural Transm (Vienna). 117(1):85-96
  Wirths O, Bethge T, Marcello A, Harmeier A, Jawhar S, Lucassen PJ, Multhaup G, Brody DL, Esparza T, Ingelsson M, Kalimo H, Lannfelt L, Bayer TA
  
• Regulation of synaptic vesicle recycling by complex formation between intersectin 1 and the clathrin adaptor complex AP2. 2010, Proceedings of the National Academy of Sciences of the United States of America 107:4206-4211
  Pechstein A, Bacetic J, Vahedi-Faridi A, Gromova K, Sundborger A, Tomlin N, Krainer G, Vorontsova O, Schafer JG, Owe SG, Cousin MA, Saenger W, Shupliakov O, Haucke V
  
• Synaptic and vesicular co-existence of VGLUT and VGAT in selected excitatory and inhibitory synapses. 2010, J Neurosci 30:7634-7645
  Zander JF, Münster-Wandowski A, Brunk I, Pahner I, Gómez-Lira G, Heinemann U, Gutiérrez R, Laube G, Ahnert-Hilger G
  
• (2011) Analysis of the influence of the amyloid-β 42 peptide on gene regulation. FU Berlin
  Barucker, C.
  
• (2011) Gemeinsames Vorkommen von VGLUT und VGAT auf synaptischen Vesikeln und in inhibitorischen und exzitatorischen Nervenendigungen; HU-Berlin
  Zander, JF
  
• (2011) LPA signalling during axon growth
  Soriguera Farés, A.
  
• (2011) Neurotoxic phospholipases directly affect synaptic vesicle function. J Neurochem 117:757-764
  Treppmann P, Brunk I, Afube T, Richter K, Ahnert-Hilger G
  
• (2011) Target-cell-specific bidirectional synaptic plasticity at the CA1-subiculum synapse. FU Berlin
  Shor, O
  
• (2011) The cellular prion protein mediates neurotoxic signalling of β-sheet-rich conformers independent of prion replication. 2011, EMBO J. 30(10):2057-70
  Resenberger UK, Harmeier A, Woerner AC, Goodman JL, Müller V, Krishnan R, Vabulas RM, Kretzschmar HA, Lindquist S, Hartl FU, Multhaup G, Winklhofer KF, Tatzelt J
  
• (2011) Toxicity of Alzheimer's disease-associated Aβ peptide is ameliorated in a Drosophila model by tight control of zinc and copper availability. Biol Chem. 392(10):919-26
  Hua, Haiqing; Münter, Lisa; Harmeier, Anja; Georgiev, Oleg; Multhaup, Gerd & Schaffner, Walter
  
• (2011): Action potentials in primary osteoblasts and osteoblast like cell line MG-63. 2011 Jun , J Bioenerg Biomembr.;43(3):311-22
  Pangalos M, Bintig W, Schlingmann B, Feyerabend F, Witte F, Begandt D, Heisterkamp A, Ngezahayo A
  
• (2012): Purinergic receptors and Ca2+ signalling in the human blood-brain barrier endothelial cell line hCMEC/D3. 2012 Mar;8, Purinergic Signal. (1):71-80
  Bintig, Willem; Begandt, Daniela; Schlingmann, Barbara; Gerhard, Linda; Pangalos, Maria; Dreyer, Lutz; Hohnjec, Natalija; Couraud, Pierre-Olivier; Romero, Ignacio A.; Weksler, Babette B. & Ngezahayo, Anaclet
  
• Adrenergic modulation of sharp wave-ripple activity in rat hippocampal slices.Hippocampus. 2012 Mar;22(3):516-33
  Ul Haq, R.; Liotta, A.; Kovacs, R.; Rösler, A.; Jarosch, M.J.; Heinemann, U. & Behrens, C.J.
  
• Cell-type-specific modulation of feedback inhibition by serotonin in the hippocampus. 2011, J Neurosci 30(38):8464–8475
  Winterer J, Stempel AV, Dugladze T, Földy C, Maziashvili N, Zivkovic AR, Priller J, Soltesz I, Gloveli T, Schmitz D
  
• Coherent phasic excitation during hippocampal ripples. 2011, Neuron. 72(1):137-52
  Maier N, Tejero-Cantero A, Dorrn AL, Winterer J, Beed PS, Morris G, Kempter R, Poulet JF, Leibold C, Schmitz D
  
• Complementary sensory and associative microcircuitry in primary olfactory cortex. 2011 Aug 24, J Neurosci.;31(34):12149-58
  Wiegand HF, Beed P, Bendels MH, Leibold C, Schmitz D, Johenning FW
  
• Histaminergic modulation of acetylcholine-induced γ oscillations in rat hippocampus. 2011 Aug 3, Neuroreport.;22(11):520-4
  Fano S, Çalışkan G, Behrens CJ, Heinemann U
  
• Histaminergic modulation of acetylcholine-induced γ oscillations in rat hippocampus. 2011 Aug 3, Neuroreport.;22(11):520-4
  Fano S, Çalışkan G, Behrens CJ, Heinemann U
  
• How synapsin I may cluster synaptic vesicles. 2011, Seminars in cell & developmental biology 22:393-399
  Shupliakov O, Haucke V, Pechstein A
  
• miRNAs Need a Trim: Regulation of miRNA Activity by Trim-NHL Proteins. 2011 AdvExpMedBiol 700:85–105
  Wulczyn FG, Cuevas E, Franzoni E, Rybak A
  
• Nonspecific effects of the gap junction blocker mefloquine on fast hippocampal network oscillations in the adult rat in vitro. 2011, Neuroscience. 192:11-9
  Behrens CJ, ul Haq R, Liotta A, Anderson ML, Heinemann U
  
• Partial disinhibition is required for transition of stimulus-induced sharp wave-ripple complexes into recurrent epileptiform discharges in rat hippocampal slices. 2011 Jan, J Neurophysiol.;105(1):172-87
  Liotta A, Caliskan G, ul Haq R, Hollnagel JO, Rösler A, Heinemann U, Behrens CJ
  
• RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. 2011 Dec 16, Science;334(6062):1565-9
  Liu KS, Siebert M, Mertel S, Knoche E, Wegener S, Wichmann C, Matkovic T, Muhammad K, Depner H, Mettke C, Bückers J, Hell SW, Müller M, Davis GW, Schmitz D, Sigrist SJ
  
• RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. 2011, Dec 16. Science. 2011 Dec 16;334(6062):1565-9
  Liu KS, Siebert M, Mertel S, Knoche E, Wegener S, Wichmann C, Matkovic T, Muhammad K, Depner H, Mettke C, Bückers J, Hell SW, Müller M, Davis GW, Schmitz D, Sigrist SJ
  
• Role of the clathrin terminal domain in regulating coated pit dynamics revealed by small molecule inhibition. Cell. 2011 Aug 5;146(3):471-84. Erratum in: Cell.;146(5):841. Tomlin, Nikolay [corrected to Tomilin, Nikolay]
  von Kleist, Lisa; Stahlschmidt, Wiebke; Bulut, Haydar; Gromova, Kira; Puchkov, Dmytro; Robertson, Mark J.; MacGregor, Kylie A.; Tomilin, Nikolay; Pechstein, Arndt; Chau, Ngoc; Chircop, Megan; Sakoff, Jennette; von Kries, Jens Peter; Saenger, Wolfram; Kräusslich, Hans-Georg; Shupliakov, Oleg; Robinson, Phillip J.; McCluskey, Adam & Haucke, Volker
  
• (2012) Impact of disinhibition and neuromodulation in hippocampal oscillations and LTP. FU Berlin
  Liotta, A.
  
• (2012) Modulation of hippocampal sharp wave-ripple activity in vitro. FU Berlin
  ul Haq, R.
  
• (2012) Novel APP/Aβ mutation K16N produces highly toxic heteromeric Aβ oligomers. EMBO Mol Med. (7):647-59
  Kaden, Daniela; Harmeier, Anja; Weise, Christoph; Munter, Lisa M.; Althoff, Veit; Rost, Benjamin R.; Hildebrand, Peter W.; Schmitz, Dietmar; Schaefer, Michael; Lurz, Rudi; Skodda, Sabine; Yamamoto, Raina; Arlt, Sönke; Finckh, Ulrich & Multhaup, Gerd
  
• (2012): From TER to trans- and paracellular resistance: Lessons from impedance spectroscopy. 2012 Jun, Ann N Y Acad Sci.;1257:142-51
  Günzel D, Zakrzewski S, Schmid T, Pangalos M, Wiedenhoeft J, Blasse C, Ozboda C, Krug SM
  
• 20 years later: A second look on DF's motor behavior. 2012, Neuropsychologia 50(1):139-44
  Himmelbach M, Boehme R, Karnath HO
  
• All layers of medial entorhinal cortex receive presubicular and parasubicular inputs. 2012 Dec 5, J Neurosci.;32(49):17620-31
  Canto, Cathrin B.; Koganezawa, Noriko; Beed, Prateep; Moser, Edvard I. & Witter, Menno P.
  
• An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. 2012, Nat Neurosci 15:827–835
  Lehmann, Sabrina M; Krüger, Christina; Park, Boyoun; Derkow, Katja; Rosenberger, Karen; Baumgart, Jan; Trimbuch, Thorsten; Eom, Gina; Hinz, Michael; Kaul, David; Habbel, Piet; Kälin, Roland; Franzoni, Eleonora; Rybak, Agnieszka; Nguyen, Duong; Veh, Rüdiger; Ninnemann, Olaf; Peters, Oliver; Nitsch, Robert; ... & Lehnardt, Seija
  
• Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. 2012, Nature 486(7402):256-60
  Schmeisser, Michael J.; Ey, Elodie; Wegener, Stephanie; Bockmann, Juergen; Stempel, A. Vanessa; Kuebler, Angelika; Janssen, Anna-Lena; Udvardi, Patrick T.; Shiban, Ehab; Spilker, Christina; Balschun, Detlef; Skryabin, Boris V.; Dieck, Susanne tom; Smalla, Karl-Heinz; Montag, Dirk; Leblond, Claire S.; Faure, Philippe; Torquet, Nicolas; Le Sourd, Anne-Marie; ... & Boeckers, Tobias M.
  
• Differential effects of blockade of ERG channels on gamma oscillations and excitability in rat hippocampal slices. 2012 Dec, Eur J Neurosci., (12):3628-35
  Fano, Silvia; Çalışkan, Gürsel & Heinemann, Uwe
  
• Differential effects of blockade of ERG channels on gamma oscillations and excitability in rat hippocampal slices. 2012 Dec, Eur J Neurosci., (12):3628-35
  Fano, Silvia; Çalışkan, Gürsel & Heinemann, Uwe
  
• Energy demand of synaptic transmission at the hippocampal Schaffercollateral synapse. 2012 Nov, J Cereb Blood Flow Metab. 32(11):2076-83
  Liotta, Agustin; Rösner, Jörg; Huchzermeyer, Christine; Wojtowicz, Anna; Kann, Oliver; Schmitz, Dietmar; Heinemann, Uwe & Kovács, Richard
  
• Expression of toll-like receptors in the developing brain. 2012, PLoS ONE 7:e37767
  Kaul, David; Habbel, Piet; Derkow, Katja; Krüger, Christina; Franzoni, Eleonora; Wulczyn, F. Gregory; Bereswill, Stefan; Nitsch, Robert; Schott, Eckart; Veh, Rüdiger; Naumann, Thomas & Lehnardt, Seija
  
• Extracellular ATP differentially affects epileptiform activity via purinergic P2X7 and adenosine A1 receptors in naive and chronic epileptic rats. 2012 Nov, Epilepsia.;53(11):1978-86
  Klaft, Zin‐Juan; Schulz, Steffen B.; Maslarova, Anna; Gabriel, Siegrun; Heinemann, Uwe & Gerevich, Zoltan
  
• Extracellularly delivered single-stranded viral RNA causes neurodegeneration dependent on TLR7. 2012 Aug 1, J Immunol.;189(3):1448-58
  Lehmann, Sabrina M.; Rosenberger, Karen; Krüger, Christina; Habbel, Piet; Derkow, Katja; Kaul, David; Rybak, Agnieszka; Brandt, Christine; Schott, Eckart; Wulczyn, F. Gregory & Lehnardt, Seija
  
• First and second generation antipsychotics influence hippocampal gamma oscillations by interactions with 5-HT3 and D3 receptors. . 2012 Dec, Br J Pharmacol ;167(7):1480-91
  Schulz, Steffen B; Heidmann, Karin E; Mike, Arpad; Klaft, Zin‐Juan; Heinemann, Uwe & Gerevich, Zoltan
  
• Grid cells in rat entorhinal cortex encode physical space with independent firing fields and phase precession at the single-trial level. 2012 Apr 17, Proc Natl Acad Sci USA.;109(16):6301-6
  Reifenstein, Eric T.; Kempter, Richard; Schreiber, Susanne; Stemmler, Martin B. & Herz, Andreas V. M.
  
• Light-controlled toxicity of engineered amyloid β-peptides. 2012 Dec 21, Chembiochem;13(18):2657-60
  Hoppmann C, Barucker C, Lorenz D, Multhaup G, Beyermann M
  
• Long-lasting increase of corticosterone after fear memory reactivation: anxiolytic effects and network activity modulation in the ventral hippocampus. 2013 Feb, Neuropsychopharmacology. (;38(3):386-94
  Albrecht, Anne; Çalışkan, Gürsel; Oitzl, Melly S; Heinemann, Uwe & Stork, Oliver
  
• Peri-infarct blood-brain barrier dysfunction facilitates induction of spreading depolarization associated with epileptiform discharges. 2012 Dec., Neurobiol Dis. 48(3):495-506
  Lapilover, E.G.; Lippmann, K.; Salar, S.; Maslarova, A.; Dreier, J.P.; Heinemann, U. & Friedman, A.
  
• Purinergic P2X, P2Y and adenosine receptors differentially modulate hippocampal gamma oscillations. 2012 Feb, Neuropharmacology.;62(2):914-24
  Schulz, Steffen B.; Klaft, Zin-Juan; Rösler, Anton R.; Heinemann, Uwe & Gerevich, Zoltan
  
• Reduced ictogenic potential of 4- aminopyridine in the hippocampal region in the pilocarpine model of epilepsy. 2012 Apr 4, Neurosci Lett.;513(2):124-8
  Zahn, Robert Karl; Liotta, Agustin; Kim, Simon; Sandow, Nora & Heinemann, Uwe
  
• (2013) Bruchpilot and RIM-binding protein determine presynaptic release; FU- Berlin
  Knoche, E.
  
• (2013) Characterization of Tmem128 – An activity regulated ER protein, interacting with the immediate early gene Arc/Arg3.1. FU Berlin
  Gutzmann, JJ
  
• (2013) Histaminergic modulation of gamma oscillations in rat hippocampus Histaminergene Modulation von Gammaoszillationen im Hippocampus einer Ratte. FU Berlin
  Fano, S
  
• A LED-based method for monitoring NAD(P)H and FAD fluorescence in cell cultures and brain slices. 2013 Jan 30, J Neurosci Methods.;212(2):222-7
  Rösner, Jörg; Liotta, Agustin; Schmitz, Dietmar; Heinemann, Uwe & Kovács, Richard
  
• Fast neurotransmitter release regulated by the endocytic scaffold intersectin. 2013, Proceedings of the National Academy of Sciences of the United States of America 110:8266-8271
  Sakaba T, Kononenko NL, Bacetic J, Pechstein A, Schmoranzer J, Yao L, Barth H, Shupliakov O, Kobler O, Aktories K, Haucke V
  
• Genome-wide profiling of the activity-dependent hippocampal transcriptome. 2013 Oct 17, PLoS One.;8(10):e76903
  Hermey, Guido; Mahlke, Claudia; Gutzmann, Jakob J.; Schreiber, Jörg; Blüthgen, Nils & Kuhl, Dietmar
  
• Inhibitory gradient along the dorsoventral axis in the medial entorhinal cortex. 2013 Sep 18, Neuron.;79(6):1197-207
  Beed, Prateep; Gundlfinger, Anja; Schneiderbauer, Sophie; Song, Jie; Böhm, Claudia; Burgalossi, Andrea; Brecht, Michael; Vida, Imre & Schmitz, Dietmar
  
• Model peptides uncover the role of the β-secretase transmembrane sequence in metal-ion mediated oligomerization. 2013 Dec 26. J Am Chem Soc. ;135(51):19354-61
  Munter, Lisa M.; Sieg, Holger; Bethge, Tobias; Liebsch, Filip; Bierkandt, Frank S.; Schleeger, Michael; Bittner, Heiko J.; Heberle, Joachim; Jakubowski, Norbert; Hildebrand, Peter W. & Multhaup, Gerd
  
• Noradrenergic interactions via autonomic nervous system: a promising target for extinction-based exposure therapy? 2013 Dec, J Neurophysiol.;110(11):2507-10
  Çalışkan, Gürsel & Albrecht, Anne
  
• Recruitment of oriens-lacunosum-moleculare interneurons during hippocampal ripples. 2013, Proc Natl Acad Sci USA 110(11):4398-403
  Pangalos, Maria; Donoso, José R.; Winterer, Jochen; Zivkovic, Aleksandar R.; Kempter, Richard; Maier, Nikolaus & Schmitz, Dietmar
  
• Reinforcement learning and dopamine in schizophrenia: dimensions of symptoms or specific features of a disease group? 2013, Frontiers in Psychiatry 4:172
  Deserno L, Boehme R, Heinz A, Schlagenhauf F
  
• Restoring polyamines protects from age-induced memory impairment in an autophagy-dependent manner. 2013 Oct;16 (Nat Neurosci. 10):1453-60
  Gupta, Varun K.; Scheunemann, Lisa; Eisenberg, Tobias; Mertel, Sara; Bhukel, Anuradha; Koemans, Tom S.; Kramer, Jamie M.; Liu, Karen S. Y.; Schroeder, Sabrina; Stunnenberg, Hendrik G.; Sinner, Frank; Magnes, Christoph; Pieber, Thomas R.; Dipt, Shubham; Fi
  
• Spermidine-triggered autophagy ameliorates memory during aging. Autophagy. 2014 Jan;10(1):178-9
  Sigrist, Stephan J; Carmona-Gutierrez, Didac; Gupta, Varun K; Bhukel, Anuradha; Mertel, Sara; Eisenberg, Tobias & Madeo, Frank
  
• Synaptic requiem: a duet for Piccolo and Bassoon. 2013 Apr 3, EMBO J.;32(7):920-2
  Kononenko N, Pechstein A, Haucke V
  
• Synaptophysin is involved in resetting of the mammalian circadian clock. 2013 Oct 1, J Circadian Rhythms.;11(1):11
  Aramendy M, Seibert S, Treppmann P, Richter K, Ahnert-Hilger G, Albrecht U
  
• The Bruchpilot cytomatrix determines the size of the readily releasable pool of synaptic vesicles. 2013 Aug 19, J Cell Biol;202(4):667-83
  Matkovic, Tanja; Siebert, Matthias; Knoche, Elena; Depner, Harald; Mertel, Sara; Owald, David; Schmidt, Manuela; Thomas, Ulrich; Sickmann, Albert; Kamin, Dirk; Hell, Stefan W.; Bürger, Jörg; Hollmann, Christina; Mielke, Thorsten; Wichmann, Carolin & Sigrist, Stephan J.
  
• The tortoise and the hare revisited. 2013 Sep 3, Elife.;2:e01233. doi: 10.7554/eLife.01233
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• The α-subunit of the trimeric GTPase Go2 regulates axonal growth. 2013, J Neurochem 124:782-794
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• Titration of Syntaxin1 in mammalian synapses reveals multiple roles in vesicle docking, priming, and release probability. 2013. J Neurosci 133:16698-16714
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• uevas Garcia, E., (2013) Study of the murine Stem Cell E3 Ubiquitin ligase Lin41 in Development and Postnatal stages through the characterization of Lin41 Gene Trap and conditional Knockout models. FU Berlin
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• (2014) Contribution of intrinsic properties of neurons on network oscillations in the rat hippocampus. FU Berlin
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• 2014 The two-neuron microcircuit: an in vitro model for studying synapse formation and function. FU Berlin
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• A presynaptic role for the cytomatrix protein GIT in synaptic vesicle recycling. 2014 Jun 12, Cell Rep;7(5):1417-25
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• Blood-brain barrier dysfunction can contribute to pharmacoresistance of seizures. 2014 Aug, Epilepsia.;55(8):1255-63
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• Changes in neural network homeostasis trigger neuropsychiatric symptoms. 2014 Feb , J Clin Invest.;124(2):696-711
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• Clathrin/ AP-2 mediate synaptic vesicle reformation from endosome-like vacuoles but are not essential for membrane retrieval at central synapses. 2014, Neuron 82: 981-988
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• Composition of Synaptic Boutons Reveals the Amounts of Vesicle Trafficking Proteins. 2014, Science 344: 1023-1028
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• Corticosterone and corticotropin-releasing factor acutely facilitate gamma oscillations in the hippocampus in vitro. 2015 Jan, Eur J Neurosci.;41(1):31-44
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• Drosophila Syd-1, liprin-α, and protein phosphatase 2A B' subunit Wrd function in a linear pathway to prevent ectopic accumulation of synaptic materials in distal axons. 2014 Jun 18, J Neurosci.;34(25):8474-87
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• Enhanced dopamine-dependent hippocampal plasticity after single MK- 801 application. 2015, Neuropsychopharmacology, 40(4):987-95
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• GABAB receptor dependent modulation of sharp wave-ripple complexes in the rat hippocampus in vitro. Neurosci Lett. 2014 Jun 27;574:15-20
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• Hilar somatostatin interneurons contribute to synchronized GABA activity in an in vitro epilepsy model. PLoS One. 2014, Jan 21;9(1):e86250
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• Investigation of synapse formation and function in a glutamatergic-GABAergic twoneuron microcircuit. 2014, J Neurosci, 34:855-68
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• Movement dependence and layer specificity of entorhinal phase precession in two-dimensional environments. 2014 Jun 24, PLoS One.;9(6):e100638
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• Nuclear translocation uncovers the amyloid peptide Aβ42 as a regulator of gene transcription. 2014 Jul 18, J Biol Chem.;289(29):20182-91
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• Nucleocytosolic depletion of the energy metabolite acetyl-coenzyme a stimulates autophagy and prolongs lifespan. 2014 Mar 4, Cell Metab.;19(3):431-44
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• The morphological and molecular nature of synaptic vesicle priming at the presynaptic active zone. 2014. Neuron. 84(2):416-31
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• Vesicle uncoating regulated by SH3- SH3 domain-mediated complex formation between endophilin and intersectin at synapses. 2015 Feb , EMBO Rep.;16(2):232-9
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• Vesicular glutamate transporters use flexible anion and cation binding sites for efficient accumulation of neurotransmitter. 2014 Dec 17, Neuron.;84(6):1287-301
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• (2015) Cannabinoid type 2 receptors mediate a celltypespecific plasticity in the hippocampus; FU-Berlin
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• (2015) Dynamics and mechanisms of blood-brain barrier dysfunction, cell damage and altered cerebral perfusion after cortical photothrombosis. (PhD – Charité)
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• (2015) Modulating hippocampal output in the pilocarpine model of epilepsy by beta-adenoceptor activation. HU-Berlin
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• (2015) Role of hippocampal network activities in stress- and fear-related processes. FU Berlin
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• (2015) Synaptic plasticity in the subiculum and its alteration in the MK-801 model of psychosis. FU Berlin
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• 5-HT receptor-mediated modulation of granule cell inhibition after juvenile stress recovers after a second exposure to adult stress. 2015, Neuroscience. 293:67-79
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• A high affinity RIM-binding protein/Aplip1 interaction prevents the formation of ectopic axonal active zones. 2015 Aug 14, Elife. 4
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• Aberrant Salience Is Related to Dysfunctional Self-Referential Processing in Psychosis. 2015, Schizophr Bull. Jul 20
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• Aberrant salience is related to reduced reinforcement learning signals and elevated dopamine synthesis capacity in healthy adults. 2015, Schizophr Bull. Jul 20
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• Alzheimer amyloid peptide aβ42 regulates gene expression of transcription and growth factors. 2015, J Alzheimers Dis., 44(2):613-24
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• Anatomical Organization and Spatiotemporal Firing Patterns of Layer 3 Neurons in the Rat Medial Entorhinal Cortex. 2015, J Neurosci. 35(36):12346-54
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• Conditional depletion of intellectual disability and Parkinsonism candidate gene ATP6AP2 in fly and mouse induces cognitive impairment and neurodegeneration. 2015 Sep 16. Hum Mol Genet. pii: ddv380
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• Differential participation of pyramidal cells in generation of spontaneous sharp wave-ripples in the mouse subiculum in vitro. 2015 Aug 28, Neurobiol Learn Mem.;125:113-119
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• Dynamical Organization of Syntaxin-1A at the Presynaptic Active Zone. 2015, PLoS Comput Biol. 11(9):e1004407
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• Functional Diversity of Subicular Principal Cells during Hippocampal Ripples. 2015 Oct 7, J. Neurosci. ;35(40):13608-18
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• Gating of hippocampal output by β-adrenergic receptor activation in the pilocarpine model of epilepsy. 2015, Neuroscience, 286:325-37
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• Lights on for the molecular players of presynaptic plasticity. 2015 May 6, Neuron.;86(3):603-4
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• Lin41/Trim71 is essential for mouse development and specifically expressed in postnatal ependymal cells of the brain. 2015, Front Cell Dev Biol 3:20
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• Long-term changes in the CA3 associative network of fear-conditioned mice. Stress. 2015 Jan 30:1-10
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• miR-128 regulates neuronal migration, outgrowth and intrinsic excitability via the intellectual disability gene Phf6. 2015, Elife 4:e04263
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• No evidence for role of extracellular choline-acetyltransferase in generation of gamma oscillations in rat hippocampal slices in vitro. Neuroscience. 2015 Jan 22;284:459-69
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• Prefrontal and Striatal Glutamate Differently Relate to Striatal Dopamine: Potential Regulatory Mechanisms of Striatal Presynaptic Dopamine Function? 2015 Jul 1, J Neurosci.;35(26):9615-21
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• Presynaptic spinophilin tunes neurexin signalling to control active zone architecture and function. 2015, Nat Commun. 6:8362
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• Serotonin Attenuates Feedback Excitation onto O-LM Interneurons. 2015 Nov;25, Cereb Cortex. (11):4572-83
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• Syntaxin 1B is important for mouse postnatal survival and proper synaptic function at the mouse neuromuscular junctions. 2015, J Neurophysiol. 114(4):2404-17
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• The GAD65 knock out mouse - a model for GABAergic processes in fear- and stress-induced psychopathology. 2015 Jan, Genes Brain Behav.;14(1):37-45
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• Ventral striatal dopamine reflects behavioral and neural signatures of model-based control during sequential decision making. 2015 Feb 3, Proc Natl Acad Sci USA.; 112(5):1595-600
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• (2015) In vitro seizure like events and changes in ionic concentration. J Neurosci Methods
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• Serotonin dependent masking of hippocampal sharp wave ripples. 2015, Neuropharmacology. 101:188-203
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