nach oben

Erschienen in:

11.08.2016 | Original Article

Adult-born dentate granule cells show a critical period of dendritic reorganization and are distinct from developmentally born cells

verfasst von: Marcel Beining, Tassilo Jungenitz, Tijana Radic, Thomas Deller, Hermann Cuntz, Peter Jedlicka, Stephan Wolfgang Schwarzacher

Erschienen in: Brain Structure and Function | Ausgabe 3/2017

Einloggen, um Zugang zu erhalten

Abstract

Adult-born dentate granule cells (abGCs) exhibit a critical developmental phase during function integration. The time window of this phase is debated and whether abGCs become indistinguishable from developmentally born mature granule cells (mGCs) is uncertain. We analyzed complete dendritic reconstructions from abGCs and mGCs using viral labeling. AbGCs from 21–77 days post intrahippocampal injection (dpi) exhibited comparable dendritic arbors, suggesting that structural maturation precedes functional integration. In contrast, significant structural differences were found compared to mGCs: AbGCs had more curved dendrites, more short terminal segments, a different branching pattern, and more proximal terminal branches. Morphological modeling attributed these differences to developmental dendritic pruning and postnatal growth of the dentate gyrus. We further correlated GC morphologies with the responsiveness to unilateral medial perforant path stimulation using the immediate–early gene Arc as a marker of synaptic activation. Only abGCs at 28 and 35 dpi but neither old abGCs nor mGCs responded to stimulation with a remodeling of their dendritic arbor. Summarized, abGCs stay distinct from mGCs and their dendritic arbor can be shaped by afferent activity during a narrow critical time window.

Nur mit Berechtigung zugänglich

Alcántara S, Ruiz M, Arcangelo GD, Ezan F, De Lecea L, Curran T, Sotelo C, Soriano E (1998) Regional and cellular patterns of reelin mRNA expression in the forebrain of the developing and adult mouse. J Neurosci 18:7779–7799PubMed

Amaral D, Scharfman H, Lavenex P (2007) The dentate gyrus: fundamental neuroanatomical organization (dentate gyrus for dummies). Prog Brain Res 153:390–394

Ascoli GA, Donohue DE, Halavi M (2007) NeuroMorpho.Org: a central resource for neuronal morphologies. J Neurosci 27:9247–9251CrossRefPubMed

Bergami M, Masserdotti G, Temprana SG, Motori E, Eriksson TM, Göbel J, Yang SM, Conzelmann KK, Schinder AF, Götz M, Berninger B (2015) A critical period for experience-dependent remodeling of adult-born neuron connectivity. Neuron 85:710–717CrossRefPubMed

Bergmann O, Spalding KL, Frisén J (2015) Adult neurogenesis in humans. Cold Spring Harb Perspect Biol 7:1–12CrossRef

Bramham CR, Alme MN, Bittins M, Kuipers SD, Nair RR, Pai B, Panja D, Schubert M, Soule J, Tiron A, Wibrand K (2010) The arc of synaptic memory. Exp Brain Res 200:125–140CrossRefPubMed

Branco T, Häusser M (2010) The single dendritic branch as a fundamental functional unit in the nervous system. Curr Opin Neurobiol 20:494–502CrossRefPubMed

Brunner J, Neubrandt M, Van-Weert S, Andrási T, Kleine Borgmann FB, Jessberger S, Szabadics J (2014) Adult-born granule cells mature through two functionally distinct states. Elife 24:e03104

Claiborne BJ, Amaral DG, Cowan WM (1990) Quantitative, three-dimensional analysis of granule cell dendrites in the rat dentate gyrus. J Comp Neurol 302:206–219CrossRefPubMed

Clelland CD, Choi M, Romberg C, Clemenson GD, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325:210–213CrossRefPubMedPubMedCentral

Cuntz H, Borst A, Segev I (2007) Optimization principles of dendritic structure. Theor Biol Med Model 4:21CrossRefPubMedPubMedCentral

Cuntz H, Forstner F, Haag J, Borst A (2008) The morphological identity of insect dendrites. PLoS Comput Biol 4:e1000251CrossRefPubMedPubMedCentral

Cuntz H, Forstner F, Borst A, Häusser M (2010) One rule to grow them all: a general theory of neuronal branching and its practical application. PLoS Comput Biol 6:e1000877CrossRefPubMedPubMedCentral

Cuntz H, Forstner F, Borst A, Häusser M (2011) The TREES toolbox—probing the basis of axonal and dendritic branching. Neuroinformatics 9:91–96CrossRefPubMed

D’Arcangelo G (2014) Reelin in the years: controlling neuronal migration and maturation in the mammalian brain. Adv Neurosci 2014:1–19CrossRef

Deng W, Mayford M, Gage FH (2013) Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice. Elife 2:e00312CrossRefPubMedPubMedCentral

Desmond NL, Levy WB (1982) A quantitative anatomical study of the granule cell dendritic fields of the rat dentate gyrus using a novel probabilistic method. J Comp Neurol 212:131–145CrossRefPubMed

Duan X, Chang JH, Ge S, Faulkner RL, Kim JY, Kitabatake Y, Liu XB, Yang CH, Jordan JD, Ma DK, Liu CY, Ganesan S, Cheng HJ, Ming GL, Lu B, Song H (2007) Disrupted-In-Schizophrenia 1 regulates integration of newly generated neurons in the adult brain. Cell 130:1146–1158CrossRefPubMedPubMedCentral

Emoto K (2011) Dendrite remodeling in development and disease. Dev Growth Differ 53:277–286CrossRefPubMed

Espósito MS, Piatti VC, Laplagne DA, Morgenstern NA, Ferrari CC, Pitossi FJ, Schinder AF (2005) Neuronal differentiation in the adult hippocampus recapitulates embryonic development. J Neurosci 25:10074–10086CrossRefPubMed

Fitzsimons CP, van Hooijdonk LW, Schouten M, Zalachoras I, Brinks V, Zheng T, Schouten TG, Saaltink DJ, Dijkmans T, Steindler DA, Verhaagen J, Verbeek FJ, Lucassen PJ, de Kloet ER, Meijer OC, Karst H, Joels M, Oitzl MS, Vreugdenhil E (2013) Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior. Mol Psychiatry 18:993–1005CrossRefPubMed

Fornasiero EF, Bonanomi D, Benfenati F, Valtorta F (2010) The role of synapsins in neuronal development. Cell Mol Life Sci 67:1383–1396CrossRefPubMed

Förster E, Zhao S, Frotscher M (2006) Laminating the hippocampus. Nat Rev Neurosci 7:259–267CrossRefPubMed

Frotscher M (2010) Role for Reelin in stabilizing cortical architecture. Trends Neurosci 33:407–414CrossRefPubMed

Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, Inokuchi K (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38:447–460CrossRefPubMed

Ge S, Yang C-H, Hsu K-S, Ming G-L, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54:559–566CrossRefPubMedPubMedCentral

Gonçalves JT, Bloyd CW, Shtrahman M, Johnston ST, Schafer ST, Parylak SL, Tran T, Chang T, Gage FH (2016) In vivo imaging of dendritic pruning in dentate granule cells. Nat Neurosci 19:788–791CrossRefPubMedPubMedCentral

Green EJ, Juraska JM (1985) The dendritic morphology of hippocampal dentate granule cells varies with their position in the granule cell layer: a quantitative Golgi study. Exp Brain Res 59:582–586CrossRefPubMed

Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, Frankland PW, Ge S (2012) Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 15:1700–1706CrossRefPubMedPubMedCentral

Hsu T-T, Lee C-T, Tai M-H, Lien C-C (2015) Differential recruitment of dentate gyrus interneuron types by commissural versus perforant pathways. Cereb Cortex 26:2715–2727CrossRefPubMed

Ivanco TL, Racine RJ, Kolb B (2000) Morphology of layer III pyramidal neurons is altered following induction of LTP in sensorimotor cortex of the freely moving rat. Synapse 37:16–22CrossRefPubMed

Jedlicka P, Schwarzacher SW, Winkels R, Kienzler F, Frotscher M, Bramham CR, Schultz C, Bas Orth C, Deller T (2009) Impairment of in vivo theta-burst long-term potentiation and network excitability in the dentate gyrus of synaptopodin-deficient mice lacking the spine apparatus and the cisternal organelle. Hippocampus 19:130–140CrossRefPubMed

Jedlicka P, Vnencak M, Krueger DD, Jungenitz T, Brose N, Schwarzacher SW (2015) Neuroligin-1 regulates excitatory synaptic transmission, LTP and EPSP-spike coupling in the dentate gyrus in vivo. Brain Struct Funct 220:47–58CrossRefPubMed

Johnston ST, Shtrahman M, Parylak S, Gonçalves JT, Gage FH (2016) Paradox of pattern separation and adult neurogenesis: a dual role for new neurons balancing memory resolution and robustness. Neurobiol Learn Mem 129:60–68CrossRefPubMed

Jungenitz T, Radic T, Jedlicka P, Schwarzacher SW (2014) High-frequency stimulation induces gradual immediate early gene expression in maturing adult-generated hippocampal granule cells. Cereb Cortex 24:1845–1857CrossRefPubMed

Kee N, Teixeira CM, Wang AH, Frankland PW (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10:355–362CrossRefPubMed

Kempermann G (2015) Activity dependency and aging in the regulation of adult neurogenesis. Cold Spring Harb Perspect Biol 7:a018929CrossRefPubMed

Koleske AJ (2013) Molecular mechanisms of dendrite stability. Nat Rev Neurosci 14:536–550CrossRefPubMedPubMedCentral

Krueppel R, Remy S, Beck H (2011) Dendritic integration in hippocampal dentate granule cells. Neuron 71:512–528CrossRefPubMed

Kügler S, Meyn L, Holzmüller H, Gerhardt E, Isenmann S, Schulz JB, Bähr M (2001) Neuron-specific expression of therapeutic proteins: evaluation of different cellular promoters in recombinant adenoviral vectors. Mol Cell Neurosci 17:78–96CrossRefPubMed

Kügler S, Kilic E, Bähr M (2003) Human synapsin 1 gene promoter confers highly neuron-specific long-term transgene expression from an adenoviral vector in the adult rat brain depending on the transduced area. Gene Ther 10:337–347CrossRefPubMed

Kuroda H, Kutner RH, Bazan NG, Reiser J (2008) A comparative analysis of constitutive and cell-specific promoters in the adult mouse hippocampus using lentivirus vector-mediated gene transfer. J Gene Med 10:1163–1175CrossRefPubMed

Laplagne DA, Espósito MS, Piatti VC, Morgenstern NA, Zhao C, van Praag H, Gage FH, Schinder AF (2006) Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4:e409CrossRefPubMedPubMedCentral

Lee H, Kang E, Goodsmith D, Yoon DY, Song H, Knierim JJ, Ming G, Christian KM (2015) DISC1-mediated dysregulation of adult hippocampal neurogenesis in rats. Front Syst Neurosci 9:1–8CrossRef

Lefebvre JL, Sanes JR, Kay JN (2015) Development of dendritic form and function. Annu Rev Cell Dev Biol 31:741–777CrossRefPubMed

Lemaire V, Tronel S, Montaron M-F, Fabre A, Dugast E, Abrous DN (2012) Long-lasting plasticity of hippocampal adult-born neurons. J Neurosci 32:3101–3108CrossRefPubMed

Li G, Pleasure SJ (2010) Ongoing interplay between the neural network and neurogenesis in the adult hippocampus. Curr Opin Neurobiol 20:126–133CrossRefPubMedPubMedCentral

Llorens-Martín M, Rábano A, Ávila J (2016) The Ever-Changing Morphology of Hippocampal Granule Neurons in Physiology and Pathology. Front Neurosci 9:1–20CrossRef

Loy R, Lynch G, Cotman CW (1977) Development of afferent lamination in the fascia dentata of the rat. Brain Res 121:229–243CrossRefPubMed

Lyford GL, Yamagata K, Kaufmann WE, Barnes CA, Sanders LK, Copeland NG, Gilbert DJ, Jenkins NA, Lanahan AA, Worley PF (1995) Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14:433–445CrossRefPubMed

Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363–366CrossRefPubMed

Marín-Burgin A, Mongiat LA, Pardi MB, Schinder AF (2012) Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 335:1238–1242CrossRefPubMedPubMedCentral

Mathews EA, Morgenstern NA, Piatti VC, Zhao C, Jessberger S, Schinder AF, Gage FH (2010) A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis. J Comp Neurol 518:4479–4490CrossRefPubMedPubMedCentral

Monfils M-H, Teskey GC (2004) Induction of long-term depression is associated with decreased dendritic length and spine density in layers III and V of sensorimotor neocortex. Synapse 53:114–121CrossRefPubMed

Mongiat LA, Espósito MS, Lombardi G, Schinder AF (2009) Reliable activation of immature neurons in the adult hippocampus. PLoS One 4:e5320CrossRefPubMedPubMedCentral

Muramatsu R, Ikegaya Y, Matsuki N, Koyama R (2007) Neonatally born granule cells numerically dominate adult mice dentate gyrus. Neuroscience 148:593–598CrossRefPubMed

Myers CEC, Scharfman HE (2011) Pattern separation in the dentate gyrus: a role for the CA3 backprojection. Hippocampus 21:1190–1215CrossRefPubMed

Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Barrera VR, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149:188–201CrossRefPubMedPubMedCentral

Norkett R, Modi S, Birsa N, Atkin TA, Ivankovic D, Pathania M, Trossbach SV, Korth C, Hirst WD, Kittler JT (2016) DISC1-dependent regulation of mitochondrial dynamics controls the morphogenesis of complex neuronal dendrites. J Biol Chem 291:613–629CrossRefPubMed

Ohkawa N, Saitoh Y, Tokunaga E, Nihonmatsu I, Ozawa F, Murayama A, Shibata F, Kitamura T, Inokuchi K (2012) Spine formation pattern of adult-born neurons is differentially modulated by the induction timing and location of hippocampal plasticity. PLoS One 7:e45270CrossRefPubMedPubMedCentral

Okuno H, Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, Nonaka M, Kawashima T, Fujii H, Takemoto-Kimura S, Abe M, Natsume R, Chowdhury S, Sakimura K, Worley PF, Bito H (2012) Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIβ. Cell 149:886–898CrossRefPubMedPubMedCentral

Peebles CL, Yoo J, Thwin MT, Palop JJ, Noebels JL, Finkbeiner S (2010) Arc regulates spine morphology and maintains network stability in vivo. Proc Natl Acad Sci USA 107:18173–18178CrossRefPubMedPubMedCentral

Pesold C, Impagnatiello F, Pisu MG, Uzunov DP, Costa E, Guidotti A, Caruncho HJ (1998) Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats. Proc Natl Acad Sci USA 95:3221–3226CrossRefPubMedPubMedCentral

Pologruto TA, Sabatini BL, Svoboda K (2003) ScanImage: flexible software for operating laser scanning microscopes. Biomed Eng Online 2:13CrossRefPubMedPubMedCentral

Radic T, Al-Qaisi O, Jungenitz T, Beining M, Schwarzacher SW (2015) Differential structural development of adult-born septal hippocampal granule cells in the Thy1-GFP mouse, nuclear size as a new index of maturation. PLoS One 10:e0135493CrossRefPubMedPubMedCentral

Rahimi O, Claiborne BJ (2007) Morphological development and maturation of granule neuron dendrites in the rat dentate gyrus. Prog Brain Res 163:167–181CrossRefPubMed

Rall W, Rinzel J (1973) Branch input resistance and steady attenuation for input to one branch of a dendritic neuron model. Biophys J 13:648–687CrossRefPubMedPubMedCentral

Reeves TM, Steward O (1986) Emergence of the capacity for LTP during reinnervation of the dentate gyrus: evidence that abnormally shaped spines can mediate LTP. Exp Brain Res 65:167–175CrossRefPubMed

Restivo L, Niibori Y, Mercaldo V, Josselyn SA, Frankland PW (2015) Development of adult-generated cell connectivity with excitatory and inhibitory cell populations in the hippocampus. J Neurosci 35:10600–10612CrossRefPubMed

Ribak CE, Shapiro LA (2007) Dendritic development of newly generated neurons in the adult brain. Brain Res Rev 55:390–394CrossRefPubMed

Rihn LL, Claiborne BJ (1990) Dendritic growth and regression in rat dentate granule cells during late postnatal development. Dev Brain Res 54:115–124CrossRef

Rosenzweig S, Wojtowicz JM (2011) Analyzing dendritic growth in a population of immature neurons in the adult dentate gyrus using laminar quantification of disjointed dendrites. Front Neurosci 5:34CrossRefPubMedPubMedCentral

Schmidt-Hieber C, Jonas P, Bischofberger J (2007) Subthreshold dendritic signal processing and coincidence detection in dentate gyrus granule cells. J Neurosci 27:8430–8441CrossRefPubMed

Schneider CJ, Cuntz H, Soltesz I (2014) Linking macroscopic with microscopic neuroanatomy using synthetic neuronal populations. PLoS Comput Biol 10:e1003921CrossRefPubMedPubMedCentral

Schuldiner O, Yaron A (2014) Mechanisms of developmental neurite pruning. Cell Mol Life Sci 72:101–119CrossRefPubMedPubMedCentral

Schwarzacher S, Vuksic M, Haas C, Burbach G, Sloviter RS, Deller T (2006) Neuronal hyperactivity induces astrocytic expression of neurocan in the adult rat hippocampus. Glia 714:704–714CrossRef

Sengupta P (2013) The Laboratory Rat: relating Its Age With Human’s. Int J Prev Med 4:624–630PubMedPubMedCentral

Sidiropoulou K, Pissadaki EK, Poirazi P (2006) Inside the brain of a neuron. EMBO Rep 7:886–892CrossRefPubMedPubMedCentral

Šišková Z, Justus D, Kaneko H, Friedrichs D, Henneberg N, Beutel T, Pitsch J, Schoch S, Becker A, von der Kammer H, Remy S (2014) Dendritic structural degeneration is functionally linked to cellular hyperexcitability in a mouse model of Alzheimer’s disease. Neuron 84:1023–1033CrossRefPubMed

St John JL, Rosene DL, Luebke JI (1997) Morphology and electrophysiology of dentate granule cells in the rhesus monkey: comparison with the rat. J Comp Neurol 387:136–147

Steward O, Wallace CS, Lyford GL, Worley PF (1998) Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 21:741–751CrossRefPubMed

Stone SSD, Teixeira CM, Zaslavsky K, Wheeler AL, Martinez-Canabal A, Wang AH, Sakaguchi M, Lozano AM, Frankland PW (2011) Functional convergence of developmentally and adult-generated granule cells in dentate gyrus circuits supporting hippocampus-dependent memory. Hippocampus 21:1348–1362CrossRefPubMed

Sun GJ, Sailor KA, Mahmood QA, Chavali N, Christian KM, Song H, Ming G (2013) Seamless reconstruction of intact adult-born neurons by serial end-block imaging reveals complex axonal guidance and development in the adult hippocampus. J Neurosci 33:11400–11411CrossRefPubMedPubMedCentral

Tavosanis G (2012) Dendritic structural plasticity. Dev Neurobiol 72:73–86CrossRefPubMed

Teixeira CM, Kron MM, Masachs N, Zhang H, Lagace DC, Martinez A, Reillo I, Duan X, Bosch C, Pujadas L, Brunso L, Song H, Eisch AJ, Borrell V, Howell BW, Parent JM, Soriano E (2012) Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus. J Neurosci 32:12051–12065CrossRefPubMedPubMedCentral

Temprana SG, Mongiat LA, Yang SM, Trinchero MF, Alvarez DD, Kropff E, Giacomini D, Beltramone N, Lanuza GM, Schinder AF (2014) Delayed coupling to feedback inhibition during a critical period for the integration of adult-born granule cells. Neuron 85:116–130CrossRefPubMedPubMedCentral

Teskey GC, Monfils M-HH, Silasi G, Kolb B, Young NA, Van Rooyen F, Larson SEM, Flynn C, Monfils M-HH, Kleim JA, Henry LC, Goertzen CD, Silasi G, Kolb B (2006) Neocortical kindling is associated with opposing alterations in dendritic morphology in neocortical layer V and striatum from neocortical layer III. Synapse 59:1–9CrossRefPubMed

Tronel S, Lemaire V, Charrier V, Montaron M-F, Abrous DN (2015) Influence of ontogenetic age on the role of dentate granule neurons. Brain Struct Funct 220:645–661CrossRefPubMed

van Praag H, Schinder AF, Christie BR, Toni N, Palmer TD, Gage FH (2002) Functional neurogenesis in the adult hippocampus. Nature 415:1030–1034CrossRefPubMed

Vuksic M, Del Turco D, Bas Orth C, Burbach GJ, Feng G, Müller CM, Schwarzacher SW, Deller T (2008) 3D-reconstruction and functional properties of GFP-positive and GFP-negative granule cells in the fascia dentata of the Thy1-GFP mouse. Hippocampus 18:364–375CrossRefPubMed

Vuksic M, Del Turco D, Vlachos A, Schuldt G, Müller CM, Schneider G, Deller T (2011) Unilateral entorhinal denervation leads to long-lasting dendritic alterations of mouse hippocampal granule cells. Exp Neurol 230:176–185CrossRefPubMed

Waung MW, Pfeiffer BE, Nosyreva ED, Ronesi JA, Huber KM (2008) Rapid translation of Arc/Arg3.1 selectively mediates mGluR-dependent LTD through persistent increases in AMPAR endocytosis rate. Neuron 59:84–97CrossRefPubMedPubMedCentral

Wilson RC (1981) Changes in translation of synaptic excitation to dentate granule cell discharge accompanying long-term potentiation. I. Differences between normal and reinnervated dentate gyrus. J Neurophysiol 46:324–338PubMed

Wilson RC, Levy WB, Steward O (1979) Functional effects of lesion-induced plasticity: long term potentiation in formal and lesion-induced temporodentate connections. Brain Res 176:65–78CrossRefPubMed

Yu D, Fan W, Wu P, Deng J, Liu J, Niu Y, Li M, Deng J (2014) Characterization of hippocampal Cajal–Retzius cells during development in a mouse model of Alzheimer’s disease (Tg2576). Neural Regen Res 9:394CrossRefPubMedPubMedCentral

Zhao C, Teng EM, Summers RG, Ming G-L, Gage FH (2006) Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus. J Neurosci 26:3–11CrossRefPubMed

Titel: Adult-born dentate granule cells show a critical period of dendritic reorganization and are distinct from developmentally born cells
verfasst von: Marcel Beining
Tassilo Jungenitz
Tijana Radic
Thomas Deller
Hermann Cuntz
Peter Jedlicka
Stephan Wolfgang Schwarzacher
Publikationsdatum: 11.08.2016
Verlag: Springer Berlin Heidelberg
Erschienen in: Brain Structure and Function / Ausgabe 3/2017
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-016-1285-y

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

^{Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag}

Kostenlos registrieren

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar "Chronische Unterbauch- und Viszeralschmerzen in der Praxis managen"

Springer Medizin

Adult-born dentate granule cells show a critical period of dendritic reorganization and are distinct from developmentally born cells

Abstract

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Stuhltransfusion könnte Fortschreiten von Parkinson-Symptomen bremsen

Frühe Tranexamsäure-Therapie nützt wenig bei Hirnblutungen

Sind Frauen die fähigeren Ärzte?

Akuter Schwindel: Wann lohnt sich eine MRT?

Update Neurologie

Live-Webinar "Chronische Unterbauch- und Viszeralschmerzen in der Praxis managen"

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 3/2017

Effects of dorsolateral prefrontal cortex lesion on motor habit and performance assessed with manual grasping and control of force in macaque monkeys

Education is associated with sub-regions of the hippocampus and the amygdala vulnerable to neuropathologies of Alzheimer’s disease

Axon diameter relates to synaptic bouton size: structural properties define computationally different types of cortical connections in primates

Dorso-medial and ventro-lateral functional specialization of the human retrosplenial complex in spatial updating and orienting

Rapid language-related plasticity: microstructural changes in the cortex after a short session of new word learning

NKCC1 up-regulation contributes to early post-traumatic seizures and increased post-traumatic seizure susceptibility

Leitlinien kompakt für die Neurologie

Neu im Fachgebiet Neurologie

Stuhltransfusion könnte Fortschreiten von Parkinson-Symptomen bremsen

Frühe Tranexamsäure-Therapie nützt wenig bei Hirnblutungen

Sind Frauen die fähigeren Ärzte?

Akuter Schwindel: Wann lohnt sich eine MRT?

Update Neurologie