Access the full text.
Sign up today, get DeepDyve free for 14 days.
Jason Snyder, Jessica Choe, Meredith Clifford, Sara Jeurling, Patrick Hurley, Ashly Brown, J. Kamhi, H. Cameron (2009)
Adult-Born Hippocampal Neurons Are More Numerous, Faster Maturing, and More Involved in Behavior in Rats than in MiceThe Journal of Neuroscience, 29
J. Altman, S. Bayer (1990)
Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periodsJournal of Comparative Neurology, 301
E. Satvat, Brandy Schmidt, Melissa Argraves, Diano Marrone, E. Markus (2011)
Changes in Task Demands Alter the Pattern of zif268 Expression in the Dentate GyrusThe Journal of Neuroscience, 31
H. Cameron, C. Woolley, B. McEwen, E. Gould (1993)
Differentiation of newly born neurons and glia in the dentate gyrus of the adult ratNeuroscience, 56
Chunmei Zhao, E. Teng, R. Summers, G. Ming, F. Gage (2006)
Distinct Morphological Stages of Dentate Granule Neuron Maturation in the Adult Mouse HippocampusThe Journal of Neuroscience, 26
Diano Marrone, M. Schaner, B. McNaughton, P. Worley, C. Barnes (2008)
Immediate-Early Gene Expression at Rest Recapitulates Recent ExperienceThe Journal of Neuroscience, 28
A. Tashiro, V. Sandler, N. Toni, Chunmei Zhao, F. Gage (2006)
NMDA-receptor-mediated, cell-specific integration of new neurons in adult dentate gyrusNature, 442
D. Dupret, Annabelle Fabre, M. Döbrössy, A. Panatier, Jose Rodriguez, S. Lamarque, V. Lemaire, S. Oliet, P. Piazza, D. Abrous (2007)
Spatial Learning Depends on Both the Addition and Removal of New Hippocampal NeuronsPLoS Biology, 5
D. Crespo, B. Stanfield, W. Cowan (2004)
Evidence that late-generated granule cells do not simply replace earlier formed neurons in the rat dentate gyrusExperimental Brain Research, 62
Matt Jones, M. Er̀rington, P. French, A. Fine, T. Bliss, S. Garel, P. Charnay, B. Bozon, S. Laroche, S. Davis (2001)
A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memoriesNature Neuroscience, 4
Kathleen Mcavoy, Kimberly Scobie, S. Berger, Craig Russo, N. Guo, Pakanat Decharatanachart, Hugo Vega-Ramirez, Sam Miake-Lye, M. Whalen, Mark Nelson, M. Bergami, D. Bartsch, R. Hen, B. Berninger, Amar Sahay (2016)
Modulating Neuronal Competition Dynamics in the Dentate Gyrus to Rejuvenate Aging Memory CircuitsNeuron, 91
T. Kitamura, Y. Saitoh, N. Takashima, A. Murayama, Yosuke Niibori, H. Ageta, M. Sekiguchi, H. Sugiyama, K. Inokuchi (2009)
Adult Neurogenesis Modulates the Hippocampus-Dependent Period of Associative Fear MemoryCell, 139
S. Jessberger, G. Kempermann (2003)
Adult‐born hippocampal neurons mature into activity‐dependent responsivenessEuropean Journal of Neuroscience, 18
G. Kempermann, H. Kuhn, F. Gage (1997)
Genetic influence on neurogenesis in the dentate gyrus of adult mice.Proceedings of the National Academy of Sciences of the United States of America, 94 19
O. Saitoh, C. Karns, E. Courchesne (2001)
Development of the hippocampal formation from 2 to 42 years: MRI evidence of smaller area dentata in autism.Brain : a journal of neurology, 124 Pt 7
E. Gould, H. Cameron, B. McEwen (1994)
Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrusJournal of Comparative Neurology, 340
Nathan Danielson, P. Kaifosh, Jeffrey Zaremba, Matthew Lovett-Barron, J. Tsai, C. Denny, Elizabeth Balough, A. Goldberg, L. Drew, R. Hen, A. Losonczy, M. Kheirbek (2016)
Distinct Contribution of Adult-Born Hippocampal Granule Cells to Context EncodingNeuron, 90
Heather McDonald, J. Wojtowicz (2005)
Dynamics of neurogenesis in the dentate gyrus of adult ratsNeuroscience Letters, 385
Linda Overstreet-Wadiche, A. Bensen, G. Westbrook (2006)
Delayed Development of Adult-Generated Granule Cells in Dentate GyrusThe Journal of Neuroscience, 26
E. Gould, A. Beylin, P. Tanapat, Alison Reeves, T. Shors (1999)
Learning enhances adult neurogenesis in the hippocampal formationNature Neuroscience, 2
Jason Snyder, Meredith Clifford, Sara Jeurling, H. Cameron (2012)
Complementary activation of hippocampal–cortical subregions and immature neurons following chronic training in single and multiple context versions of the water mazeBehavioural Brain Research, 227
Shawn Jones, Omid Rahimi, M. O'Boyle, Daniel Diaz, B. Claiborne (2003)
Maturation of granule cell dendrites after mossy fiber arrival in hippocampal field CA3Hippocampus, 13
H. Cameron, R. McKay (2001)
Adult neurogenesis produces a large pool of new granule cells in the dentate gyrusJournal of Comparative Neurology, 435
Sabrina Wang, B. Scott, J. Wojtowicz (2000)
Heterogenous properties of dentate granule neurons in the adult rat.Journal of neurobiology, 42 2
I. Amrein, L. Slomianka, H. Lipp (2004)
Granule cell number, cell death and cell proliferation in the dentate gyrus of wild‐living rodentsEuropean Journal of Neuroscience, 20
A. Álvarez-Buylla, J. Kirn (1997)
Birth, migration, incorporation, and death of vocal control neurons in adult songbirds.Journal of neurobiology, 33 5
M. Boldrini, M. Boldrini, Adrienne Santiago, R. Hen, A. Dwork, G. Rosoklija, G. Rosoklija, H. Tamir, V. Arango, J. Mann (2013)
Hippocampal Granule Neuron Number and Dentate Gyrus Volume in Antidepressant-Treated and Untreated Major DepressionNeuropsychopharmacology, 38
D. Laplagne, M. Soledad, Espó Sito, Veró Nica, C. Piatti, Nicolá, A. Morgenstern, Chunmei Zhao, Henriette Praag, Fred Gage, A. Schinder (2006)
Functional Convergence of Neurons Generated in the Developing and Adult HippocampusPLoS Biology, 4
A. Sierra, J. Encinas, J. Deudero, J. Chancey, G. Enikolopov, Linda Overstreet-Wadiche, S. Tsirka, M. Maletić-Savatić (2010)
Microglia shape adult hippocampal neurogenesis through apoptosis-coupled phagocytosis.Cell stem cell, 7 4
M. McKinnon, K. Yucel, A. Nazarov, G. MacQueen (2009)
A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder.Journal of psychiatry & neuroscience : JPN, 34 1
N. Kee, C. Teixeira, Afra Wang, P. Frankland (2007)
Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrusNature Neuroscience, 10
M. Rao, A. Shetty (2004)
Efficacy of doublecortin as a marker to analyse the absolute number anddendritic growth of newly generated neurons in the adult dentate gyrusEuropean Journal of Neuroscience, 19
M. Moscovitch, R. Cabeza, G. Winocur, L. Nadel (2016)
Episodic Memory and Beyond: The Hippocampus and Neocortex in Transformation.Annual review of psychology, 67
R. Chambers, S. Conroy (2007)
Network Modeling of Adult Neurogenesis: Shifting Rates of Neuronal Turnover Optimally Gears Network Learning according to Novelty GradientJournal of Cognitive Neuroscience, 19
C. Raineki, Parker Holman, J. Debiec, Melissa Bugg, Allyson Beasley, R. Sullivan (2010)
Functional emergence of the hippocampus in context fear learning in infant ratsHippocampus, 20
S. Tronel, Annabelle Fabre, V. Charrier, S. Oliet, F. Gage, D. Abrous (2010)
Spatial learning sculpts the dendritic arbor of adult-born hippocampal neuronsProceedings of the National Academy of Sciences, 107
Alice Schlessinger, W. Cowan, D. Gottlieb (1975)
An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the ratJournal of Comparative Neurology, 159
C. Alberini, Alessio Travaglia (2017)
Infantile Amnesia: A Critical Period of Learning to Learn and RememberThe Journal of Neuroscience, 37
N. DeCarolis, Maxwell Mechanic, D. Petrik, Adam Carlton, Jessica Ables, S. Malhotra, R. Bachoo, M. Götz, D. Lagace, A. Eisch (2013)
In vivo contribution of nestin‐ and GLAST‐lineage cells to adult hippocampal neurogenesisHippocampus, 23
A. Olariu, K. Cleaver, Lauren Shore, Michelle Brewer, H. Cameron (2005)
A natural form of learning can increase and decrease the survival of new neurons in the dentate gyrusHippocampus, 15
D. Alvarez, Damiana Giacomini, S. Yang, M. Trinchero, Silvio Temprana, Karina Büttner, Natalia Beltramone, A. Schinder (2016)
A disynaptic feedback network activated by experience promotes the integration of new granule cellsScience, 354
V. Lemaire, S. Tronel, M. Montaron, Annabelle Fabre, E. Dugast, D. Abrous (2012)
Long-Lasting Plasticity of Hippocampal Adult-Born NeuronsThe Journal of Neuroscience, 32
Emily Mathews, Nicolás Morgenstern, Verónica Piatti, Chunmei Zhao, S. Jessberger, A. Schinder, F. Gage (2010)
A Distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesisJournal of Comparative Neurology, 518
A. Veyrac, Alexandra Gros, E. Bruel-Jungerman, C. Rochefort, F. Borgmann, S. Jessberger, S. Laroche (2013)
Zif268/egr1 gene controls the selection, maturation and functional integration of adult hippocampal newborn neurons by learningProceedings of the National Academy of Sciences, 110
K. Fabricius, G. Wörtwein, B. Pakkenberg (2008)
The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampusBrain Structure & Function, 212
P. Worley, B. Christy, Y. Nakabeppu, R. Bhat, A. Cole, J. Baraban (1991)
Constitutive expression of zif268 in neocortex is regulated by synaptic activity.Proceedings of the National Academy of Sciences of the United States of America, 88
G. Kempermann, D. Gast, G. Kronenberg, M. Yamaguchi, F. Gage (2003)
Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice, 130
B. Richards, P. Frankland (2017)
The Persistence and Transience of MemoryNeuron, 94
Yan Gu, M. Arruda-Carvalho, Jia Wang, Stephen Janoschka, S. Josselyn, P. Frankland, S. Ge (2012)
Optical controlling reveals time-dependent roles for adult-born dentate granule cellsNature neuroscience, 15
C. Oomen, H. Soeters, N. Audureau, L. Vermunt, F. Hasselt, E. Manders, M. Joëls, H. Krugers, P. Lucassen (2010)
Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female ratsPsychopharmacology, 214
P. Worley, R. Bhat, J. Baraban, C. Erickson, B. Mcnaughton, C. Barnes (1993)
Thresholds for synaptic activation of transcription factors in hippocampus: correlation with long-term enhancement, 13
R. Muramatsu, Y. Ikegaya, N. Matsuki, R. Koyama (2007)
Neonatally born granule cells numerically dominate adult mice dentate gyrusNeuroscience, 148
G. Kempermann, H. Kuhn, F. Gage (1997)
More hippocampal neurons in adult mice living in an enriched environmentNature, 386
Katherine Akers, Alonso Martínez-canabal, L. Restivo, A. Yiu, Antonietta Cristofaro, H. Hsiang, Anne Wheeler, A. Guskjolen, Yosuke Niibori, Hirotaka Shoji, Koji Ohira, Blake Richards, Tsuyoshi Miyakawa, S. Josselyn, P. Frankland (2014)
Hippocampal Neurogenesis Regulates Forgetting During Adulthood and InfancyScience, 344
Jason Brown, S. Couillard-Després, C. Cooper-Kuhn, J. Winkler, L. Aigner, H. Kuhn (2003)
Transient expression of doublecortin during adult neurogenesisJournal of Comparative Neurology, 467
Shaina Cahill, R. Yu, Dylan Green, Evgenia Todorova, Jason Snyder (2016)
Early survival and delayed death of developmentally-born dentate gyrus neuronsbioRxiv
J. Guzowski, B. McNaughton, C. Barnes, P. Worley (1999)
Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensemblesNature Neuroscience, 2
Jason Snyder, H. Cameron (2012)
Could adult hippocampal neurogenesis be relevant for human behavior?Behavioural Brain Research, 227
M. Döbrössy, M. Döbrössy, Elodie Drapeau, C. Aurousseau, M. Moal, P. Piazza, D. Abrous (2003)
Differential effects of learning on neurogenesis: learning increases or decreases the number of newly born cells depending on their birth dateMolecular Psychiatry, 8
S. Becker (2005)
A computational principle for hippocampal learning and neurogenesisHippocampus, 15
Tracy Larson, Nivretta Thatra, Brian Lee, Eliot Brenowitz (2014)
Reactive Neurogenesis in Response to Naturally Occurring Apoptosis in an Adult BrainThe Journal of Neuroscience, 34
I. Mahar, I. Mahar, B. Labonté, B. Labonté, S. Yogendran, S. Yogendran, E. Isingrini, L. Perret, M. Davoli, A. Rachalski, B. Giros, G. Turecki, N. Mechawar, N. Mechawar (2017)
Disrupted hippocampal neuregulin-1/ErbB3 signaling and dentate gyrus granule cell alterations in suicideTranslational Psychiatry, 7
Leslie Meltzer, Raghu Yabaluri, K. Deisseroth (2005)
A role for circuit homeostasis in adult neurogenesisTrends in Neurosciences, 28
J. Altman, S. Bayer (1990)
Mosaic organization of the hippocampal neuroepithelium and the multiple germinal sources of dentate granule cellsJournal of Comparative Neurology, 301
B. Boss, G. Peterson, W. Cowan (1985)
On the number of neurons in the dentate gyrus of the ratBrain Research, 338
M. Esposito, Verónica Piatti, D. Laplagne, Nicolás Morgenstern, C. Ferrari, F. Pitossi, A. Schinder (2005)
Neuronal Differentiation in the Adult Hippocampus Recapitulates Embryonic DevelopmentThe Journal of Neuroscience, 25
K. Akers, D. Hamilton (2007)
Comparison of developmental trajectories for place and cued navigation in the Morris water task.Developmental psychobiology, 49 6
M. Brandt, S. Jessberger, B. Steiner, G. Kronenberg, K. Reuter, A. Bick-Sander, W. Behrens, G. Kempermann (2003)
Transient calretinin expression defines early postmitotic step of neuronal differentiation in adult hippocampal neurogenesis of miceMolecular and Cellular Neuroscience, 24
C. Montes-Rodríguez, Valérie Lapointe, Vivek Trivedi, Q. Lu, Aubrey Demchuk, B. McNaughton (2013)
Postnatal development of Homer1a in the rat hippocampusHippocampus, 23
S. Tronel, V. Lemaire, V. Charrier, M. Montaron, D. Abrous (2014)
Influence of ontogenetic age on the role of dentate granule neuronsBrain Structure and Function, 220
Xuefeng Liu, Shilpa Tilwalli, G. Ye, P. Lio, J. Pasternak, B. Trommer (2000)
Morphologic and electrophysiologic maturation in developing dentate gyrus granule cellsBrain Research, 856
A. Tashiro, Hiroshi Makino, F. Gage (2007)
Experience-Specific Functional Modification of the Dentate Gyrus through Adult Neurogenesis: A Critical Period during an Immature StageThe Journal of Neuroscience, 27
P. Rapp, M. Gallagher (1996)
Preserved neuron number in the hippocampus of aged rats with spatial learning deficits.Proceedings of the National Academy of Sciences of the United States of America, 93 18
D. Lodge, A. Grace (2011)
Hippocampal dysregulation of dopamine system function and the pathophysiology of schizophrenia.Trends in pharmacological sciences, 32 9
Jason Snyder, L. Glover, Kaitlin Sanzone, J. Kamhi, H. Cameron (2009)
The effects of exercise and stress on the survival and maturation of adult‐generated granule cellsHippocampus, 19
J. Guzowski, B. Setlow, E. Wagner, J. McGaugh (2001)
Experience-Dependent Gene Expression in the Rat Hippocampus after Spatial Learning: A Comparison of the Immediate-Early GenesArc, c-fos, and zif268The Journal of Neuroscience, 21
C. Mandyam, Gwyndolen Harburg, A. Eisch (2007)
Determination of key aspects of precursor cell proliferation, cell cycle length and kinetics in the adult mouse subgranular zoneNeuroscience, 146
C. Schumann, J. Hamstra, B. Goodlin‐Jones, L. Lotspeich, H. Kwon, M. Buonocore, C. Lammers, A. Reiss, D. Amaral (2004)
The Amygdala Is Enlarged in Children But Not Adolescents with Autism; the Hippocampus Is Enlarged at All AgesThe Journal of Neuroscience, 24
M. Boldrini, Tanya Butt, Adrienne Santiago, H. Tamir, A. Dwork, G. Rosoklija, V. Arango, R. Hen, J. Mann (2014)
Benzodiazepines and the potential trophic effect of antidepressants on dentate gyrus cells in mood disorders.The international journal of neuropsychopharmacology, 17 12
K. Spalding, O. Bergmann, K. Alkass, S. Bernard, M. Salehpour, H. Huttner, Emil Boström, Isabelle Westerlund, Céline Vial, B. Buchholz, G. Possnert, D. Mash, H. Druid, J. Frisén (2013)
Dynamics of Hippocampal Neurogenesis in Adult HumansCell, 153
C. Tamminga, A. Stan, A. Wagner (2010)
The hippocampal formation in schizophrenia.The American journal of psychiatry, 167 10
S. Ge, Chih-hao Yang, K. Hsu, G. Ming, Hongjun Song (2007)
A Critical Period for Enhanced Synaptic Plasticity in Newly Generated Neurons of the Adult BrainNeuron, 54
Shirley Bayer (2004)
Changes in the total number of dentate granule cells in juvenile and adult rats: A correlated volumetric and 3H-thymidine autoradiographic studyExperimental Brain Research, 46
Jason Snyder, Jason Snyder, Preethi Ramchand, Sarah Rabbett, Ruvim Radik, J. Wojtowicz, H. Cameron (2011)
Septo-temporal gradients of neurogenesis and activity in 13-month-old ratsNeurobiology of Aging, 32
Jason Snyder, Ruvim Radik, J. Wojtowicz, H. Cameron (2009)
Anatomical gradients of adult neurogenesis and activity: Young neurons in the ventral dentate gyrus are activated by water maze trainingHippocampus, 19
S. Bayer, J. Yackel, P. Puri (1982)
Neurons in the rat dentate gyrus granular layer substantially increase during juvenile and adult life.Science, 216 4548
T. Nakashiba, J. Cushman, K. Pelkey, S. Renaudineau, D. Buhl, T. McHugh, V. Barrera, R. Chittajallu, Keisuke Iwamoto, C. McBain, M. Fanselow, S. Tonegawa (2012)
Young Dentate Granule Cells Mediate Pattern Separation, whereas Old Granule Cells Facilitate Pattern CompletionCell, 149
J. Epp, M. Spritzer, L. Galea (2007)
Hippocampus-dependent learning promotes survival of new neurons in the dentate gyrus at a specific time during cell maturationNeuroscience, 149
J. Rudy (1993)
Contextual conditioning and auditory cue conditioning dissociate during development.Behavioral neuroscience, 107 5
Kylie Huckleberry, Gary Kane, Rita Mathis, Sarah Cook, J. Clutton, M. Drew (2015)
Behavioral experience induces zif268 expression in mature granule cells but suppresses its expression in immature granule cellsFrontiers in Systems Neuroscience, 9
A. Dayer, Abigail Ford, K. Cleaver, M. Yassaee, H. Cameron (2003)
Short‐term and long‐term survival of new neurons in the rat dentate gyrusJournal of Comparative Neurology, 460
S. Stone, C. Teixeira, K. Zaslavsky, A. Wheeler, Alonso Martínez-canabal, Afra Wang, M. Sakaguchi, Andres Lozano, P. Frankland (2011)
Functional convergence of developmentally and adult‐generated granule cells in dentate gyrus circuits supporting hippocampus‐dependent memoryHippocampus, 21
The storage and persistence of memories depends on plasticity in the hippocampus. Adult neurogenesis produces new neurons that mature through critical periods for plasticity and cellular survival, which determine their contributions to learning and memory. However, most granule neurons are generated prior to adulthood; the maturational timecourse of these neurons is poorly understood compared to adult‐born neurons but is essential to identify how the dentate gyrus (DG), as a whole, contributes to behavior. To characterize neurons born in the early postnatal period, we labeled DG neurons born on postnatal day 6 (P6) with BrdU and quantified maturation and survival across early (1 hr to 8 weeks old) and late (2–6 months old) cell ages. We find that the dynamics of developmentally‐born neuron survival is essentially the opposite of neurons born in adulthood: P6‐born neurons did not go through a period of cell death during their immature stages (from 1 to 8 weeks). In contrast, 17% of P6‐born neurons died after reaching maturity, between 2 and 6 months of age. Delayed death was evident from the loss of BrdU+ cells as well as pyknotic BrdU+caspase3+ neurons within the superficial granule cell layer. Patterns of DCX, NeuN, and activity‐dependent Fos expression indicate that developmentally‐born neurons mature over several weeks and a sharp peak in zif268 expression at 2 weeks suggests that developmentally‐born neurons mature faster than adult‐born neurons (which peak at 3 weeks). Collectively, our findings are relevant for understanding how developmentally‐born DG neurons contribute to memory and disorders throughout the lifespan. High levels of early survival and zif268 expression may promote learning, while also rendering neurons sensitive to insults at defined stages. Late neuronal death in young adulthood may result in the loss of hundreds of thousands of DG neurons, which could impact memory persistence and contribute to hippocampal/DG atrophy in disorders such as depression.
Hippocampus – Wiley
Published: Nov 1, 2017
Keywords: ; ; ; ;
Read and print from thousands of top scholarly journals.
Already have an account? Log in
Bookmark this article. You can see your Bookmarks on your DeepDyve Library.
To save an article, log in first, or sign up for a DeepDyve account if you don’t already have one.
Copy and paste the desired citation format or use the link below to download a file formatted for EndNote
Access the full text.
Sign up today, get DeepDyve free for 14 days.
All DeepDyve websites use cookies to improve your online experience. They were placed on your computer when you launched this website. You can change your cookie settings through your browser.