Functional differentiation of adult-born neurons along the septotemporal axis of the dentate gyrus.

Over the past several decades, the proliferation and integration of adult-born neurons into existing hippocampal circuitry has been implicated in a wide range of behaviors, including novelty recognition, pattern separation, spatial learning, anxiety behaviors, and antidepressant response. In this review, we suggest that the diversity in behavioral requirements for new neurons may be partly caused by separate functional roles of individual neurogenic niches. Growing evidence shows that the hippocampal formation can be compartmentalized not only along the classic trisynaptic circuit, but also along a longitudinal septotemporal axis. We suggest that subpopulations of hippocampal adult-born neurons may be specialized for distinct mnemonic- or mood-related behavioral tasks. We will examine the literature supporting a functional and anatomical dissociation of the hippocampus along the longitudinal axis and discuss techniques to functionally dissect the roles of adult-born hippocampal neurons in these distinct subregions.

[1]  D. Abrous,et al.  A new chapter in the field of memory: adult hippocampal neurogenesis , 2011, The European journal of neuroscience.

[2]  F. Gage,et al.  Resolving New Memories: A Critical Look at the Dentate Gyrus, Adult Neurogenesis, and Pattern Separation , 2011, Neuron.

[3]  C. Belzung,et al.  Neurogenesis along the septo-temporal axis of the hippocampus: Are depression and the action of antidepressants region-specific? , 2013, Neuroscience.

[4]  R. Hen,et al.  Neurogenesis and affective disorders , 2011, The European journal of neuroscience.

[5]  Eric J. Nestler,et al.  Chronic Antidepressant Treatment Increases Neurogenesis in Adult Rat Hippocampus , 2000, The Journal of Neuroscience.

[6]  F. Gage,et al.  New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? , 2010, Nature Reviews Neuroscience.

[7]  Jacob Raber,et al.  Radiation-Induced Cognitive Impairments are Associated with Changes in Indicators of Hippocampal Neurogenesis , 2004, Radiation research.

[8]  D. Amaral,et al.  Entorhinal cortex of the rat: Topographic organization of the cells of origin of the perforant path projection to the dentate gyrus , 1998, The Journal of comparative neurology.

[9]  Natalie L. Trent,et al.  The ventral hippocampus and the lateral septum work in tandem to regulate rats' open-arm exploration in the elevated plus-maze , 2010, Physiology & Behavior.

[10]  M. Drew,et al.  4‐ to 6‐week‐old adult‐born hippocampal neurons influence novelty‐evoked exploration and contextual fear conditioning , 2012, Hippocampus.

[11]  E. Maguire,et al.  London taxi drivers and bus drivers: A structural MRI and neuropsychological analysis , 2006, Hippocampus.

[12]  S. Tonegawa,et al.  Young Dentate Granule Cells Mediate Pattern Separation, whereas Old Granule Cells Facilitate Pattern Completion , 2012, Cell.

[13]  Arthur W. Toga,et al.  Genomic–anatomic evidence for distinct functional domains in hippocampal field CA1 , 2009, Proceedings of the National Academy of Sciences.

[14]  Diano F. Marrone,et al.  Location is everything: Neurons born during fluoxetine treatment accumulate in regions that do not support spatial learning , 2012, Neuropharmacology.

[15]  J. Cryan,et al.  Blockade of the GABAB receptor increases neurogenesis in the ventral but not dorsal adult hippocampus: Relevance to antidepressant action , 2012, Neuropharmacology.

[16]  A. Ylinen,et al.  Reciprocal Connections between the Amygdala and the Hippocampal Formation, Perirhinal Cortex, and Postrhinal Cortex in Rat: A Review , 2000, Annals of the New York Academy of Sciences.

[17]  W. Cowan,et al.  An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat , 1977, The Journal of comparative neurology.

[18]  Fred H. Gage,et al.  Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice , 2003, Development.

[19]  J. Qiao,et al.  PG13 Packaging Cells Produce Recombinant Retroviruses Carrying a Diphtheria Toxin Mutant Which Kills Cancer Cells , 2002, Journal of Virology.

[20]  F. Gage,et al.  Mechanisms and Functional Implications of Adult Neurogenesis , 2008, Cell.

[21]  R. Hen,et al.  Effects of adult‐generated granule cells on coordinated network activity in the dentate gyrus , 2012, Hippocampus.

[22]  L. Galea,et al.  Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats , 2010, Neuroscience.

[23]  J. Altman,et al.  Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats , 1965, The Journal of comparative neurology.

[24]  R. Hen,et al.  Requirement of Hippocampal Neurogenesis for the Behavioral Effects of Antidepressants , 2003, Science.

[25]  Karl J. Friston,et al.  Segregating the functions of human hippocampus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  S. Korsmeyer,et al.  Essential role of BAX,BAK in B cell homeostasis and prevention of autoimmune disease. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[27]  C. Belzung,et al.  Differential environmental regulation of neurogenesis along the septo-temporal axis of the hippocampus , 2012, Neuropharmacology.

[28]  T. Hafting,et al.  Finite Scale of Spatial Representation in the Hippocampus , 2008, Science.

[29]  E. D. Leonardo,et al.  Adolescent but not adult-born neurons are critical for susceptibility to chronic social defeat , 2014, Front. Behav. Neurosci..

[30]  Allan R. Jones,et al.  A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing , 2012, Nature Neuroscience.

[31]  F. Gage,et al.  Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo , 1996, Nature.

[32]  F. Gage,et al.  Retrovirus-mediated single-cell gene knockout technique in adult newborn neurons in vivo , 2006, Nature Protocols.

[33]  H. Sackeim,et al.  Necessity of Hippocampal Neurogenesis for the Therapeutic Action of Antidepressants in Adult Nonhuman Primates , 2011, PloS one.

[34]  R. Hen,et al.  Beneficial behavioural and neurogenic effects of agomelatine in a model of depression/anxiety. , 2012, The international journal of neuropsychopharmacology.

[35]  H. Cameron,et al.  Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle , 2007, The Journal of comparative neurology.

[36]  Hannu J. Aronen,et al.  Psychopathy and the posterior hippocampus , 2001, Behavioural Brain Research.

[37]  David J. Anderson,et al.  Reversible Silencing of Neuronal Excitability in Behaving Mice by a Genetically Targeted, Ivermectin-Gated Cl− Channel , 2007, Neuron.

[38]  Jason S. Snyder,et al.  Inhibition of neurogenesis interferes with hippocampus‐dependent memory function , 2006, Hippocampus.

[39]  S. Jinno Topographic differences in adult neurogenesis in the mouse hippocampus: A stereology‐based study using endogenous markers , 2011, Hippocampus.

[40]  R. Hen,et al.  The current state of the neurogenic theory of depression and anxiety , 2015, Current Opinion in Neurobiology.

[41]  F. Gage,et al.  Development of neural circuits in the adult hippocampus. , 2009, Current topics in developmental biology.

[42]  N. Sousa,et al.  Mapping cellular gains and losses in the postnatal dentate gyrus: Implications for psychiatric disorders , 2006, Experimental Neurology.

[43]  D. Lowenstein,et al.  Seizure-induced neurogenesis: are more new neurons good for an adult brain? , 2002, Progress in brain research.

[44]  A. F. Schinder,et al.  Requirement of adult-born neurons for hippocampus-dependent learning , 2012, Behavioural Brain Research.

[45]  S. Becker,et al.  A model of hippocampal neurogenesis in memory and mood disorders , 2007, Trends in Cognitive Sciences.

[46]  Allan R. Jones,et al.  Genomic Anatomy of the Hippocampus , 2008, Neuron.

[47]  A. Fenton,et al.  Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation , 2011, Nature.

[48]  R. J. McDonald,et al.  Dorsal/ventral hippocampus, fornix, and conditioned place preference , 2001, Hippocampus.

[49]  N. Sousa,et al.  Epigenetic (de)regulation of adult hippocampal neurogenesis: implications for depression , 2011, Clinical Epigenetics.

[50]  Suzanne Wood,et al.  Reduced posterior hippocampal volume in posttraumatic stress disorder. , 2008, The Journal of clinical psychiatry.

[51]  N. Torquet,et al.  Activation of adult-born neurons facilitates learning and memory , 2012, Nature Neuroscience.

[52]  Kwang-Soo Kim,et al.  Functional neurogenesis in the adult midbrain , 2006 .

[53]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[54]  Mi-Sung Kim,et al.  Functional and mechanistic exploration of an adult neurogenesis‐promoting small molecule , 2012, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[55]  Ryoichiro Kageyama,et al.  Temporal regulation of Cre recombinase activity in neural stem cells , 2006, Genesis.

[56]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[57]  A. F. Schinder,et al.  The Timing for Neuronal Maturation in the Adult Hippocampus Is Modulated by Local Network Activity , 2011, Journal of Neuroscience.

[58]  M. N. Rajah,et al.  Group differences in anterior hippocampal volume and in the retrieval of spatial and temporal context memory in healthy young versus older adults , 2010, Neuropsychologia.

[59]  J. Rawlins,et al.  Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. , 2002, Behavioral neuroscience.

[60]  G. Teuchert-Noodt,et al.  Adult treatment with haloperidol increases dentate granule cell proliferation in the gerbil hippocampus , 1998, Journal of Neural Transmission.

[61]  P. Frankland,et al.  Suppression of adult neurogenesis impairs population coding of similar contexts in hippocampal CA3 region , 2012, Nature Communications.

[62]  K O Lim,et al.  Anterior hippocampal volume deficits in nonamnesic, aging chronic alcoholics. , 1995, Alcoholism, clinical and experimental research.

[63]  Ove Wiborg,et al.  Hippocampal Cytogenesis Correlates to Escitalopram-Mediated Recovery in a Chronic Mild Stress Rat Model of Depression , 2006, Neuropsychopharmacology.

[64]  R. Cuppini,et al.  Spatial learning affects immature granule cell survival in adult rat dentate gyrus , 2000, Neuroscience Letters.

[65]  F. Gage,et al.  Neurons born in the adult dentate gyrus form functional synapses with target cells , 2008, Nature Neuroscience.

[66]  E. D. Kirby,et al.  Acute stress enhances adult rat hippocampal neurogenesis and activation of newborn neurons via secreted astrocytic FGF2 , 2013, eLife.

[67]  Tom den Heijer,et al.  Hippocampal Head Size Associated with Verbal Memory Performance in Nondemented Elderly , 2002, NeuroImage.

[68]  E. Gould,et al.  Dominance Hierarchy Influences Adult Neurogenesis in the Dentate Gyrus , 2004, The Journal of Neuroscience.

[69]  A. Fenton,et al.  Adult‐born hippocampal neurons promote cognitive flexibility in mice , 2012, Hippocampus.

[70]  Gang Chen,et al.  Contextual Fear Conditioning in Humans: Cortical-Hippocampal and Amygdala Contributions , 2008, The Journal of Neuroscience.

[71]  C. Rampon,et al.  Long-Term Potentiation Enhances Neurogenesis in the Adult Dentate Gyrus , 2006, The Journal of Neuroscience.

[72]  G. Bedi,et al.  Impact of Social Status and Antidepressant Treatment on Neurogenesis in the Baboon Hippocampus , 2014, Neuropsychopharmacology.

[73]  G. Fishell,et al.  Tanycytes of the Hypothalamic Median Eminence Form a Diet-Responsive Neurogenic Niche , 2012, Nature Neuroscience.

[74]  René Hen,et al.  Serotonin receptor expression along the dorsal–ventral axis of mouse hippocampus , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[75]  Hongjun Song,et al.  Localized CT-Guided Irradiation Inhibits Neurogenesis in Specific Regions of the Adult Mouse Brain , 2011, Radiation research.

[76]  M. Héry,et al.  Agomelatine, a New Antidepressant, Induces Regional Changes in Hippocampal Neurogenesis , 2006, Biological Psychiatry.

[77]  R. Hen,et al.  Drug-Dependent Requirement of Hippocampal Neurogenesis in a Model of Depression and of Antidepressant Reversal , 2008, Biological Psychiatry.

[78]  Carol A Barnes,et al.  Integration of New Neurons into Functional Neural Networks , 2006, The Journal of Neuroscience.

[79]  R. Hen,et al.  Molecular heterogeneity along the dorsal–ventral axis of the murine hippocampal CA1 field: a microarray analysis of gene expression , 2006, Neuroscience.

[80]  C. Belzung,et al.  Neurogenesis-Independent Antidepressant-Like Effects on Behavior and Stress Axis Response of a Dual Orexin Receptor Antagonist in a Rodent Model of Depression , 2012, Neuropsychopharmacology.

[81]  G. Buzsáki,et al.  Distinct Representations and Theta Dynamics in Dorsal and Ventral Hippocampus , 2010, The Journal of Neuroscience.

[82]  R. Hen,et al.  Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders , 2012, Nature Neuroscience.

[83]  M. Drew,et al.  Neurogenesis-Dependent and -Independent Effects of Fluoxetine in an Animal Model of Anxiety/Depression , 2009, Neuron.

[84]  Rene Hen,et al.  Young and excitable: the function of new neurons in the adult mammalian brain , 2005, Current Opinion in Neurobiology.

[85]  A. Eisch,et al.  Epigenetics, hippocampal neurogenesis, and neuropsychiatric disorders: Unraveling the genome to understand the mind , 2010, Neurobiology of Disease.

[86]  F. Gage,et al.  Genetic influence on neurogenesis in the dentate gyrus of adult mice. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[87]  W M Cowan,et al.  Quantitative, three‐dimensional analysis of granule cell dendrites in the rat dentate gyrus , 1990, The Journal of comparative neurology.

[88]  Takeshi Izumi,et al.  The Serotonergic Projection from the Median Raphe Nucleus to the Ventral Hippocampus is Involved in the Retrieval of Fear Memory Through the Corticotropin-Releasing Factor Type 2 Receptor , 2010, Neuropsychopharmacology.

[89]  A. Malhotra,et al.  Increased stress and smaller anterior hippocampal volume , 2006, Neuroreport.

[90]  D. Amaral,et al.  The three-dimensional organization of the hippocampal formation: A review of anatomical data , 1989, Neuroscience.

[91]  John K. Robinson,et al.  Changes in hippocampal morphology following chronic treatment with the synthetic cannabinoid WIN 55,212-2 , 2000, Brain Research.

[92]  A. Eisch,et al.  The neurogenesis hypothesis of affective and anxiety disorders: Are we mistaking the scaffolding for the building? , 2012, Neuropharmacology.

[93]  G. Kempermann,et al.  Adult‐born hippocampal neurons mature into activity‐dependent responsiveness , 2003, The European journal of neuroscience.

[94]  W. A. Wilson,et al.  Potassium-induced epileptiform activity in area CA3 varies markedly along the septotemporal axis of the rat hippocampus , 1986, Brain Research.

[95]  L. Seress,et al.  Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. , 1981, Journal of anatomy.

[96]  E. McAuley,et al.  Exercise training increases size of hippocampus and improves memory , 2011, Proceedings of the National Academy of Sciences.

[97]  P. Schwartzkroin,et al.  Axon arbors and synaptic connections of hippocampal mossy cells in the rat in vivo , 1996, The Journal of comparative neurology.

[98]  Jason S. Snyder,et al.  Late Maturation of Adult-Born Neurons in the Temporal Dentate Gyrus , 2012, PloS one.

[99]  J. García-Verdugo,et al.  Adult‐derived neural precursors transplanted into multiple regions in the adult brain , 1999, Annals of neurology.

[100]  Stephen Maren,et al.  Hippocampus and Pavlovian fear conditioning in rats: muscimol infusions into the ventral, but not dorsal, hippocampus impair the acquisition of conditional freezing to an auditory conditional stimulus. , 2004, Behavioral neuroscience.

[101]  H Eichenbaum,et al.  Afferent connections of the perirhinal cortex in the rat , 1983, The Journal of comparative neurology.

[102]  Jason S. Snyder,et al.  Anatomical gradients of adult neurogenesis and activity: Young neurons in the ventral dentate gyrus are activated by water maze training , 2009, Hippocampus.

[103]  T. Kosaka,et al.  Stereological estimation of numerical densities of glutamatergic principal neurons in the mouse hippocampus , 2009, Hippocampus.

[104]  G. Ming,et al.  Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions , 2011, Neuron.

[105]  D. Abrous,et al.  Interaction between Neurogenesis and Hippocampal Memory System: New Vistas. , 2015, Cold Spring Harbor perspectives in biology.

[106]  B. McNaughton,et al.  Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience , 2005, Hippocampus.

[107]  P. Frankland,et al.  Posttraining Ablation of Adult-Generated Neurons Degrades Previously Acquired Memories , 2011, The Journal of Neuroscience.

[108]  Morris Moscovitch,et al.  A Hippocampal Marker of Recollection Memory Ability among Healthy Young Adults: Contributions of Posterior and Anterior Segments , 2011, Neuron.

[109]  R. Racine,et al.  Epileptiform burst responses in ventral vs dorsal hippocampal slices , 1985, Brain Research.

[110]  C. Shively,et al.  Behavioral and neurobiological characteristics of social stress versus depression in nonhuman primates , 2012, Experimental Neurology.

[111]  M. Glickstein,et al.  Afferent and Efferent Connections of Temporal Association Cortex in the Rat: A Horseradish Peroxidase Study , 1991, The European journal of neuroscience.

[112]  R. Hen,et al.  Experience Dictates Stem Cell Fate in the Adult Hippocampus , 2011, Neuron.

[113]  Ethan M. Goldberg,et al.  Smaller anterior hippocampal formation volume in antipsychotic-naive patients with first-episode schizophrenia. , 2003, The American journal of psychiatry.

[114]  Janet Wiles,et al.  Potential role for adult neurogenesis in the encoding of time in new memories , 2006, Nature Neuroscience.

[115]  L. Swanson,et al.  Analysis of direct hippocampal cortical field CA1 axonal projections to diencephalon in the rat , 2006, The Journal of comparative neurology.

[116]  K. Deisseroth,et al.  Circuit-breakers: optical technologies for probing neural signals and systems , 2007, Nature Reviews Neuroscience.

[117]  L. Saksida,et al.  A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation , 2009, Science.

[118]  R. Gross,et al.  Differences in hippocampal mitotic activity within the dorsal and ventral hippocampus following flurothyl seizures in mice , 2002, Neuroscience Letters.

[119]  R. Hen,et al.  Functional dissociation of adult‐born neurons along the dorsoventral axis of the dentate gyrus , 2014, Hippocampus.

[120]  G. Kempermann,et al.  Adult-Generated Hippocampal Neurons Allow the Flexible Use of Spatially Precise Learning Strategies , 2009, PloS one.

[121]  M. Moser,et al.  Reduced fear expression after lesions of the ventral hippocampus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[122]  B. McNaughton,et al.  Comparison of spatial firing characteristics of units in dorsal and ventral hippocampus of the rat , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[123]  T. Freund,et al.  Distribution, ultrastructure, and connectivity of calretinin‐immunoreactive mossy cells of the mouse dentate gyrus , 1997, Hippocampus.

[124]  Hongkui Zeng,et al.  Differential Control of Learning and Anxiety along the Dorsoventral Axis of the Dentate Gyrus , 2013, Neuron.

[125]  Nicola Maggio,et al.  Unique regulation of long term potentiation in the rat ventral hippocampus , 2007, Hippocampus.

[126]  F. Gage,et al.  Functional neurogenesis in the adult hippocampus , 2002, Nature.

[127]  T. Kosaka,et al.  Patterns of expression of neuropeptides in GABAergic nonprincipal neurons in the mouse hippocampus: Quantitative analysis with optical disector , 2003, The Journal of comparative neurology.

[128]  Chunmei Zhao,et al.  Functional Convergence of Neurons Generated in the Developing and Adult Hippocampus , 2006, PLoS biology.

[129]  C. Bardy,et al.  How, When, and Where New Inhibitory Neurons Release Neurotransmitters in the Adult Olfactory Bulb , 2010, Journal of Neuroscience.

[130]  F. Gage,et al.  Experience-Specific Functional Modification of the Dentate Gyrus through Adult Neurogenesis: A Critical Period during an Immature Stage , 2007, The Journal of Neuroscience.

[131]  C. Brock Kirwan,et al.  A possible negative influence of depression on the ability to overcome memory interference , 2013, Behavioural Brain Research.

[132]  I. Iordachita,et al.  CT Guidance is Needed to Achieve Reproducible Positioning of the Mouse Head for Repeat Precision Cranial Irradiation , 2010, Radiation research.

[133]  E. Tulving,et al.  Hippocampal PET activations of memory encoding and retrieval: The HIPER model , 1998, Hippocampus.

[134]  Joseph E LeDoux,et al.  Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. , 1992, Behavioral neuroscience.

[135]  Fred H. Gage,et al.  Endogenous norepinephrine and serotonin within the hippocampal formation during the development and recovery from septal hyperractivity , 1978, Pharmacology Biochemistry and Behavior.

[136]  Peter Kazanzides,et al.  High-resolution, small animal radiation research platform with x-ray tomographic guidance capabilities. , 2008, International journal of radiation oncology, biology, physics.

[137]  H. Nielsen,et al.  Transcriptome differentiation along the dorso–ventral axis in laser-captured microdissected rat hippocampal granular cell layer , 2010, Neuroscience.

[138]  C. Greer,et al.  Dynamic Contribution of Nestin-Expressing Stem Cells to Adult Neurogenesis , 2007, The Journal of Neuroscience.

[139]  Arturo Alvarez-Buylla,et al.  Mosaic Organization of Neural Stem Cells in the Adult Brain , 2007, Science.

[140]  T. Ohtsuka,et al.  Continuous neurogenesis in the adult brain , 2009, Development, growth & differentiation.

[141]  K. Sung,et al.  Regional differences in enhanced neurogenesis in the dentate gyrus of adult rats after transient forebrain ischemia. , 2003, Molecules and cells.

[142]  M. Witter,et al.  Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region , 1989, Progress in Neurobiology.

[143]  T. Kosaka,et al.  Quantitative analysis of GABAergic neurons in the mouse hippocampus, with optical disector using confocal laser scanning microscope , 1998, Brain Research.

[144]  T. Kosaka,et al.  Ionic currents underlying rhythmic bursting of ventral mossy cells in the developing mouse dentate gyrus , 2003, The European journal of neuroscience.

[145]  Suzanna Becker,et al.  Adult hippocampal neurogenesis reduces memory interference in humans: opposing effects of aerobic exercise and depression , 2013, Front. Neurosci..

[146]  Roy G. Thompson,et al.  Differential distribution of norepinephrine and serotonin along the dorsal-ventral axis of the hippocampal formation , 1980, Brain Research Bulletin.

[147]  Rene Hen,et al.  Adult hippocampal neurogenesis in depression , 2007, Nature Neuroscience.

[148]  Karen L. Smith,et al.  Structural and functional asymmetry in the normal and epileptic rat dentate gyrus , 2002, The Journal of comparative neurology.

[149]  L. Swanson,et al.  Spatial organization of direct hippocampal field CA1 axonal projections to the rest of the cerebral cortex , 2007, Brain Research Reviews.

[150]  F. Gage,et al.  Gene Expression Profiling of Neural Stem Cells and Their Neuronal Progeny Reveals IGF2 as a Regulator of Adult Hippocampal Neurogenesis , 2012, The Journal of Neuroscience.

[151]  Z. Qiu,et al.  The epigenetic switches for neural development and psychiatric disorders. , 2013, Journal of genetics and genomics = Yi chuan xue bao.

[152]  REGIONAL DIFFERENCES IN THE HIPPOCAMPUS OF THE CAT. I. SPECIFIC DISCHARGE PATTERNS OF THE DORSAL AND VENTRAL HIPPOCAMPUS AND THEIR ROLE IN GENERALIZED SEIZURES. , 1964, Electroencephalography and clinical neurophysiology.

[153]  W. Wurst,et al.  A powerful transgenic tool for fate mapping and functional analysis of newly generated neurons , 2010, BMC Neuroscience.

[154]  S. Ge,et al.  A Critical Period for Enhanced Synaptic Plasticity in Newly Generated Neurons of the Adult Brain , 2007, Neuron.

[155]  M. Boldrini,et al.  Hippocampal Angiogenesis and Progenitor Cell Proliferation Are Increased with Antidepressant Use in Major Depression , 2012, Biological Psychiatry.

[156]  G. Sperk,et al.  Regional heterogeneity in the distribution of neurotransmitter markers in the rat hippocampus , 1991, Neuroscience.

[157]  T. Hökfelt,et al.  Enhanced hippocampal noradrenaline and serotonin release in galanin-overexpressing mice after repeated forced swimming test , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[158]  William B. Levy,et al.  Granule cell dendritic spine density in the rat hippocampus varies with spine shape and location , 1985, Neuroscience Letters.

[159]  H. Cameron,et al.  Adrenal hormones suppress cell division in the adult rat dentate gyrus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[160]  D. Amaral,et al.  Perirhinal and postrhinal cortices of the rat: Interconnectivity and connections with the entorhinal cortex , 1998, The Journal of comparative neurology.

[161]  A. F. Schinder,et al.  Neuronal Differentiation in the Adult Hippocampus Recapitulates Embryonic Development , 2005, The Journal of Neuroscience.