Old Dogs Learning New Tricks: Neuroplasticity Beyond the Juvenile Period.

Twenty years ago, the prevalent view in psychology was that although learning and the formation of new memories are lifelong occurrences, the neural changes associated with these events were all in the existing receptors. No new neural hardware, from synapses to neurons, was thought to appear after a protracted period early in life. In the past 20 years, another view has supplanted this one, showing that although the juvenile period is especially suited to neuroplastic adaptation, there is hard neuroplastic change later in life as well. We review a selection of evidence for this view from both animal and human models, showing how it reflects three principles of neuroplasticity: 1) earlier and later experience-induced changes to neuroarchitecture differ in degree more so than in type; 2) the types of experiences that lead to neuroplastic change narrow with age; and 3) differences in the amenability of neural circuitry to change result from basic differences in neuroarchitecture and neuroenvironment in different phases of development.

[1]  S. Weiss,et al.  Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. , 1992, Science.

[2]  P. Lledo,et al.  Integrating new neurons into the adult olfactory bulb: joining the network, life–death decisions, and the effects of sensory experience , 2005, Trends in Neurosciences.

[3]  P. Kuhl,et al.  Foreign-language experience in infancy: Effects of short-term exposure and social interaction on phonetic learning , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[4]  E. Gould,et al.  Neurogenesis in the Dentate Gyrus of the Adult Tree Shrew Is Regulated by Psychosocial Stress and NMDA Receptor Activation , 1997, The Journal of Neuroscience.

[5]  T. Hensch Critical period regulation. , 2004, Annual review of neuroscience.

[6]  Jonathan R. Whitlock,et al.  Learning Induces Long-Term Potentiation in the Hippocampus , 2006, Science.

[7]  Mohamed Sabaawi,et al.  Book Review: The Mind and the Brain: Neuroplasticity and the Power of Mental Force. By Jeffrey M. Schwartz and Sharon Begley. New York, NY: HarperCollins Publishers, Inc. , 2004 .

[8]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[9]  C. Büchel,et al.  Temporal and Spatial Dynamics of Brain Structure Changes during Extensive Learning , 2006, The Journal of Neuroscience.

[10]  M. Poo,et al.  Propagation of activity-dependent synaptic depression in simple neural networks , 1997, Nature.

[11]  D. Bavelier,et al.  Neural organization and plasticity of language , 1998, Current Opinion in Neurobiology.

[12]  Michael J Meaney,et al.  Neurodevelopmental sequelae of postnatal maternal care in rodents: clinical and research implications of molecular insights. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[13]  Stephen M. Smith,et al.  Age-related changes in grey and white matter structure throughout adulthood , 2010, NeuroImage.

[14]  J. Hirsch,et al.  Distinct cortical areas associated with native and second languages , 1997, Nature.

[15]  L. C. Klein,et al.  Behavioral responses to physical vs. social novelty in male and female laboratory rats , 2011, Behavioural Processes.

[16]  E. Jarvis,et al.  Learned Birdsong and the Neurobiology of Human Language , 2004, Annals of the New York Academy of Sciences.

[17]  Takao K. Hensch,et al.  Lynx1, a Cholinergic Brake, Limits Plasticity in Adult Visual Cortex , 2010, Science.

[18]  Naomi B. Pitskel,et al.  Rapid and Reversible Recruitment of Early Visual Cortex for Touch , 2008, PloS one.

[19]  H. Ohki‐Hamazaki,et al.  Demonstration of a Neural Circuit Critical for Imprinting Behavior in Chicks , 2010, The Journal of Neuroscience.

[20]  A. Senghas,et al.  Children Creating Core Properties of Language: Evidence from an Emerging Sign Language in Nicaragua , 2004, Science.

[21]  A. Decasper,et al.  Prenatal maternal speech influences newborns' perception of speech sounds , 1986 .

[22]  Christian Büchel,et al.  Training-Induced Brain Structure Changes in the Elderly , 2008, The Journal of Neuroscience.

[23]  Eric I Knudsen,et al.  Anatomical traces of juvenile learning in the auditory system of adult barn owls , 2005, Nature Neuroscience.

[24]  C. Gilbert,et al.  Axons and Synaptic Boutons Are Highly Dynamic in Adult Visual Cortex , 2006, Neuron.

[25]  A. Parent,et al.  Newly generated neurons in the amygdala and adjoining cortex of adult primates , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[26]  W. Greenough,et al.  Experience-driven brain plasticity: beyond the synapse. , 2004, Neuron glia biology.

[27]  André Parent,et al.  Evidence of newly generated neurons in the human olfactory bulb. , 2004, Brain research. Developmental brain research.

[28]  A. Glenberg,et al.  Processing Abstract Language Modulates Motor System Activity , 2008, Quarterly journal of experimental psychology.

[29]  M. Bear,et al.  Modulation of Long-Term Synaptic Depression in Visual Cortex by Acetylcholine and Norepinephrine , 1999, The Journal of Neuroscience.

[30]  R. DeTeresa,et al.  Neocortical cell counts in normal human adult aging , 1987, Annals of neurology.

[31]  D. Feldman Synaptic mechanisms for plasticity in neocortex. , 2009, Annual review of neuroscience.

[32]  J. Kaas,et al.  Injury-induced reorganization of somatosensory cortex is accompanied by reductions in GABA staining. , 1991, Somatosensory & motor research.

[33]  Eric I. Knudsen,et al.  Adaptive auditory plasticity in developing and adult animals , 2007, Progress in Neurobiology.

[34]  M. Feller,et al.  Mechanisms underlying development of visual maps and receptive fields. , 2008, Annual review of neuroscience.

[35]  P. Haydon Glia: listening and talking to the synapse , 2001, Nature Reviews Neuroscience.

[36]  F. Rösler,et al.  Speech processing activates visual cortex in congenitally blind humans , 2002, The European journal of neuroscience.

[37]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[38]  A. Huberman Mammalian DSCAMs: They Won't Help You Find a Partner, but They'll Guarantee You Some Personal Space , 2009, Neuron.

[39]  M. Mishkin,et al.  Massive cortical reorganization after sensory deafferentation in adult macaques. , 1991, Science.

[40]  T. Teyler Long-term potentiation and memory. , 1987, International journal of neurology.

[41]  E G Jones,et al.  Thalamic and brainstem contributions to large-scale plasticity of primate somatosensory cortex. , 1998, Science.

[42]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[43]  Elizabeth Gould,et al.  Is there a link between adult neurogenesis and learning? , 2006, Hippocampus.

[44]  T. Elbert,et al.  Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation , 1995, Nature.

[45]  Ione Fine,et al.  Visual stimuli activate auditory cortex in the deaf , 2001, Nature Neuroscience.

[46]  Eric J. Warrant,et al.  Visual training improves underwater vision in children , 2006, Vision Research.

[47]  K. Svoboda,et al.  Spine growth precedes synapse formation in the adult neocortex in vivo , 2006, Nature Neuroscience.

[48]  D. Maurer,et al.  Multiple sensitive periods in human visual development: evidence from visually deprived children. , 2005, Developmental psychobiology.

[49]  Bogdan Draganski,et al.  Neuroplasticity: Changes in grey matter induced by training , 2004, Nature.

[50]  J. Disterhoft,et al.  Associative Learning Elicits the Formation of Multiple-Synapse Boutons , 2001, The Journal of Neuroscience.

[51]  Veronique D. Bohbot,et al.  Maze training in mice induces MRI-detectable brain shape changes specific to the type of learning , 2011, NeuroImage.

[52]  Henriette van Praag,et al.  Neurogenesis and Exercise: Past and Future Directions , 2008, NeuroMolecular Medicine.

[53]  C. Lois,et al.  Long-distance neuronal migration in the adult mammalian brain. , 1994, Science.

[54]  P. Rakić,et al.  Continuation of neurogenesis in the hippocampus of the adult macaque monkey. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[55]  T. Wiesel,et al.  Receptive field dynamics in adult primary visual cortex , 1992, Nature.

[56]  R. McKay,et al.  Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus , 2001, The Journal of comparative neurology.

[57]  M. Simmel PHANTOM EXPERIENCES FOLLOWING AMPUTATION IN CHILDHOOD , 1962, Journal of neurology, neurosurgery, and psychiatry.

[58]  W. Singer,et al.  Modulation of visual cortical plasticity by acetylcholine and noradrenaline , 1986, Nature.

[59]  K M Harris,et al.  Stability in Synapse Number and Size at 2 Hr after Long-Term Potentiation in Hippocampal Area CA1 , 1998, The Journal of Neuroscience.

[60]  F. Gage,et al.  Adult‐generated neurons in the dentate gyrus send axonal projections to field CA3 and are surrounded by synaptic vesicles , 1999, The Journal of comparative neurology.

[61]  Eleanor A. Maguire,et al.  Navigational expertise may compromise anterograde associative memory , 2009, Neuropsychologia.

[62]  D. Hubel,et al.  Extent of recovery from the effects of visual deprivation in kittens. , 1965, Journal of neurophysiology.

[63]  D. Pisoni,et al.  Training Japanese listeners to identify English /r/and /l/: Long-term retention of learning in perception and production , 1999, Perception & psychophysics.

[64]  L. Cohen,et al.  Neuroplasticity in the context of motor rehabilitation after stroke , 2011, Nature Reviews Neurology.

[65]  Sandra Blakeslee,et al.  Phantoms in the Brain , 1998 .

[66]  Janet F. Werker,et al.  Cross-Language Speech Perception : Initial Capabilities and Developmental Change , 2001 .

[67]  G. Bartzokis,et al.  Age-related changes in frontal and temporal lobe volumes in men: a magnetic resonance imaging study. , 2001, Archives of general psychiatry.

[68]  Hugo J Spiers,et al.  Talent in the taxi: a model system for exploring expertise , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[69]  C D Gilbert,et al.  Circuitry, architecture, and functional dynamics of visual cortex. , 1993, Cerebral cortex.

[70]  Agatha D. Lee,et al.  Genetics of Brain Fiber Architecture and Intellectual Performance , 2009, The Journal of Neuroscience.

[71]  M. Just,et al.  Altering Cortical Connectivity: Remediation-Induced Changes in the White Matter of Poor Readers , 2009, Neuron.

[72]  Bryan Kolb,et al.  Experience-dependent changes in dendritic arbor and spine density in neocortex vary qualitatively with age and sex , 2003, Neurobiology of Learning and Memory.

[73]  Li I. Zhang,et al.  Persistent and specific influences of early acoustic environments on primary auditory cortex , 2001, Nature Neuroscience.

[74]  Elizabeth Gould,et al.  Structural plasticity and hippocampal function. , 2010, Annual review of psychology.

[75]  Christian Büchel,et al.  Changes in Gray Matter Induced by Learning—Revisited , 2008, PloS one.

[76]  E. Knudsen Fundamental components of attention. , 2007, Annual review of neuroscience.

[77]  Frances A Champagne,et al.  Epigenetic influences on brain development and plasticity , 2009, Current Opinion in Neurobiology.

[78]  Karl J. Friston,et al.  Different activation patterns in the visual cortex of late and congenitally blind subjects. , 1998, Brain : a journal of neurology.

[79]  V. Ramachandran,et al.  Behavioral and magnetoencephalographic correlates of plasticity in the adult human brain. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[80]  Heidi Johansen-Berg,et al.  Behavioural relevance of variation in white matter microstructure. , 2010, Current opinion in neurology.

[81]  M. Bear,et al.  Bidirectional synaptic mechanisms of ocular dominance plasticity in visual cortex , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[82]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[83]  Stefan Skare,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Extensive Blockinpiano Blockinpracticing Blockinhas Blockinregionally Specific Blockineffects Blockinon Blockinwhite Blockinmatter Blockindevelopment , 2022 .

[84]  I. Robertson,et al.  Rehabilitation of brain damage: brain plasticity and principles of guided recovery. , 1999, Psychological bulletin.

[85]  T. Krahe,et al.  Neocortical plasticity deficits in fetal alcohol spectrum disorders: Lessons from barrel and visual cortex , 2008, Journal of neuroscience research.

[86]  L. Westlye,et al.  Associations between regional cortical thickness and attentional networks as measured by the attention network test. , 2011, Cerebral cortex.

[87]  G. Ellis‐Davies,et al.  Structural basis of long-term potentiation in single dendritic spines , 2004, Nature.

[88]  B. Mcewen,et al.  Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[89]  C. Rampon,et al.  New neurons in the dentate gyrus are involved in the expression of enhanced long‐term memory following environmental enrichment , 2005, The European journal of neuroscience.

[90]  M. Rutter,et al.  Are there biological programming effects for psychological development? Findings from a study of Romanian adoptees. , 2004, Developmental psychology.

[91]  M. Hallett,et al.  Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. , 1995, Journal of neurophysiology.

[92]  E. Callaway Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

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

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

[95]  V. Ramachandran,et al.  The perception of phantom limbs. The D. O. Hebb lecture. , 1998, Brain : a journal of neurology.

[96]  Michael J Meaney,et al.  Epigenetics and the biological definition of gene x environment interactions. , 2010, Child development.

[97]  C. Gilbert Adult cortical dynamics. , 1998, Physiological reviews.

[98]  Agnès Gruart,et al.  Involvement of the CA3–CA1 Synapse in the Acquisition of Associative Learning in Behaving Mice , 2006, The Journal of Neuroscience.

[99]  E. Smith,et al.  Multiple sensitive periods in the development of the primate visual system. , 1986, Science.

[100]  Mark H. Johnson,et al.  CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE New Advances in Understanding Sensitive Periods in Brain Development , 2022 .

[101]  G. Recanzone Experience-dependent plasticity , 2022 .

[102]  J. S. Johnson,et al.  Critical period effects in second language learning: The influence of maturational state on the acquisition of English as a second language , 1989, Cognitive Psychology.

[103]  S. Stephen Risk, resilience, and gene x environment interactions in rhesus monkeys , 2009 .

[104]  K. Svoboda,et al.  Experience-dependent structural synaptic plasticity in the mammalian brain , 2009, Nature Reviews Neuroscience.

[105]  P. Kuhl,et al.  Speech perception in infancy predicts language development in the second year of life: a longitudinal study. , 2004, Child development.

[106]  Kentaro Abe,et al.  Songbirds possess the spontaneous ability to discriminate syntactic rules , 2011, Nature Neuroscience.

[107]  M. Merzenich,et al.  Experience-Dependent Adult Cortical Plasticity Requires Cognitive Association between Sensation and Reward , 2006, Neuron.

[108]  E. Kandel,et al.  Molecular biology of learning: modulation of transmitter release. , 1982, Science.

[109]  K. Svoboda,et al.  Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo , 2000, Nature.

[110]  E Gould,et al.  Estrogen Stimulates a Transient Increase in the Number of New Neurons in the Dentate Gyrus of the Adult Female Rat , 1999, The Journal of Neuroscience.

[111]  E. Gould,et al.  Sleep deprivation inhibits adult neurogenesis in the hippocampus by elevating glucocorticoids , 2006, Proceedings of the National Academy of Sciences.

[112]  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.

[113]  J. Altman,et al.  Are New Neurons Formed in the Brains of Adult Mammals? , 1962, Science.

[114]  S. Maier,et al.  Exercise does not modify spatial memory, brain autoimmunity, or antibody response in aged F-344 rats , 1991, Neurobiology of Aging.

[115]  L. Merabet,et al.  The plastic human brain cortex. , 2005, Annual review of neuroscience.

[116]  D. Buonomano,et al.  Cortical plasticity: from synapses to maps. , 1998, Annual review of neuroscience.

[117]  B. Rockstroh,et al.  Increased Cortical Representation of the Fingers of the Left Hand in String Players , 1995, Science.

[118]  W. Singer Development and plasticity of cortical processing architectures. , 1995, Science.

[119]  F. Engert,et al.  Dendritic spine changes associated with hippocampal long-term synaptic plasticity , 1999, Nature.

[120]  M. Sur,et al.  Development and plasticity of cortical areas and networks , 2001, Nature Reviews Neuroscience.

[121]  T. Mexia,et al.  Author ' s personal copy , 2009 .

[122]  S. Rauch,et al.  Meditation experience is associated with increased cortical thickness , 2005, Neuroreport.

[123]  Pat Levitt,et al.  How the timing and quality of early experiences influence the development of brain architecture. , 2010, Child development.

[124]  Hans-Jochen Heinze,et al.  Experience-dependent plasticity of white-matter microstructure extends into old age , 2010, Neuropsychologia.

[125]  Bruce Fischl,et al.  Regional white matter volume differences in nondemented aging and Alzheimer's disease , 2009, NeuroImage.

[126]  C. Gross,et al.  Neurogenesis in the neocortex of adult primates. , 1999, Science.

[127]  L. C. Katz,et al.  Early development of ocular dominance columns. , 2000, Science.

[128]  M. Rosenzweig Modification of Brain Circuits through Experience , 2007 .

[129]  A. Fasolo,et al.  Neurogenesis in the Caudate Nucleus of the Adult Rabbit , 2006, The Journal of Neuroscience.

[130]  D. J. Felleman,et al.  Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation , 1983, Neuroscience.

[131]  S. Hobfoll Conservation of resources. A new attempt at conceptualizing stress. , 1989, The American psychologist.

[132]  Leslie B. Cohen,et al.  From perception to cognition , 1987 .

[133]  C. Shatz,et al.  Brain Waves and Brain Wiring: The Role of Endogenous and Sensory-Driven Neural Activity in Development , 1999, Pediatric Research.

[134]  R. Malenka The long-term potential of LTP , 2003, Nature Reviews Neuroscience.

[135]  Á. Pascual-Leone,et al.  The metamodal organization of the brain. , 2001, Progress in brain research.

[136]  P. Bach-y-Rita,et al.  Sensory substitution and the human–machine interface , 2003, Trends in Cognitive Sciences.

[137]  M. Joëls,et al.  Maternal care determines rapid effects of stress mediators on synaptic plasticity in adult rat hippocampal dentate gyrus , 2009, Neurobiology of Learning and Memory.

[138]  D. Spalding The Principles of Psychology , 1873, Nature.

[139]  David Dupret,et al.  Spatial Learning Depends on Both the Addition and Removal of New Hippocampal Neurons , 2007, PLoS biology.

[140]  J. Sanes,et al.  LTP: perils and progress , 2003, Nature Reviews Neuroscience.

[141]  W. Greenough,et al.  Experience and brain development. , 1987, Child development.

[142]  K. Svoboda,et al.  Structure and function of dendritic spines. , 2002, Annual review of physiology.

[143]  E. Bennett,et al.  Brain changes in response to experience. , 1972 .

[144]  L. Chalupa,et al.  Retinal waves are unlikely to instruct the formation of eye-specific retinogeniculate projections , 2009, Neural Development.

[145]  A. Meltzoff,et al.  Intermodal matching by human neonates , 1979, Nature.

[146]  N. Fox,et al.  Cognitive Recovery in Socially Deprived Young Children: The Bucharest Early Intervention Project , 2007, Science.

[147]  Judith M. Kearins,et al.  Visual spatial memory in Australian Aboriginal children of desert regions , 1981, Cognitive Psychology.

[148]  J. Werker,et al.  Cross-language speech perception: Evidence for perceptual reorganization during the first year of life , 1984 .

[149]  F. Fazio,et al.  Brain processing of native and foreign languages , 1996, NeuroImage.

[150]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[151]  Karel Svoboda,et al.  Structural Plasticity Underlies Experience-Dependent Functional Plasticity of Cortical Circuits , 2010, The Journal of Neuroscience.

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

[153]  J. Donoghue,et al.  Plasticity and primary motor cortex. , 2000, Annual review of neuroscience.

[154]  Luigi Cattaneo,et al.  Numbers within Our Hands: Modulation of Corticospinal Excitability of Hand Muscles during Numerical Judgment , 2007, Journal of Cognitive Neuroscience.

[155]  Adi Mizrahi,et al.  Sensory Input Enhances Synaptogenesis of Adult-Born Neurons , 2009, The Journal of Neuroscience.

[156]  K. Zentgraf,et al.  Cognitive motor processes: The role of motor imagery in the study of motor representations , 2009, Brain Research Reviews.

[157]  W. Greenough,et al.  Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[158]  J. Bourne,et al.  Do thin spines learn to be mushroom spines that remember? , 2007, Current Opinion in Neurobiology.

[159]  C. Gilbert,et al.  Axonal sprouting accompanies functional reorganization in adult cat striate cortex , 1994, Nature.

[160]  M M Merzenich,et al.  Alterations in correlated activity parallel ICMS-induced representational plasticity. , 1993, Neuroreport.

[161]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

[162]  B. Stanfield,et al.  Evidence that granule cells generated in the dentate gyrus of adult rats extend axonal projections , 2004, Experimental Brain Research.

[163]  Pico Caroni,et al.  Structural plasticity of axon terminals in the adult , 2007, Current Opinion in Neurobiology.

[164]  D. Muller,et al.  Spine dynamics and synapse remodeling during LTP and memory processes. , 2008, Progress in brain research.

[165]  V. Ramachandran,et al.  Acute plasticity in the human somatosensory cortex following amputation , 1998, Neuroreport.

[166]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[167]  W. James The Principles of Psychology, Vol. I , 2008 .

[168]  V. Schmithorst,et al.  Cognitive functions correlate with white matter architecture in a normal pediatric population: A diffusion tensor MRI study , 2005, Human brain mapping.

[169]  K. Svoboda,et al.  Cell Type-Specific Structural Plasticity of Axonal Branches and Boutons in the Adult Neocortex , 2006, Neuron.

[170]  M. Abrahamsson,et al.  Superior Underwater Vision in a Human Population of Sea Gypsies , 2003, Current Biology.

[171]  F. Nottebohm,et al.  Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[172]  F. Gage,et al.  Neurogenesis in the adult human hippocampus , 1998, Nature Medicine.

[173]  D. Bavelier,et al.  Cross-modal plasticity: where and how? , 2002, Nature Reviews Neuroscience.

[174]  A. Sirigu,et al.  Illusory movements of the paralyzed limb restore motor cortex activity , 2003, NeuroImage.

[175]  T. Murphy,et al.  Plasticity during stroke recovery: from synapse to behaviour , 2009, Nature Reviews Neuroscience.

[176]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[177]  E. Gould,et al.  Learning enhances adult neurogenesis in the hippocampal formation , 1999, Nature Neuroscience.

[178]  C. Gross,et al.  Neurogenesis in Adult Mammals: Some Progress and Problems , 2002, The Journal of Neuroscience.

[179]  Robert Haslinger,et al.  Rapid Structural Remodeling of Thalamocortical Synapses Parallels Experience-Dependent Functional Plasticity in Mouse Primary Visual Cortex , 2010, The Journal of Neuroscience.

[180]  Danielle M. Santarelli,et al.  The Developing Brain , 2017 .

[181]  Daphne Bavelier,et al.  Removing Brakes on Adult Brain Plasticity: From Molecular to Behavioral Interventions , 2010, The Journal of Neuroscience.

[182]  D. Hubel,et al.  Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. , 1965, Journal of neurophysiology.

[183]  Xiujuan Geng,et al.  Short-term meditation induces white matter changes in the anterior cingulate , 2010, Proceedings of the National Academy of Sciences.

[184]  Fred H. Gage,et al.  Exercise Enhances Learning and Hippocampal Neurogenesis in Aged Mice , 2005, The Journal of Neuroscience.

[185]  Neeraj Jain,et al.  Subcortical Contributions to Massive Cortical Reorganizations , 1999, Neuron.

[186]  KM Jacobs,et al.  Reshaping the cortical motor map by unmasking latent intracortical connections , 1991, Science.

[187]  L. C. Katz,et al.  Development of cortical circuits: Lessons from ocular dominance columns , 2002, Nature Reviews Neuroscience.

[188]  E. Gould,et al.  Neurogenesis in the adult is involved in the formation of trace memories , 2001, Nature.

[189]  P. Rakic No More Cortical Neurons for You , 2006, Science.

[190]  E I Knudsen,et al.  Capacity for plasticity in the adult owl auditory system expanded by juvenile experience. , 1998, Science.

[191]  T. Nurmikko,et al.  Phantom limb pain, cortical reorganization and the therapeutic effect of mental imagery , 2008, Brain : a journal of neurology.

[192]  Gerd Kempermann,et al.  The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for? , 2008, Trends in Neurosciences.

[193]  Elizabeth Gould,et al.  How widespread is adult neurogenesis in mammals? , 2007, Nature Reviews Neuroscience.

[194]  F. Schweizer,et al.  Synapses , 2022, European Lisp Symposium.

[195]  L. Luo,et al.  Axon retraction and degeneration in development and disease. , 2005, Annual review of neuroscience.

[196]  M. Ptito,et al.  Cross-modal plasticity revealed by electrotactile stimulation of the tongue in the congenitally blind. , 2005, Brain : a journal of neurology.

[197]  E. Knudsen,et al.  Mechanisms of experience-dependent plasticity in the auditory localization pathway of the barn owl , 1999, Journal of Comparative Physiology A.

[198]  Kristen M. Harris,et al.  Plasticity-Induced Growth of Dendritic Spines by Exocytic Trafficking from Recycling Endosomes , 2006, Neuron.

[199]  Sharon Begley,et al.  The Mind and the Brain: Neuroplasticity and the Power of Mental Force , 2002 .

[200]  C. Nelson CURRENT DIRECTIONS IN PSYCHOLOGICAL SCIENCE 43 the effects of maternal stress on fetal brain development , 2022 .

[201]  Adam G. Thomas,et al.  Functional but not structural changes associated with learning: An exploration of longitudinal Voxel-Based Morphometry (VBM) , 2009, NeuroImage.

[202]  E. Gould,et al.  Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus , 1998, International Journal of Developmental Neuroscience.

[203]  Gerd Kempermann,et al.  Experience-Induced Neurogenesis in the Senescent Dentate Gyrus , 1998, The Journal of Neuroscience.

[204]  Christelle Rochefort,et al.  Enriched Odor Exposure Increases the Number of Newborn Neurons in the Adult Olfactory Bulb and Improves Odor Memory , 2002, The Journal of Neuroscience.

[205]  Timothy Edward John Behrens,et al.  Training induces changes in white matter architecture , 2009, Nature Neuroscience.

[206]  G. Ramakers,et al.  Maternal Care and Hippocampal Plasticity: Evidence for Experience-Dependent Structural Plasticity, Altered Synaptic Functioning, and Differential Responsiveness to Glucocorticoids and Stress , 2008, The Journal of Neuroscience.

[207]  J. Naegele,et al.  Genetics of central nervous system developmental disorders. , 2001, Child and adolescent psychiatric clinics of North America.

[208]  J. Kaas,et al.  Growth of new brainstem connections in adult monkeys with massive sensory loss. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[209]  W. Greenough,et al.  Differential Rearing Alters Spine Density on Medium-Sized Spiny Neurons in the Rat Corpus Striatum: Evidence for Association of Morphological Plasticity with Early Response Gene Expression , 1995, Neurobiology of Learning and Memory.

[210]  J. Giedd Structural Magnetic Resonance Imaging of the Adolescent Brain , 2004, Annals of the New York Academy of Sciences.

[211]  U. Lindenberger,et al.  A theoretical framework for the study of adult cognitive plasticity. , 2010, Psychological bulletin.

[212]  P. Wong,et al.  Alterations in spatial learning and memory after forced exercise , 2006, Brain Research.

[213]  Eric I. Knudsen,et al.  Incremental training increases the plasticity of the auditory space map in adult barn owls , 2002, Nature.

[214]  T. Shimazaki,et al.  [Mammalian neural stem cells]. , 2008, Tanpakushitsu kakusan koso. Protein, nucleic acid, enzyme.

[215]  Michael M Merzenich,et al.  Perceptual Learning Directs Auditory Cortical Map Reorganization through Top-Down Influences , 2006, The Journal of Neuroscience.