Sensitive Periods in the Development of the Brain and Behavior

Experience exerts a profound influence on the brain and, therefore, on behavior. When the effect of experience on the brain is particularly strong during a limited period in development, this period is referred to as a sensitive period. Such periods allow experience to instruct neural circuits to process or represent information in a way that is adaptive for the individual. When experience provides information that is essential for normal development and alters performance permanently, such sensitive periods are referred to as critical periods. Although sensitive periods are reflected in behavior, they are actually a property of neural circuits. Mechanisms of plasticity at the circuit level are discussed that have been shown to operate during sensitive periods. A hypothesis is proposed that experience during a sensitive period modifies the architecture of a circuit in fundamental ways, causing certain patterns of connectivity to become highly stable and, therefore, energetically preferred. Plasticity that occurs beyond the end of a sensitive period, which is substantial in many circuits, alters connectivity patterns within the architectural constraints established during the sensitive period. Preferences in a circuit that result from experience during sensitive periods are illustrated graphically as changes in a stability landscape, a metaphor that represents the relative contributions of genetic and experiential influences in shaping the information processing capabilities of a neural circuit. By understanding sensitive periods at the circuit level, as well as understanding the relationship between circuit properties and behavior, we gain a deeper insight into the critical role that experience plays in shaping the development of the brain and behavior.

[1]  E. Hess,et al.  A Laboratory Approach to the Study of Imprinting , 1954 .

[2]  Imprinting. , 1960, Science.

[3]  J. P. Scott.  Critical periods in behavioral development. , 1962, Science.

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

[5]  D. Hubel,et al.  Binocular interaction in striate cortex of kittens reared with artificial squint. , 1965, Journal of neurophysiology.

[6]  P. Marler.  A comparative approach to vocal learning: Song development in white-crowned sparrows. , 1970 .

[7]  P. Marler.  Birdsong and speech development: could there be parallels? , 1970, American scientist.

[8]  Klaus Immelmann,et al.  Sexual and Other Long-Term Aspects of Imprinting in Birds and Other Species , 1972 .

[9]  C. Blakemore,et al.  Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period , 1974, The Journal of physiology.

[10]  Myron A. Hofer,et al.  Imprinting: Early Experience and the Developmental Psychobiology of Attachment , 1975 .

[11]  S. Oyama.  A sensitive period for the acquisition of a nonnative phonological system , 1976 .

[12]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[13]  S. Curtiss.  Genie: A Psycholinguistic Study of a Modern-Day "Wild Child" , 1977 .

[14]  M. Stryker,et al.  Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. , 1978, The Journal of physiology.

[15]  J. Schmidt,et al.  The relationship of α-bungarotoxin binding activity and cholinergic termination within the rat hippocampus , 1979, Neuroscience.

[16]  D. Hubel,et al.  The development of ocular dominance columns in normal and visually deprived monkeys , 1980, The Journal of comparative neurology.

[17]  C. Blakemore,et al.  Recovery from monocular deprivation in the monkey. I. Reversal of physiological effects in the visual cortex , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[18]  P. D. Spear,et al.  Critical periods for effects of monocular deprivation: differences between striate and extrastriate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  伊藤 正男.  The cerebellum and neural control , 1984 .

[20]  A. Arnold,et al.  Forebrain lesions disrupt development but not maintenance of song in passerine birds. , 1984, Science.

[21]  M. Konishi,et al.  Birdsong: from behavior to neuron. , 1985, Annual review of neuroscience.

[22]  G. Mower,et al.  Role of visual experience in activating critical period in cat visual cortex. , 1985, Journal of Neurophysiology.

[23]  F. Duffy,et al.  Dark rearing prolongs physiological but not anatomical plasticity of the cat visual cortex , 1985, The Journal of comparative neurology.

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

[25]  L. Baptista,et al.  Song development in the white-crowned sparrow: social factors and sex differences , 1986, Animal Behaviour.

[26]  W. Greenough,et al.  Differential rearing effects on rat visual cortex synapses. III. Neuronal and glial nuclei, boutons, dendrites, and capillaries , 1987, Brain Research.

[27]  L. Cooper,et al.  A physiological basis for a theory of synapse modification. , 1987, Science.

[28]  W. Singer,et al.  Pharmacological induction of use-dependent receptive field modifications in the visual cortex. , 1988, Science.

[29]  Peter M. Duppenthaler.  Maturational Constraints on Language Learning , 1990 .

[30]  N. Daw,et al.  GAP-43 in the cat visual cortex during postnatal development , 1990, Visual Neuroscience.

[31]  D. Prince,et al.  Postnatal maturation of the GABAergic system in rat neocortex. , 1991, Journal of neurophysiology.

[32]  J. Steeves,et al.  Suppression of the onset of myelination extends the permissive period for the functional repair of embryonic spinal cord. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[33]  N. Daw,et al.  Critical period for monocular deprivation in the cat visual cortex. , 1992, Journal of neurophysiology.

[34]  H. Neville,et al.  Fractionating language: different neural subsystems with different sensitive periods. , 1992, Cerebral cortex.

[35]  Mark F. Bear,et al.  Neocortical long-term potentiation , 1993, Current Opinion in Neurobiology.

[36]  A. Groothuis.  Advances in the Study of Behavior , 1993 .

[37]  M P Stryker,et al.  Rapid remodeling of axonal arbors in the visual cortex. , 1993, Science.

[38]  P. Kuhl.  Learning and representation in speech and language , 1994, Current Opinion in Neurobiology.

[39]  K. Fox,et al.  Critical period control in sensory cortex , 1994, Current Opinion in Neurobiology.

[40]  H. Rodman.  Development of inferior temporal cortex in the monkey. , 1994, Cerebral cortex.

[41]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[42]  N W Daw,et al.  Mechanisms of plasticity in the visual cortex. The Friedenwald Lecture. , 1994, Investigative ophthalmology & visual science.

[43]  T. Devoogd,et al.  Song Isolation Is Associated with Maintaining High Spine Frequencies on Zebra Finch IMAN Neurons , 1995, Neurobiology of Learning and Memory.

[44]  Nigel W. Daw,et al.  Mechanisms of Plasticity in the Visual Cortex , 1995 .

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

[46]  C. ten Cate,et al.  Early experience and plasticity of song in adult male zebra finches (Taeniopygia guttata) , 1996 .

[47]  H. Neville,et al.  Maturational Constraints on Functional Specializations for Language Processing: ERP and Behavioral Evidence in Bilingual Speakers , 1996, Journal of Cognitive Neuroscience.

[48]  E. Smith,et al.  Loss of stereopsis in monkeys following prismatic binocular dissociation during infancy , 1996, Behavioural Brain Research.

[49]  N. Daw.  Critical periods and strabismus: what questions remain? , 1997, Optometry and vision science : official publication of the American Academy of Optometry.

[50]  A. Arnold,et al.  Developmental plasticity in neural circuits for a learned behavior. , 1997, Annual review of neuroscience.

[51]  A. Doupe.  Song- and Order-Selective Neurons in the Songbird Anterior Forebrain and their Emergence during Vocal Development , 1997, The Journal of Neuroscience.

[52]  Shakti Sharma,et al.  Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. , 1997, Science.

[53]  P. Rakić,et al.  Early divergence of magnocellular and parvocellular functional subsystems in the embryonic primate visual system. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[54]  M. Stryker,et al.  Local GABA circuit control of experience-dependent plasticity in developing visual cortex. , 1998, Science.

[55]  M. Kilgard,et al.  Cortical map reorganization enabled by nucleus basalis activity. , 1998, Science.

[56]  G. Horn.  Visual imprinting and the neural mechanisms of recognition memory , 1998, Trends in Neurosciences.

[57]  E. Knudsen,et al.  Sensitive Periods for Visual Calibration of the Auditory Space Map in the Barn Owl Optic Tectum , 1998, The Journal of Neuroscience.

[58]  R. C. Honey,et al.  Imprinting, learning and development: from behaviour to brain and back , 1998, Trends in Neurosciences.

[59]  M. Stryker,et al.  Morphology of Single Geniculocortical Afferents and Functional Recovery of the Visual Cortex after Reverse Monocular Deprivation in the Kitten , 1998, The Journal of Neuroscience.

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

[61]  Ross A. Thompson,et al.  Early attachment and later development. , 1999 .

[62]  G. Yeni-Komshian,et al.  Age Constraints on Second-Language Acquisition , 1999 .

[63]  S. Bernstein,et al.  Introduction , 2022 .

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

[65]  Richard Mooney,et al.  Sensitive periods and circuits for learned birdsong , 1999, Current Opinion in Neurobiology.

[66]  R. Mooney,et al.  Androgens modulate NMDA receptor-mediated EPSCs in the zebra finch song system. , 1999, Journal of neurophysiology.

[67]  R. Nicoll,et al.  Long-term potentiation--a decade of progress? , 1999, Science.

[68]  Phillip R. Shaver,et al.  Handbook of attachment : theory, research, and clinical applications , 1999 .

[69]  J. Partridge,et al.  Selective acquisition of AMPA receptors over postnatal development suggests a molecular basis for silent synapses , 1999, Nature Neuroscience.

[70]  P. Kuhl,et al.  Birdsong and human speech: common themes and mechanisms. , 1999, Annual review of neuroscience.

[71]  L. Petitto,et al.  Biological Foundations of Language , 1967, Neurology.

[72]  M. Fagiolini,et al.  Inhibitory threshold for critical-period activation in primary visual cortex , 2000, Nature.

[73]  E. G. Jones,et al.  Cortical and subcortical contributions to activity-dependent plasticity in primate somatosensory cortex. , 2000, Annual review of neuroscience.

[74]  J. Trachtenberg,et al.  Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. , 2000, Science.

[75]  Nicoletta Berardi,et al.  Critical periods during sensory development , 2000, Current Opinion in Neurobiology.

[76]  S. Nelson,et al.  Hebb and homeostasis in neuronal plasticity , 2000, Current Opinion in Neurobiology.

[77]  R. Nicoll,et al.  Synaptic plasticity and dynamic modulation of the postsynaptic membrane , 2000, Nature Neuroscience.

[78]  S. J. Martin,et al.  Synaptic plasticity and memory: an evaluation of the hypothesis. , 2000, Annual review of neuroscience.

[79]  David R. Colman,et al.  Molecular Modification of N-Cadherin in Response to Synaptic Activity , 2000, Neuron.

[80]  D. Feldman,et al.  Timing-Based LTP and LTD at Vertical Inputs to Layer II/III Pyramidal Cells in Rat Barrel Cortex , 2000, Neuron.

[81]  L Shapiro,et al.  Making memories stick: cell-adhesion molecules in synaptic plasticity. , 2000, Trends in cell biology.

[82]  E. Kandel.  The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses , 2001, Science.

[83]  E. Knudsen,et al.  GABAergic Inhibition Antagonizes Adaptive Adjustment of the Owl's Auditory Space Map during the Initial Phase of Plasticity , 2001, The Journal of Neuroscience.

[84]  Elissa L. Newport,et al.  Critical thinking about critical periods: Perspectives on a critical period for language acquisition. , 2001 .

[85]  D. Feldman.  A New Critical Period for Sensory Map Plasticity , 2001, Neuron.

[86]  M P Stryker,et al.  Rapid Anatomical Plasticity of Horizontal Connections in the Developing Visual Cortex , 2001, The Journal of Neuroscience.

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

[88]  C. Cepko,et al.  Regulating proliferation during retinal development , 2001, Nature Reviews Neuroscience.

[89]  E I Knudsen,et al.  Adaptive Axonal Remodeling in the Midbrain Auditory Space Map , 2001, The Journal of Neuroscience.

[90]  M. Meaney,et al.  Environmental Enrichment Reverses the Effects of Maternal Separation on Stress Reactivity , 2002, The Journal of Neuroscience.

[91]  E. Knudsen.  Instructed learning in the auditory localization pathway of the barn owl , 2002, Nature.

[92]  A. Kirkwood,et al.  Dark Rearing Alters the Development of GABAergic Transmission in Visual Cortex , 2002, The Journal of Neuroscience.

[93]  L. Maffei,et al.  Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex , 2002, Science.

[94]  A. Huberman,et al.  Neurotrophins and visual cortical plasticity. , 2002, Progress in brain research.

[95]  Joseph E LeDoux,et al.  Parallels between cerebellum- and amygdala-dependent conditioning , 2002, Nature Reviews Neuroscience.

[96]  M. Poo,et al.  Reversal and Stabilization of Synaptic Modifications in a Developing Visual System , 2003, Science.

[97]  D. Feldman,et al.  Ocular Dominance Plasticity in Mature Mice , 2003, Neuron.

[98]  S. Strittmatter,et al.  Targeting the Nogo Receptor to Treat Central Nervous System Injuries , 2003, Nature Reviews Drug Discovery.

[99]  Daniel E Feldman,et al.  Development of Columnar Topography in the Excitatory Layer 4 to Layer 2/3 Projection in Rat Barrel Cortex , 2003, The Journal of Neuroscience.

[100]  Eric R. Kandel,et al.  A Neuronal Isoform of CPEB Regulates Local Protein Synthesis and Stabilizes Synapse-Specific Long-Term Facilitation in Aplysia , 2003, Cell.

[101]  M. Ehlers.  Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system , 2003, Nature Neuroscience.

[102]  A. Kania,et al.  Topographic Motor Projections in the Limb Imposed by LIM Homeodomain Protein Regulation of Ephrin-A:EphA Interactions , 2003, Neuron.

[103]  D. Linden,et al.  The other side of the engram: experience-driven changes in neuronal intrinsic excitability , 2003, Nature Reviews Neuroscience.

[104]  Cristopher M Niell,et al.  Live optical imaging of nervous system development. , 2004, Annual review of physiology.

[105]  B. Barres,et al.  Role for glia in synaptogenesis , 2004, Glia.

[106]  H. Scheich.  Neural correlates of auditory filial imprinting , 1987, Journal of Comparative Physiology A.

[107]  E. S. Ruthazer,et al.  Insights into activity-dependent map formation from the retinotectal system: a middle-of-the-brain perspective. , 2004, Journal of neurobiology.

[108]  Gabriel Horn,et al.  Pathways of the past: the imprint of memory , 2004, Nature Reviews Neuroscience.

[109]  M. Rutter.  Multiple meanings of a developmental perspective on psychopathology , 2005 .

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

[111]  S. Sollars.  Chorda tympani nerve transection at different developmental ages produces differential effects on taste bud volume and papillae morphology in the rat. , 2005, Journal of neurobiology.

[112]  P. Kuhl,et al.  Early Speech Perception and Later Language Development: Implications for the "Critical Period" , 2005 .

[113]  René Hen,et al.  Genetics of affective and anxiety disorders. , 2006, Annual review of psychology.

[114]  John M Desesso,et al.  Postnatal growth and morphological development of the brain: a species comparison. , 2006, Birth defects research. Part B, Developmental and reproductive toxicology.

[115]  P. Hagoort,et al.  Development of the Human Cortex and the Concept of “Critical” or “Sensitive” Periods , 2006 .

[116]  David Birdsong,et al.  Age and Second Language Acquisition and Processing: A Selective Overview , 2006 .

[117]  Y. Arshavsky.  “Scientific roots” of dualism in neuroscience , 2006, Progress in Neurobiology.

[118]  Tal Savion-Lemieux,et al.  The effect of early musical training on adult motor performance: evidence for a sensitive period in motor learning , 2006, Experimental Brain Research.

[119]  Heinke,et al.  Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons , 2022 .

[120]  Brian J. Wiltgen,et al.  Expert face processing requires visual input to the right hemisphere during infancy , 2022 .