Pyramidal cell development: postnatal spinogenesis, dendritic growth, axon growth, and electrophysiology

Here we review recent findings related to postnatal spinogenesis, dendritic and axon growth, pruning and electrophysiology of neocortical pyramidal cells in the developing primate brain. Pyramidal cells in sensory, association and executive cortex grow dendrites, spines and axons at different rates, and vary in the degree of pruning. Of particular note is the fact that pyramidal cells in primary visual area (V1) prune more spines than they grow during postnatal development, whereas those in inferotemporal (TEO and TE) and granular prefrontal cortex (gPFC; Brodmann's area 12) grow more than they prune. Moreover, pyramidal cells in TEO, TE and the gPFC continue to grow larger dendritic territories from birth into adulthood, replete with spines, whereas those in V1 become smaller during this time. The developmental profile of intrinsic axons also varies between cortical areas: those in V1, for example, undergo an early proliferation followed by pruning and local consolidation into adulthood, whereas those in area TE tend to establish their territory and consolidate it into adulthood with little pruning. We correlate the anatomical findings with the electrophysiological properties of cells in the different cortical areas, including membrane time constant, depolarizing sag, duration of individual action potentials, and spike-frequency adaptation. All of the electrophysiological variables ramped up before 7 months of age in V1, but continued to ramp up over a protracted period of time in area TE. These data suggest that the anatomical and electrophysiological profiles of pyramidal cells vary among cortical areas at birth, and continue to diverge into adulthood. Moreover, the data reveal that the “use it or lose it” notion of synaptic reinforcement may speak to only part of the story, “use it but you still might lose it” may be just as prevalent in the cerebral cortex.

[1]  R. Guillery Is postnatal neocortical maturation hierarchical? , 2005, Trends in Neurosciences.

[2]  R. Petralia,et al.  Histological and ultrastructural localization of the kainate receptor subunits, KA2 and GluR6/7, in the rat nervous system using selective antipeptide antibodies , 1994, The Journal of comparative neurology.

[3]  G. Elston,et al.  Parvalbumin-, Calbindin-, and Calretinin-Immunoreactive Neurons in the Prefrontal Cortex of the Owl Monkey (Aotus trivirgatus): A Standardized Quantitative Comparison with Sensory and Motor Areas , 2003, Brain, Behavior and Evolution.

[4]  Javier de Felipe Oroquieta,et al.  Pyramidal cells in prefrontal cortex: comparative observations reveal unparalleled specializations in neuronal structure among primate species , 2011 .

[5]  Javier DeFelipe,et al.  Double bouquet cell in the human cerebral cortex and a comparison with other mammals , 2005, The Journal of comparative neurology.

[6]  Rafael Yuste,et al.  Dendritic size of pyramidal neurons differs among mouse cortical regions. , 2006, Cerebral cortex.

[7]  R. S. Jones The NMDA receptor Edited by J. C. Watkins and G. L. Collinridge. Oxford University Press, New York (1990) 242 pp. £45.00 , 1991, Neuroscience.

[8]  G. Knott,et al.  Dendritic spine plasticity—Current understanding from in vivo studies , 2008, Brain Research Reviews.

[9]  I Fujita,et al.  Intrinsic connections in the macaque inferior temporal cortex , 1996, The Journal of comparative neurology.

[10]  G. Elston,et al.  Pyramidal cell specialization in the occipitotemporal cortex of the vervet monkey , 2005, Neuroreport.

[11]  R. Chase,et al.  Comparative morphology of three types of projection‐identified pyramidal neurons in the superficial layers of cat visual cortex , 1996, The Journal of comparative neurology.

[12]  Intrinsic horizontal axons in inferior temporal and primary visual cortices of macaque monkey: A developmental study , 1998, Neuroscience Research.

[13]  M. Willson Normal and Abnormal Development , 1973 .

[14]  Benjamin Sivyer,et al.  Direction selectivity in the retina: symmetry and asymmetry in structure and function , 2012, Nature Reviews Neuroscience.

[15]  Paul Manger,et al.  Pyramidal cells in V1 of African rodents are bigger, more branched and more spiny than those in primates , 2013, Front. Neuroanat..

[16]  J. DeFelipe,et al.  GABAergic complex basket formations in the human neocortex , 2010, The Journal of comparative neurology.

[17]  M. Hatten,et al.  The role of Rho GTPase proteins in CNS neuronal migration , 2011, Developmental neurobiology.

[18]  J. DeFelipe,et al.  Density and morphology of dendritic spines in mouse neocortex , 2006, Neuroscience.

[19]  G. Elston Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. , 2003, Cerebral cortex.

[20]  Jelliffe Vergleichende Lokalisationslehre der Grosshirnrinde , 1910 .

[21]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TE and TEO with medial temporal- lobe structures in infant and adult monkeys , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  Dendritic computation of direction selectivity by retinal ganglion cells. , 2000, Science.

[23]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[24]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[25]  P. Rakić,et al.  Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  M. Rosa,et al.  Visuotopic reorganization in the primary visual cortex of adult cats following monocular and binocular retinal lesions. , 1996, Cerebral cortex.

[27]  J. Kaas,et al.  Rapid reorganization of cortical maps in adult cats following restricted deafferentation in retina , 1992, Vision Research.

[28]  F. Valverde,et al.  Apical dendritic spines of the visual cortex and light deprivation in the mouse , 2004, Experimental Brain Research.

[29]  Anne-Marie M Oswald,et al.  Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. , 2008, Journal of neurophysiology.

[30]  M. Livingstone,et al.  Mechanisms of Direction Selectivity in Macaque V1 , 1998, Neuron.

[31]  Zimmermann Rr Analysis of discrimination learning capacities in the infant rhesus monkey. , 1961 .

[32]  R. Metherate,et al.  Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. , 1999, Brain research. Developmental brain research.

[33]  E. Uemura,et al.  Age-related changes in prefrontal cortex of Macaca mulatta: Quantitative analysis of dendritic branching patterns , 1980, Experimental Neurology.

[34]  T. Bonhoeffer,et al.  Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex , 2008, Nature Neuroscience.

[35]  B. Jacobs,et al.  Life‐span dendritic and spine changes in areas 10 and 18 of human cortex: A quantitative golgi study , 1997, The Journal of comparative neurology.

[36]  J. Lund,et al.  Intrinsic laminar lattice connections in primate visual cortex , 1983, The Journal of comparative neurology.

[37]  M G Rosa,et al.  Monocular focal retinal lesions induce short–term topographic plasticity in adult cat visual cortex , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  G. Elston,et al.  The Pyramidal Cell in Cognition: A Comparative Study in Human and Monkey , 2001, The Journal of Neuroscience.

[39]  R. Yuste,et al.  Cortical area and species differences in dendritic spine morphology , 2002, Journal of neurocytology.

[40]  H. Kennedy,et al.  Role of directed growth and target selection in the formation of cortical pathways: Prenatal development of the projection of area V2 to area V4 in the monkey , 1996, The Journal of comparative neurology.

[41]  R. Wenthold,et al.  The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1 , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  G. Elston,et al.  Specialization in pyramidal cell structure in the cingulate cortex of the Chacma baboon (Papio ursinus): An intracellular injection study of the posterior and anterior cingulate gyrus with comparative notes on the macaque and vervet monkeys , 2005, Neuroscience Letters.

[43]  P. Somogyi,et al.  Salient features of synaptic organisation in the cerebral cortex 1 Published on the World Wide Web on 3 March 1998. 1 , 1998, Brain Research Reviews.

[44]  G. Elston,et al.  Dendritic structure varies as a function of eccentricity in V1: A quantitative study of NADPH diaphorase neurons in the diurnal South American rodent agouti, Dasyprocta prymnolopha , 2012, Neuroscience.

[45]  A. Vercelli,et al.  Morphology of visual callosal neurons with different locations, contralateral targets or patterns of development , 2004, Experimental Brain Research.

[46]  G. Elston,et al.  Interlaminar differences in the pyramidal cell phenotype in cortical areas 7m and STP (the superior temporal polysensory area) of the macaque monkey , 2001, Experimental Brain Research.

[47]  K. Nakajima Control of tangential/non-radial migration of neurons in the developing cerebral cortex , 2007, Neurochemistry International.

[48]  P S Goldman-Rakic,et al.  The “Psychic” Neuron of the Cerebral Cortex , 1999, Annals of the New York Academy of Sciences.

[49]  Marco Aurelio M. Freire,et al.  Specialization of pyramidal cell structure in the visual areas V1, V2 and V3 of the South American rodent, Dasyprocta primnolopha , 2006, Brain Research.

[50]  G. Elston,et al.  Regional specialization in pyramidal cell structure in the limbic cortex of the vervet monkey (Cercopithecus pygerythrus): an intracellular injection study of the anterior and posterior cingulate gyrus , 2005, Experimental Brain Research.

[51]  Y. Yoshimura,et al.  Comparison of electrophysiological properties of layer III pyramidal neurons between cortical areas V1 and TE of the macaque , 2007, Neuroscience Research.

[52]  G. Elston Pyramidal cell heterogeneity in the visual cortex of the nocturnal new world owl monkey (aotus trivirgatus) , 2003, Neuroscience.

[53]  Lynne Kiorpes,et al.  Development of sensitivity to visual motion in macaque monkeys , 2004, Visual Neuroscience.

[54]  C. Blakemore,et al.  Pyramidal neurons in layer 5 of the rat visual cortex. II. Development of electrophysiological properties , 1994, The Journal of comparative neurology.

[55]  G. Elston,et al.  Specialization in pyramidal cell structure in the sensory-motor cortex of the Chacma baboon (Papio ursinus) with comparative notes on macaque and vervet monkeys. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[56]  P. Goldman-Rakic,et al.  Development and plasticity of the primate cerebral cortex. , 1990, Clinics in perinatology.

[57]  Lynne Kiorpes,et al.  Neural limitations on visual development in primates , 2004 .

[58]  J. DeFelipe,et al.  Microstructure of the neocortex: Comparative aspects , 2002, Journal of neurocytology.

[59]  G. Elston,et al.  A study of pyramidal cell structure in the cingulate cortex of the macaque monkey with comparative notes on inferotemporal and primary visual cortex. , 2004, Cerebral cortex.

[60]  Jon H. Kaas,et al.  Regional Specialization in Pyramidal Cell Structure in the Visual Cortex of the Galago: An Intracellular Injection Study of Striate and Extrastriate Areas with Comparative Notes on New World and Old World Monkeys , 2005, Brain, Behavior and Evolution.

[61]  G. Elston Specialization of the Neocortical Pyramidal Cell during Primate Evolution , 2007 .

[62]  G. Orban,et al.  Investigation of cortical reorganization in area 17 and nine extrastriate visual areas through the detection of changes in immediate early gene expression as induced by retinal lesions , 2000, The Journal of comparative neurology.

[63]  J. Lund,et al.  Neuronal composition and development in lamina 4C of monkey striate cortex , 1983, The Journal of comparative neurology.

[64]  C. W. Picanço-Diniz,et al.  Morphometric variability of nicotinamide adenine dinucleotide phosphate diaphorase neurons in the primary sensory areas of the rat , 2012, Neuroscience.

[65]  J. Lund,et al.  Widespread periodic intrinsic connections in the tree shrew visual cortex. , 1982, Science.

[66]  R. Zimmermann Analysis of discrimination learning capacities in the infant Rhesus monkey. , 1961, Journal of comparative and physiological psychology.

[67]  German Barrionuevo,et al.  Synaptic targets of the intrinsic axon collaterals of supragranular pyramidal neurons in monkey prefrontal cortex , 2001, The Journal of comparative neurology.

[68]  J. Lund,et al.  Spine formation and maturation of type 1 synapses on spiny stellate neurons in primate visual cortex , 1983, The Journal of comparative neurology.

[69]  Zhong-Wei Zhang,et al.  Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. , 2004, Journal of neurophysiology.

[70]  G. Elston,et al.  The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. , 1997, Cerebral cortex.

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

[72]  Javier DeFelipe,et al.  Spine distribution in cortical pyramidal cells: a common organizational principle across species. , 2002, Progress in brain research.

[73]  G. Elston,et al.  Specialization in pyramidal cell structure in the sensory-motor cortex of the vervet monkey (Cercopethicus pygerythrus) , 2005, Neuroscience.

[74]  E G Jones,et al.  Neurochemical gradient along the monkey occipito-temporal cortical pathway. , 1994, Neuroreport.

[75]  Distribution, morphology, and γ-aminobutyric acid immunoreactivity of horizontally projecting neurons in the macaque inferior temporal cortex , 2001 .

[76]  M. London,et al.  Dendritic computation. , 2005, Annual review of neuroscience.

[77]  N. Spruston Pyramidal neurons: dendritic structure and synaptic integration , 2008, Nature Reviews Neuroscience.

[78]  P S Goldman-Rakic,et al.  Architectonics of the parietal and temporal association cortex in the strepsirhine primate Galago compared to the anthropoid primate Macaca , 1991, The Journal of comparative neurology.

[79]  P. Hof,et al.  Dendritic morphology of pyramidal neurons in the chimpanzee neocortex: regional specializations and comparison to humans. , 2013, Cerebral cortex.

[80]  A. Cowey,et al.  Patterns of inter- and intralaminar GABAergic connections distinguish striate (V1) and extrastriate (V2, V4) visual cortices and their functionally specialized subdivisions in the rhesus monkey , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[81]  Ichiro Fujita,et al.  Spinogenesis and pruning from early visual onset to adulthood: an intracellular injection study of layer III pyramidal cells in the ventral visual cortical pathway of the macaque monkey. , 2010, Cerebral cortex.

[82]  K. Rockland,et al.  The pyramidal cell of the sensorimotor cortex of the macaque monkey: phenotypic variation. , 2002, Cerebral cortex.

[83]  Guy N Elston,et al.  Pyramidal neurons of granular prefrontal cortex of the galago: complexity in evolution of the psychic cell in primates. , 2005, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.

[84]  J. Movshon,et al.  Development of sensitivity to visual texture modulation in macaque monkeys. , 2010, Journal of Vision.

[85]  P S Goldman-Rakic,et al.  Prenatal specification of callosal connections in rhesus monkey , 1991, The Journal of comparative neurology.

[86]  Bartlett W. Mel,et al.  Impact of Active Dendrites and Structural Plasticity on the Memory Capacity of Neural Tissue , 2001, Neuron.

[87]  H. Spinnler The prefrontal cortex, Anatomy, physiology, and neuropsychology of the frontal lobe, J.M. Fuster. Raven Press, New York (1980), IX-222 pages , 1981 .

[88]  H. Markram,et al.  Morphological Development of Thick-Tufted Layer V Pyramidal Cells in the Rat Somatosensory Cortex , 2011, Front. Neuroanat..

[89]  J. Kaas,et al.  Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. , 1990, Science.

[90]  Bob Jacobs,et al.  Regional Dendritic Variation in Primate Cortical Pyramidal Cells , 2002 .

[91]  Alan Peters,et al.  A technique for estimating total spine numbers on golgi‐impregnated dendrites , 1979, The Journal of comparative neurology.

[92]  J. DeFelipe,et al.  Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. , 1993, Cerebral cortex.

[93]  P. Rakić,et al.  Synaptogenesis in monkey somatosensory cortex. , 1991, Cerebral cortex.

[94]  H. Rodman,et al.  Cortical projections to anterior inferior temporal cortex in infant macaque monkeys , 1994, Visual Neuroscience.

[95]  J. Eayrs,et al.  Postnatal development of the cerebral cortex in the rat. , 1959, Journal of anatomy.

[96]  Milos Judas,et al.  Lifespan alterations of basal dendritic trees of pyramidal neurons in the human prefrontal cortex: a layer-specific pattern. , 2008, Cerebral cortex.

[97]  J. DeFelipe,et al.  Distribution of neurons expressing tyrosine hydroxylase in the human cerebral cortex , 2007, Journal of anatomy.

[98]  J. Lund,et al.  Postnatal development of thalamic recipient neurons in the monkey striate cortex: Comparison of spine acquisition and dendritic growth of layer 4C alpha and beta spiny stellate neurons , 1991, The Journal of comparative neurology.

[99]  G. Elston,et al.  Variation in the spatial relationship between parvalbumin immunoreactive interneurones and pyramidal neurones in rat somatosensory cortex. , 1999, NeuroReport.

[100]  Earl L. Smith,et al.  Postnatal development of onset transient responses in macaque V1 AND V2 neurons. , 2008, Journal of neurophysiology.

[101]  L. Becker,et al.  Dendritic development in human occipital cortical neurons. , 1984, Brain research.

[102]  M. Koenderink,et al.  Postnatal maturation of the layer III pyramidal neurons in the human prefrontal cortex: a quantitative Golgi analysis , 1994, Brain Research.

[103]  J. Mallett A Sense of Direction , 2003, Science's STKE.

[104]  R. Yuste,et al.  Non-synaptic dendritic spines in neocortex , 2007, Neuroscience.

[105]  J. Morrison,et al.  Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis , 1995, The Journal of comparative neurology.

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

[107]  P. Huttenlocher Morphometric study of human cerebral cortex development , 1990, Neuropsychologia.

[108]  P. Rakic,et al.  Principles of neural cell migration , 1990, Experientia.

[109]  G. Elston,et al.  Cortical integration in the visual system of the macaque monkey: large-scale morphological differences in the pyramidal neurons in the occipital, parietal and temporal lobes , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[110]  J. Jacobs,et al.  Regional dendritic and spine variation in human cerebral cortex: a quantitative golgi study. , 2001, Cerebral cortex.

[111]  I. Fujita,et al.  Spinogenesis and Pruning Scales across Functional Hierarchies , 2009, The Journal of Neuroscience.

[112]  Theresa A. Jones,et al.  Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage , 1992, Brain Research.

[113]  M. L. Pucak,et al.  Synaptic targets of pyramidal neurons providing intrinsic horizontal connections in monkey prefrontal cortex , 1998, The Journal of comparative neurology.

[114]  I. Fujita,et al.  Spinogenesis and Pruning in the Anterior Ventral Inferotemporal Cortex of the Macaque Monkey: An Intracellular Injection Study of Layer III Pyramidal Cells , 2011, Front. Neuroanat..

[115]  G. Elston Pyramidal Cells of the Frontal Lobe: All the More Spinous to Think With , 2000, The Journal of Neuroscience.

[116]  R. Wenthold,et al.  Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[117]  Giovanni Maria Carlomagno,et al.  Heat flux sensors and infrared thermography , 2007, J. Vis..

[118]  Patrick R Hof,et al.  Influence of Highly Distinctive Structural Properties on the Excitability of Pyramidal Neurons in Monkey Visual and Prefrontal Cortices , 2012, The Journal of Neuroscience.

[119]  Edward G Jones,et al.  The origins of cortical interneurons: mouse versus monkey and human. , 2009, Cerebral cortex.

[120]  G. Elston,et al.  Distribution and patterns of connectivity of interneurons containing calbindin, calretinin, and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey , 1999, The Journal of comparative neurology.

[121]  W. R. Taylor,et al.  Diverse Synaptic Mechanisms Generate Direction Selectivity in the Rabbit Retina , 2002, The Journal of Neuroscience.

[122]  M G Rosa,et al.  Cellular heterogeneity in cerebral cortex: A study of the morphology of pyramidal neurones in visual areas of the marmoset monkey , 1999, The Journal of comparative neurology.

[123]  G. Elston,et al.  Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. , 1998, Cerebral cortex.

[124]  Guy N Elston,et al.  Ipsilateral corticocortical projections to the primary and middle temporal visual areas of the primate cerebral cortex: area‐specific variations in the morphology of connectionally identified pyramidal cells , 2006, The European journal of neuroscience.

[125]  G. Elston,et al.  Pyramidal Cells in Prefrontal Cortex of Primates: Marked Differences in Neuronal Structure Among Species , 2010, Frontiers in Neuroanatomy.

[126]  J. Lund,et al.  A quantitative investigation of spine and dendrite development of neurons in visual cortex (area 17) of Macaca nemestrina monkeys , 1979, The Journal of comparative neurology.

[127]  K. Brodmann Neuere Forschungsergebnisse der Großhirnrindenanatomie mit besonderer Berücksichtigung anthropologischer Fragen , 1913, Naturwissenschaften.

[128]  D. V. van Essen,et al.  Development of connections within and between areas V1 and V2 of macaque monkeys , 1996, The Journal of comparative neurology.

[129]  William D. Hopkins,et al.  Comparative neuronal morphology of the cerebellar cortex in afrotherians, carnivores, cetartiodactyls, and primates , 2014, Front. Neuroanat..

[130]  A. Zaitsev,et al.  Functional maturation of excitatory synapses in layer 3 pyramidal neurons during postnatal development of the primate prefrontal cortex. , 2008, Cerebral cortex.

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

[132]  L. Kiorpes,et al.  Linking structure and function: Development of lateral spatial interactions in macaque monkeys , 2013, Visual Neuroscience.

[133]  C. Gross,et al.  Response properties of neurons in temporal cortical visual areas of infant monkeys. , 1993, Journal of neurophysiology.

[134]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[135]  P. Rakic Evolution of the neocortex: Perspective from developmental biology , 2010 .

[136]  A. Chédotal Should I stay or should I go? Becoming a granule cell , 2010, Trends in Neurosciences.

[137]  Earl L. Smith,et al.  Receptive-Field Subfields of V2 Neurons in Macaque Monkeys Are Adult-Like Near Birth , 2013, The Journal of Neuroscience.

[138]  Leslie G. Ungerleider,et al.  Transient subcortical connections of inferior temporal areas TE and TEO in infant macaque monkeys , 1995, The Journal of comparative neurology.

[139]  J. S. Lund,et al.  Synchronous development of pyramidal neuron dendritic spines and parvalbumin-immunoreactive chandelier neuron axon terminals in layer III of monkey prefrontal cortex , 1995, Neuroscience.

[140]  G. Elston,et al.  Pyramidal cell specialization in the occipitotemporal cortex of the Chacma baboon (Papio ursinus) , 2005, Experimental Brain Research.

[141]  I. Fujita,et al.  Spinogenesis and pruning in the primary auditory cortex of the macaque monkey (Macaca fascicularis): An intracellular injection study of layer III pyramidal cells , 2010, Brain Research.

[142]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. , 1994, Cerebral cortex.

[143]  Shintaro Funahashi,et al.  Information Processes in the Primate Prefrontal Cortex in Relation to Working Memory Processes , 2002, Reviews in the neurosciences.

[144]  Bob Jacobs,et al.  Regional Dendritic Variation in Neonatal Human Cortex: A Quantitative Golgi Study , 2005, Developmental Neuroscience.

[145]  P. Huttenlocher Synaptic density in human frontal cortex - developmental changes and effects of aging. , 1979, Brain research.

[146]  G. Elston The pyramidal neuron in occipital, temporal and prefrontal cortex of the owl monkey (Aotus trivirgatus): regional specialization in cell structure , 2003, The European journal of neuroscience.

[147]  J. DeFelipe,et al.  Demonstration of glutamate-positive axon terminals forming asymmetric synapses in cat neocortex , 1988, Brain Research.

[148]  Y. Chino,et al.  Development of temporal response properties and contrast sensitivity of V1 and V2 neurons in macaque monkeys. , 2007, Journal of neurophysiology.

[149]  Y. Chino,et al.  Normal and Abnormal Development of the Neuronal Response Properties in Primate Visual Cortex , 2003 .

[150]  R. Malach,et al.  Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex , 1993, The Journal of comparative neurology.

[151]  M. Colonnier,et al.  Postnatal changes in the number of neurons and synapses in the visual cortex (area 17) of the macaque monkey: A stereological analysis in normal and monocularly deprived animals , 1982, The Journal of comparative neurology.

[152]  P. Hof,et al.  Synaptogenesis and development of pyramidal neuron dendritic morphology in the chimpanzee neocortex resembles humans , 2013, Proceedings of the National Academy of Sciences.

[153]  G. Collingridge,et al.  The NMDA Receptor , 1995 .

[154]  J. Anthony Movshon,et al.  Development of sensitivity to global form and motion in macaque monkeys (Macaca nemestrina) , 2012, Vision Research.

[155]  H. Hirsch,et al.  Exposure to lines of only one orientation modifies dendritic morphology of cells in the visual cortex of the cat , 1982, The Journal of comparative neurology.

[156]  P. Rakić,et al.  Tempo of neurogenesis and synaptogenesis in the primate cingulate mesocortex: Comparison with the neocortex , 1995, The Journal of comparative neurology.

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

[158]  W. Taylor,et al.  Direction selectivity in the retina , 2002, Current Opinion in Neurobiology.

[159]  E. Smith,et al.  Postnatal development of disparity sensitivity in visual area 2 (v2) of macaque monkeys. , 2008, Journal of neurophysiology.

[160]  D. McCormick,et al.  Post‐natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. , 1987, The Journal of physiology.

[161]  H. Kennedy,et al.  Segregation of callosal and association pathways during development in the visual cortex of the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[162]  J. Pettigrew,et al.  The effect of visual experience on the development of stimulus specificity by kitten cortical neurones , 1974, The Journal of physiology.

[163]  F. Rossi,et al.  Molecular mechanisms of dendritic spine development and maintenance. , 2008, Acta neurobiologiae experimentalis.

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

[165]  P. Hof,et al.  Regional distribution of neurofilament and calcium-binding proteins in the cingulate cortex of the macaque monkey. , 1992, Cerebral cortex.

[166]  I. Fujita,et al.  Contrasting forms of synaptic plasticity in monkey inferotemporal and primary visual cortices , 1997, Neuroreport.

[167]  G. Elston,et al.  Morphological variability of NADPH diaphorase neurons across areas V1, V2, and V3 of the common agouti , 2010, Brain Research.

[168]  P. Rakić,et al.  Synaptogenesis in visual cortex of normal and preterm monkeys: evidence for intrinsic regulation of synaptic overproduction. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[169]  D. Lewis,et al.  Horizontal synaptic connections in monkey prefrontal cortex: an in vitro electrophysiological study. , 2000, Cerebral cortex.

[170]  I. Fujita,et al.  Organization of horizontal axons in the inferior temporal cortex and primary visual cortex of the macaque monkey. , 2005, Cerebral cortex.

[171]  Bartlett W. Mel,et al.  Cortical rewiring and information storage , 2004, Nature.

[172]  J. Kleim,et al.  Synaptogenesis and dendritic growth in the cortex opposite unilateral sensorimotor cortex damage in adult rats: a quantitative electron microscopic examination , 1996, Brain Research.

[173]  Ichiro Fujita,et al.  Postnatal development of dendritic structure of layer III pyramidal neurons in the medial prefrontal cortex of marmoset , 2014, Brain Structure and Function.

[174]  Christina M. Weaver,et al.  Age-related changes to layer 3 pyramidal cells in the rhesus monkey visual cortex. , 2015, Cerebral cortex.

[175]  Ichiro Fujita,et al.  Postnatal development of layer III pyramidal cells in the primary visual, inferior temporal, and prefrontal cortices of the marmoset , 2012, Front. Neural Circuits.

[176]  P. Goldman-Rakic,et al.  Concurrent overproduction of synapses in diverse regions of the primate cerebral cortex. , 1986, Science.

[177]  J. P. Schwartz,et al.  Development and Plasticity , 1997 .

[178]  J. Kaas,et al.  Specializations of the granular prefrontal cortex of primates: implications for cognitive processing. , 2006, The anatomical record. Part A, Discoveries in molecular, cellular, and evolutionary biology.