Functional maturation of excitatory synapses in layer 3 pyramidal neurons during postnatal development of the primate prefrontal cortex
Abstract
In the primate dorsolateral prefrontal cortex (DLPFC), the density of excitatory synapses decreases by 40-50% during adolescence. Although such substantial circuit refinement might underlie the adolescence-related maturation of working memory performance, its functional significance remains poorly understood. The consequences of synaptic pruning may depend on the properties of the eliminated synapses. Are the synapses eliminated during adolescence functionally immature, as is the case during early brain development? Or do maturation-independent features tag synapses for pruning? We examined excitatory synaptic function in monkey DLPFC during postnatal development by studying properties that reflect synapse maturation in rat cortex. In 3-month-old (early postnatal) monkeys, excitatory inputs to layer 3 pyramidal neurons had immature properties, including higher release probability, lower alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA)/N-methyl-D-aspartate (NMDA) ratio, and longer duration of NMDA-mediated synaptic currents, associated with greater sensitivity to the NMDA receptor subunit B (NR2B) subunit-selective antagonist ifenprodil. In contrast, excitatory synaptic inputs in neurons from preadolescent (15 months old) and adult (42 or 84 months old) monkeys had similar functional properties. We therefore conclude that the contribution of functionally immature synapses decreases significantly before adolescence begins. Thus, remodeling of excitatory connectivity in the DLPFC during adolescence may occur in the absence of widespread maturational changes in synaptic strength.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Functional measures of excitatory AMPA and NMDA mediated currents in frontal cortex pyramidal neurons do not change between the juvenile and adolescent periods in macaques or mice.
“Functional measures of excitatory AMPA and NMDA mediated currents in frontal cortex pyramidal neurons do not change between the juvenile and adolescent periods in macaques or mice (Gonzalez-Burgos et al., 2008; Vandenberg et al., 2015)”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Gonzalez-Burgos et al., 2008
Cites
Dynamic mapping of human cortical development during childhood through early adulthood
Gogtay, N., Giedd, J. N., Lusk, L., Hayashi, K. M., Greenstein, D., Vaituzis, A. C., Nugent, T. F., Herman, D. H., Clasen, L. S., Toga, A. W., et al. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402680101 · Cited by 5,604 · cited 1× · see citing works
“1999), a decrease usually interpreted to result from the massive synaptic pruning occurring during this period (Gogtay et al. 2004).”
BackgroundBrain development during childhood and adolescence: a longitudinal MRI study
Giedd, J. N., Blumenthal, J., Jeffries, N. O., Castellanos, F. X., Liu, H., Zijdenbos, A., Paus, T., Evans, A. C., & Rapoport, J. L. (1999) · Nature Neuroscience · doi:10.1038/13158 · Cited by 5,552 · see citing works
The Glutamate Receptor Ion Channels
Dingledine, R., Borges, K., Bowie, D., & Traynelis, S. F. (1999) · Pharmacological Reviews · doi:10.1016/s0031-6997(24)01394-2 · Cited by 3,554 · see citing works
Synaptic Activity and the Construction of Cortical Circuits
Katz, L. C., & Shatz, C. J. (1996) · Science · doi:10.1126/science.274.5290.1133 · Cited by 3,048 · see citing works
Monyer, H., Burnashev, N., Laurie, D. J., Sakmann, B., & Seeburg, P. H. (1994) · Neuron · doi:10.1016/0896-6273(94)90210-0 · Cited by 2,989 · see citing works
Cognitive and affective development in adolescence
Steinberg, L. (2005) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.12.005 · Cited by 2,978 · see citing works
(2024) · Pharmacological Reviews · doi:10.1124/pr · Cited by 2,680 · see citing works
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
Critical period plasticity in local cortical circuits
Hensch, T. K. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1787 · Cited by 2,323 · see citing works
Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex
Trachtenberg, J. T., Chen, B. E., Knott, G. W., Feng, G., Sanes, J. R., Welker, E., & Svoboda, K. (2002) · Nature · doi:10.1038/nature01273 · Cited by 1,927 · see citing works
Maturation of Cognitive Processes From Late Childhood to Adulthood
Luna, B., Garver, K. E., Urban, T. A., Lazar, N. A., & Sweeney, J. A. (2004) · Child Development · doi:10.1111/j.1467-8624.2004.00745.x · Cited by 1,351 · see citing works
Translating developmental time across mammalian species
Clancy, B., Darlington, R. B., & Finlay, B. L. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00171-3 · Cited by 1,221 · see citing works
Long-term dendritic spine stability in the adult cortex
Grutzendler, J., Kasthuri, N., & Gan, W.-B. (2002) · Nature · doi:10.1038/nature01276 · Cited by 1,198 · see citing works
Changing subunit composition of heteromeric NMDA receptors during development of rat cortex
Sheng, M., Cummings, J., Roldan, L. A., Jan, Y. N., & Jan, L. Y. (1994) · Nature · doi:10.1038/368144a0 · Cited by 1,170 · see citing works
Schizophrenia as a Disorder of Neurodevelopment
Lewis, D. A., & Levitt, P. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142754 · Cited by 1,163 · see citing works
Self-citationConcurrent overproduction of synapses in diverse regions of the primate cerebral cortex
Rakic, P., Bourgeois, J.-P., Eckenhoff, M. F., Zecevic, N., & Goldman-Rakic, P. S. (1986) · Science · doi:10.1126/science.3952506 · Cited by 1,133 · cited 3× · see citing works
“no significant changes in the density of inhibitory synapses are observed in the neocortex during adolescence (Rakic et al. 1986; De Felipe et al. 1997).”
BackgroundTransient and persistent dendritic spines in the neocortex in vivo
Holtmaat, A. J. G. D., Trachtenberg, J. T., Wilbrecht, L., Shepherd, G. M., Zhang, X., Knott, G. W., & Svoboda, K. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.003 · Cited by 1,131 · see citing works
The development of ocular dominance columns in normal and visually deprived monkeys
Le Vay, S., Wiesel, T. N., & Hubel, D. H. (1980) · Journal of Comparative Neurology · doi:10.1002/cne.901910102 · Cited by 1,123 · see citing works
Stuart, G. J., Dodt, H., & Sakmann, B. J. (1993) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00374949 · Cited by 804 · see citing works
Long-term potentiation and functional synapse induction in developing hippocampus
Durand, G. M., Kovalchuk, Y., & Konnerth, A. (1996) · Nature · doi:10.1038/381071a0 · Cited by 789 · see citing works
Huettner, J. E., & Bean, B. P. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.4.1307 · Cited by 751 · see citing works
Activity-Dependent Decrease in NMDA Receptor Responses During Development of the Visual Cortex
Carmignoto, G., & Vicini, S. (1992) · Science · doi:10.1126/science.1279803 · Cited by 716 · see citing works
NMDA Receptor Subunit Composition Controls Synaptic Plasticity by Regulating Binding to CaMKII
Barria, A., & Malinow, R. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.034 · Cited by 709 · see citing works
Synaptogenesis in the Prefrontal Cortex of Rhesus Monkeys
Bourgeois, J.-P., Goldman-Rakic, P. S., & Rakic, P. (1994) · Cerebral Cortex · doi:10.1093/cercor/4.1.78 · Cited by 687 · see citing works
Development of long-term dendritic spine stability in diverse regions of cerebral cortex
Zuo, Y., Lin, A., Chang, P., & Gan, W.-B. (2005) · Neuron · doi:10.1016/j.neuron.2005.04.001 · Cited by 684 · see citing works
Experience-dependent and cell-type-specific spine growth in the neocortex
Holtmaat, A., Wilbrecht, L., Knott, G. W., Welker, E., & Svoboda, K. (2006) · Nature · doi:10.1038/nature04783 · Cited by 631 · see citing works
The probability of transmitter release at a mammalian central synapse
Hessler, N. A., Shirke, A. M., & Malinow, R. (1993) · Nature · doi:10.1038/366569a0 · Cited by 617 · see citing works
Nonuniform probability of glutamate release at a hippocampal synapse.
Rosenmund, C., Clements, J., & Westbrook, G. (1993) · Science · doi:10.1126/science.7901909 · Cited by 616 · see citing works
NR2A Subunit Expression Shortens NMDA Receptor Synaptic Currents in Developing Neocortex
Flint, A. C., Maisch, U. S., Weishaupt, J. H., Kriegstein, A. R., & Monyer, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02469.1997 · Cited by 615 · see citing works
Bourgeois, J., & Rakic, P. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-07-02801.1993 · Cited by 567 · see citing works
Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents
Lester, R. A. J., Clements, J. D., Westbrook, G. L., & Jahr, C. E. (1990) · Nature · doi:10.1038/346565a0 · Cited by 564 · see citing works
Spine growth precedes synapse formation in the adult neocortex in vivo
Knott, G. W., Holtmaat, A., Wilbrecht, L., Welker, E., & Svoboda, K. (2006) · Nature Neuroscience · doi:10.1038/nn1747 · Cited by 563 · see citing works
Maturation of a Central Glutamatergic Synapse
Wu, G.-Y., Malinow, R., & Cline, H. T. (1996) · Science · doi:10.1126/science.274.5289.972 · Cited by 546 · see citing works
Silent synapses during development of thalamocortical inputs
Isaac, J. T. R., Crair, M. C., Nicoll, R. A., & Malenka, R. C. (1997) · Neuron · doi:10.1016/s0896-6273(00)80267-6 · Cited by 507 · see citing works
MECHANISMS OF VERTEBRATE SYNAPTOGENESIS
Waites, C. L., Craig, A. M., & Garner, C. C. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144336 · Cited by 483 · see citing works
Neurocognitive development of the ability to manipulate information in working memory
Crone, E. A., Wendelken, C., Donohue, S. E., Leijenhorst, L. V., & Bunge, S. A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510088103 · Cited by 463 · see citing works
Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex
Zuo, Y., Yang, G., Kwon, E., & Gan, W.-B. (2005) · Nature · doi:10.1038/nature03715 · Cited by 436 · see citing works
Mirnics, K., Middleton, F. A., Lewis, D. A., & Levitt, P. R. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01862-2 · Cited by 393 · see citing works
Lewis, D. (1997) · Neuropsychopharmacology · doi:10.1016/s0893-133x(96)00277-1 · Cited by 388 · see citing works
Self-citationRegulation of hippocampal transmitter release during development and long-term potentiation.
Bolshakov, V. Y., & Siegelbaum, S. (1995) · Science · doi:10.1126/science.7569903 · Cited by 385 · see citing works
Liu, X.-B., Murray, K. D., & Jones, E. G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2476-04.2004 · Cited by 316 · see citing works
Synaptic and Extrasynaptic NMDA Receptor NR2 Subunits in Cultured Hippocampal Neurons
Thomas, C. G., Miller, A., & Westbrook, G. L. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00771.2005 · Cited by 286 · see citing works
Activation of Silent Synapses by Rapid Activity-Dependent Synaptic Recruitment of AMPA Receptors
Liao, D., Scannevin, R. H., & Huganir, R. L. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-16-06008.2001 · Cited by 286 · see citing works
Development of cortical circuits: Lessons from ocular dominance columns
Katz, L. C., & Crowley, J. C. (2002) · Nature reviews. Neuroscience · doi:10.1038/nrn703 · Cited by 276 · see citing works
Inhibitory synaptogenesis in mouse somatosensory cortex
DeFelipe, J. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.7.619 · Cited by 276 · see citing works
Cooperation between independent hippocampal synapses is controlled by glutamate uptake
Arnth-Jensen, N., Jabaudon, D., & Scanziani, M. (2002) · Nature Neuroscience · doi:10.1038/nn825 · Cited by 260 · see citing works
Subtype-Dependence of NMDA Receptor Channel Open Probability
Chen, N., Luo, T., & Raymond, L. A. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-16-06844.1999 · Cited by 260 · see citing works
Estrogen Alters Spine Number and Morphology in Prefrontal Cortex of Aged Female Rhesus Monkeys
Hao, J., Rapp, P. R., Leffler, A. E., Leffler, S. R., Janssen, W. G. M., Lou, W. Y. W., McKay, H. M., Roberts, J. A., Wearne, S. L., Hof, P. R., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3440-05.2006 · Cited by 257 · see citing works
Axons and synaptic boutons are highly dynamic in adult visual cortex
Stettler, D. D., Yamahachi, H., Li, W., Denk, W., & Gilbert, C. D. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.018 · Cited by 256 · see citing works
Anderson, S. A., Classey, J. D., Condé, F., Lund, J. S., & Lewis, D. A. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00051-j · Cited by 245 · see citing works
Testa, C. M., Friberg, I. K., Weiss, S. W., & Standaert, D. G. (1998) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19980105)390:1 · Cited by 237 · see citing works
Zhang, Z. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00855.2003 · Cited by 210 · see citing works
Tang, Y. C. (2003) · Cerebral Cortex · doi:10.1093/cercor/bhg121 · Cited by 197 · see citing works
Rumpel, S., Hatt, H. H., & Gottmann, K. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-21-08863.1998 · Cited by 184 · see citing works
Montgomery, J. M., Pavlidis, P., & Madison, D. V. (2001) · Neuron · doi:10.1016/s0896-6273(01)00244-6 · Cited by 170 · see citing works
Horizontal synaptic connections in monkey prefrontal cortex: An in vitro electrophysiological study
Gonzalez-Burgos, G. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.1.82 · Cited by 169 · see citing works
Diamond, J. S. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.5125-04.2005 · Cited by 164 · see citing works
Glutamate receptor ion channels.
Mayer, M. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.05.004 · Cited by 163 · see citing works
Lozovaya, N. A., Grebenyuk, S. E., Tsintsadze, T. S., Feng, B., Monaghan, D. T., & Krishtal, O. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.063792 · Cited by 162 · see citing works
Spontaneous and evoked synaptic rewiring in the neonatal neocortex
Bé, J.-V. L., & Markram, H. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0604691103 · Cited by 159 · see citing works
Peripubertal refinement of the intrinsic and associational circuitry in monkey prefrontal cortex
Woo, T.-U., Pucak, M. L., Kye, C. H., Matus, C. V., & Lewis, D. A. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00059-6 · Cited by 157 · see citing works
Timing of the Critical Period for Plasticity of Ocular Dominance Columns in Macaque Striate Cortex
Horton, J. C., & Hocking, D. R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03684.1997 · Cited by 151 · see citing works
Franks, K. M., & Isaacson, J. S. (2005) · Neuron · doi:10.1016/j.neuron.2005.05.024 · Cited by 138 · see citing works
Changes in synaptic structure underlie the developmental speeding of AMPA receptor–mediated EPSCs
Cathala, L., Holderith, N. B., Nusser, Z., DiGregorio, D. A., & Cull-Candy, S. G. (2005) · Nature Neuroscience · doi:10.1038/nn1534 · Cited by 127 · see citing works
‘Deaf, mute and whispering’ silent synapses: their role in synaptic plasticity
Voronin, L. L., & Cherubini, E. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2003.058966 · Cited by 125 · see citing works
Lewis, D. A., Cruz, D. A., Eggan, S. M., & Erickson, S. L. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1308.008 · Cited by 121 · see citing works
AMPA signalling in nascent glutamatergic synapses: there and not there!
Groc, L., Gustafsson, B., & Hanse, E. (2006) · Trends in Neurosciences · doi:10.1016/j.tins.2006.01.005 · Cited by 118 · see citing works
Cruz, D. A., Eggan, S. M., & Lewis, D. A. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10833 · Cited by 118 · see citing works
Erisir, A., & Harris, J. L. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-12-05208.2003 · Cited by 111 · see citing works
Eye Opening Rapidly Induces Synaptic Potentiation and Refinement
Lü, W., & Constantine‐Paton, M. (2004) · Neuron · doi:10.1016/j.neuron.2004.06.031 · Cited by 101 · see citing works
Mechanisms Underlying Developmental Speeding in AMPA-EPSC Decay Time at the Calyx of Held
Koike‐Tani, M., Saitoh, N., & Takahashi, T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3861-04.2005 · Cited by 97 · see citing works
Acute versus chronic NMDA receptor blockade and synaptic AMPA receptor delivery
Zhu, J., & Malinow, R. (2002) · Nature Neuroscience · doi:10.1038/nn0602-850 · Cited by 97 · see citing works
Nakayama, K., Kiyosue, K., & Taguchi, T. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4115-04.2005 · Cited by 84 · see citing works
Maturation of prefrontal cortex in the monkey revealed by local reversible cryogenic depression
Goldman, P. S., & Alexander, G. E. (1977) · Nature · doi:10.1038/267613a0 · Cited by 79 · see citing works
Kumar, S. S., & Huguenard, J. R. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.6.2973 · Cited by 78 · see citing works
Lozovaya, N., Kopanitsa, M. V., Boychuk, Y. A., & Krishtal, O. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00638-1 · Cited by 76 · see citing works
Yanagisawa, T., Tsumoto, T., & Kimura, F. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03756.x · Cited by 69 · see citing works
Schizophrenia: a genetic disorder of the synapse?
Owen, M. J., O’Donovan, M. C., & Harrison, P. J. (2005) · BMJ · doi:10.1136/bmj.330.7484.158 · Cited by 67 · see citing works
Mierau, S. B., Meredith, R. M., Upton, A. L., & Paulsen, O. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0402916101 · Cited by 67 · see citing works
Silent Synapses in the Immature Visual Cortex: Layer-Specific Developmental Regulation
Rumpel, S., Kattenstroth, G., & Gottmann, K. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00443.2003 · Cited by 65 · see citing works
Postsynaptic receptor mechanisms underlying developmental speeding of synaptic transmission
Takahashi, T. (2005) · Neuroscience Research · doi:10.1016/j.neures.2005.07.005 · Cited by 59 · see citing works
Developmental Changes in Release Properties of the CA3-CA1 Glutamate Synapse in Rat Hippocampus
Wasling, P., Hanse, E., & Gustafsson, B. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00464.2004 · Cited by 57 · see citing works
González‐Burgos, G. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh015 · Cited by 54 · see citing works
Bourne, J. N., Kirov, S. A., Sorra, K. E., & Harris, K. M. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.06.020 · Cited by 40 · see citing works
Fu, Z., Logan, S. M., & Vicini, S. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2004.079467 · Cited by 39 · see citing works
Huttenlocher (1997) · doi:10.1002/(sici)1096-9861(19971020)387:2
Flagged first, then by citations
Cited by
Sorted by citations
Extraordinary neoteny of synaptic spines in the human prefrontal cortex
Petanjek, Z., Judaš, M., Šimić, G., Rašin, M. R., Uylings, H. B. M., Rakic, P., & Kostović, I. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1105108108 · Cited by 1,411 · see citing works
Burnett, S., Sebastian, C., Cohen Kadosh, K., & Blakemore, S.-J. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.011 · Cited by 391 · see citing works
Neuroplasticity of Neocortical Circuits in Schizophrenia
Lewis, D. A., & González‐Burgos, G. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301563 · Cited by 362 · see citing works
MicroRNA, mRNA, and protein expression link development and aging in human and macaque brain
Somel, M., Guo, S., Fu, N., Yan, Z., Hu, H. Y., Xu, Y., Yuan, Y., Ning, Z., Hu, Y., Menzel, C., et al. (2010) · Genome Research · doi:10.1101/gr.106849.110 · Cited by 285 · see citing works
Changes in the adolescent brain and the pathophysiology of psychotic disorders
Keshavan, M. S., Giedd, J. N., Lau, J. Y. F., Lewis, D. A., & Paus, T. (2014) · The Lancet Psychiatry · doi:10.1016/s2215-0366(14)00081-9 · Cited by 247 · see citing works
GABA Neuron Alterations, Cortical Circuit Dysfunction and Cognitive Deficits in Schizophrenia
González‐Burgos, G., Fish, K. N., & Lewis, D. A. (2011) · Neural Plasticity · doi:10.1155/2011/723184 · Cited by 244 · see citing works
Cell Type-Specific Development of NMDA Receptors in the Interneurons of Rat Prefrontal Cortex
Wang, H.-X., & Gao, W. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.20 · Cited by 198 · see citing works
Wang, H., Stradtman, G. G., Wang, X.-J., & Gao, W.-J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804318105 · Cited by 199 · see citing works
Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex?
Piekarski, D. J., Johnson, C. M., Boivin, J. R., Thomas, A. W., Lin, W. C., Delevich, K., M. Galarce, E., & Wilbrecht, L. (2017) · Brain Research · doi:10.1016/j.brainres.2016.08.042 · Cited by 175 · see citing works
Hashimoto, T., Nguyen, Q. L., Rotaru, D., Keenan, T., Arion, D., Beneyto, M., Gonzalez-Burgos, G., & Lewis, D. A. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.01.004 · Cited by 151 · see citing works
Self-citationPagani, M., Barsotti, N., Bertero, A., Trakoshis, S., Ulysse, L., Locarno, A., Misevičiūtė, I., Felice, A. D., Canella, C., Supekar, K., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26131-z · Cited by 148 · see citing works
Elston, G. N., & Fujita, I. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00078 · Cited by 150 · see citing works
Lewis, D. A. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08156.x · Cited by 142 · see citing works
Hoftman, G. D., & Lewis, D. A. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr029 · Cited by 128 · see citing works
Amygdala Gene Expression Correlates of Social Behavior in Monkeys Experiencing Maternal Separation
Sabatini, M. J., Ebert, P., Lewis, D. A., Levitt, P., Cameron, J. L., & Mirnics, K. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4765-06.2007 · Cited by 125 · see citing works
Hoftman, G. D., Datta, D., & Lewis, D. A. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2016.05.022 · Cited by 109 · see citing works
Developmental regulation of the NMDA receptor subunits, NR3A and NR1, in human prefrontal cortex
Henson, M. A., Roberts, A. C., Salimi, K., Vadlamudi, S., Hamer, R. M., Gilmore, J. H., Jarskog, L. F., & Philpot, B. D. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn017 · Cited by 110 · see citing works
Cho, R. Y., Walker, C. P. R., Polizzotto, N. R., Wozny, T. A., Fissell, C., Chen, C. A., & Lewis, D. A. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht341 · Cited by 109 · see citing works
Prefrontal Cortical Circuits in Schizophrenia
Volk, D. W., & Lewis, D. A. (2010) · Current topics in behavioral neurosciences · doi:10.1007/7854_2010_44 · Cited by 106 · see citing works
Adolescent Maturation of Cortical Dopamine
O’Donnell, P. (2010) · Neurotoxicity Research · doi:10.1007/s12640-010-9157-3 · Cited by 107 · see citing works
Hamilton, G. F., Whitcher, L. T., & Klintsova, A. Y. (2009) · Synapse · doi:10.1002/syn.20711 · Cited by 98 · see citing works
Monaco, S. A., Gulchina, Y., & Gao, W. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.06.022 · Cited by 92 · see citing works
Li, Y.-C., Xi, D., Roman, J., Huang, Y.-Q., & Gao, W. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3336-09.2009 · Cited by 89 · see citing works
Dienel, S. J., Schoonover, K. E., & Lewis, D. A. (2022) · Biological Psychiatry · doi:10.1016/j.biopsych.2022.03.002 · Cited by 81 · see citing works
Development of visual working memory precision in childhood
Heyes, S. B., Zokaei, N., van der Staaij, I., Bays, P. M., & Masud Husain, B. (2012) · Developmental Science · doi:10.1111/j.1467-7687.2012.01148.x · Cited by 80 · see citing works
McQuail, J. A., Beas, B. S., Kelly, K. B., Simpson, K. L., Frazier, C. J., Setlow, B., & Bizon, J. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2332-16.2016 · Cited by 80 · see citing works
Counotte, D. S., Smit, A. B., Pattij, T., & Spijker, S. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.05.010 · Cited by 77 · see citing works
Neurophysiological changes with age probed by inverse modeling of EEG spectra
van Albada, S. J., Kerr, C. C., Chiang, A. K., RENNIE, C. J., & Robinson, P. A. (2009) · Clinical Neurophysiology · doi:10.1016/j.clinph.2009.09.021 · Cited by 77 · see citing works
Brai, E., Marathe, S. V., Astori, S., Fredj, N. B., Perry, E., Lamy, C. M., Scotti, A. L., & Alberi, L. A. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00447 · Cited by 73 · see citing works
Gao, W., Yang, S.-S., Mack, N. R., & Chamberlin, L. A. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01196-w · Cited by 70 · see citing works
Pérez-Rodríguez, M., Arroyo‐García, L. E., Prius-Mengual, J., Andrade‐Talavera, Y., Armengol, J. A., Pérez-Villegas, E. M., Duque‐Feria, P., Flores, G., & Moreno, A. R. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy194 · Cited by 69 · see citing works
Electrophysiological classes of layer 2/3 pyramidal cells in monkey prefrontal cortex
Zaitsev, A. V., Povysheva, N. V., González‐Burgos, G., & Lewis, D. A. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00859.2011 · Cited by 67 · see citing works
Eggan, S. M., Mizoguchi, Y., Stoyak, S. R., & Lewis, D. A. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp179 · Cited by 64 · see citing works
Role of netrin-1 in the organization and function of the mesocorticolimbic dopamine system
Flores, C. (2011) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.100171 · Cited by 64 · see citing works
A computational neuroscience approach to schizophrenia and its onset
Rolls, E. T., & Deco, G. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.001 · Cited by 65 · see citing works
Gonzalez-Burgos, G., Miyamae, T., Pafundo, D. E., Yoshino, H., Rotaru, D. C., Hoftman, G., Datta, D., Zhang, Y., Hammond, M., Sampson, A. R., et al. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu122 · Cited by 64 · see citing works
He, H., Mahnke, A. H., Doyle, S., Fan, N., Wang, C.-C., Hall, B. J., Tang, Y., Inglis, F. M., Chen, C., & Erickson, J. D. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.4505-11.2012 · Cited by 64 · see citing works
Povysheva, N. V., & Johnson, J. W. (2012) · Journal of Neurophysiology · doi:10.1152/jn.01017.2011 · Cited by 62 · see citing works
Self-citationDatta, D., Arion, D., & Lewis, D. A. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu040 · Cited by 59 · see citing works
Petanjek, Z., Sedmak, D., Džaja, D., Hladnik, A., Rašin, M. R., & Milošević, N. J. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00122 · Cited by 64 · see citing works
An integrated network model of psychotic symptoms
Looijestijn, J., Blom, J. D., Aleman, A., Hoek, H. W., & Goekoop, R. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.09.016 · Cited by 55 · see citing works
Cruz, D. A., Lovallo, E., Stockton, S. D., Rasband, M. N., & Lewis, D. A. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22006 · Cited by 51 · see citing works
Neuroplasticity of excitatory and inhibitory cortical circuits in schizophrenia
Lewis, D. A. (2009) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2009.11.3/dalewis · Cited by 53 · see citing works
Cortical Opioid Markers in Schizophrenia and across Postnatal Development
Volk, D. W., Radchenkova, P., Er, W., Sengupta, E. J., & Lewis, D. A. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr202 · Cited by 51 · see citing works
Beneyto, M., & Lewis, D. A. (2010) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2010.08.003 · Cited by 50 · see citing works
Urban, K. R., Li, Y., & Gao, W. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.01.004 · Cited by 50 · see citing works
González‐Burgos, G., Rotaru, D. C., Zaitsev, A. V., Povysheva, N. V., & Lewis, D. A. (2008) · Journal of Neurophysiology · doi:10.1152/jn.91161.2008 · Cited by 47 · see citing works
Persistent Synapse Loss Induced by Repetitive LTD in Developing Rat Hippocampal Neurons
Shinoda, Y., Tanaka, T., Tominaga‐Yoshino, K., & Ogura, A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010390 · Cited by 42 · see citing works
Kerr, M. I., Wall, M. J., & Richardson, M. J. E. (2013) · The Journal of Physiology · doi:10.1113/jphysiol.2012.244392 · Cited by 40 · see citing works
Reserve pool neuron transmitter respecification: Novel neuroplasticity
Dulcis, D., & Spitzer, N. C. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20920 · Cited by 38 · see citing works
Amakhin, D. V., Malkin, S. L., Ergina, J. L., Kryukov, K. A., Veniaminova, E. A., Zubareva, O. E., & Zaitsev, A. V. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00264 · Cited by 37 · see citing works
Uhlhaas, P. J. (2011) · Schizophrenia Bulletin · doi:10.1093/schbul/sbr025 · Cited by 37 · see citing works
Tendilla‐Beltrán, H., Sanchez-Islas, N. D. C., Marina-Ramos, M., Leza, J. C., & Flores, G. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101967 · Cited by 34 · see citing works
Prius-Mengual, J., Pérez-Rodríguez, M., Andrade‐Talavera, Y., & Moreno, A. R. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-1187-5 · Cited by 29 · see citing works
Approximate Invariance of Metabolic Energy per Synapse during Development in Mammalian Brains
Karbowski, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033425 · Cited by 27 · see citing works
Cholinergic and Adenosinergic Modulation of Synaptic Release
Yang, D., Ding, C., Qi, G., & Feldmeyer, D. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2020.06.006 · Cited by 24 · see citing works
Hepatic arginase deficiency fosters dysmyelination during postnatal CNS development
Liu, X.-B., Haney, J. R., Cantero, G., Lambert, J., Otero‐García, M., Truong, B., Gropman, A. L., Cobos, I., Cederbaum, S. D., & Lipshutz, G. S. (2019) · JCI Insight · doi:10.1172/jci.insight.130260 · Cited by 25 · see citing works
Vandenberg, A., Piekarski, D. J., Caporale, N., Munoz-Cuevas, F. J., & Wilbrecht, L. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00005 · Cited by 22 · see citing works
Sedmak, D., Hrvoj-Mihić, B., Džaja, D., Habek, N., Uylings, H. B. M., & Petanjek, Z. (2018) · Croatian Medical Journal · doi:10.3325/cmj.2018.59.189 · Cited by 22 · see citing works
Sequence of Molecular Events during the Maturation of the Developing Mouse Prefrontal Cortex
Ueda, S., Niwa, M., Hioki, H., Sohn, J., Kaneko, T., Sawa, A., & Sakurai, T. (2015) · Complex Psychiatry · doi:10.1159/000430095 · Cited by 20 · see citing works
Persistent storage capability impairs decision making in a biophysical network model
Standage, D., & Paré, M. (2011) · Neural Networks · doi:10.1016/j.neunet.2011.05.004 · Cited by 19 · see citing works
The Unique Properties of the Prefrontal Cortex and Mental Illness
Gao, W., Wang, H.-X., Melissa, A., & Li, Y. (2012) · InTech eBooks · doi:10.5772/35868 · Cited by 17 · see citing works
Dienel, S. J., Ciesielski, A. J., Bazmi, H. H., Profozich, E., Fish, K. N., & Lewis, D. A. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa341 · Cited by 15 · see citing works
Saberi, A., Wischnewski, K. J., Jung, K., Lotter, L. D., Schaare, H. L., Banaschewski, T., Barker, G. J., Bokde, A. L. W., Desrivières, S., Flor, H., et al. (2025) · Science Advances · doi:10.1126/sciadv.adr8164 · Cited by 18 · see citing works
Short‐term field stimulation mimics synaptic maturation of hippocampal synapses
Bagley, E. E., & Westbrook, G. L. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.224964 · Cited by 12 · see citing works
Sekizawa, S., Joad, J. P., Pinkerton, K. E., & Bonham, A. C. (2009) · Toxicology and Applied Pharmacology · doi:10.1016/j.taap.2009.10.009 · Cited by 12 · see citing works
Chen, T., Zhang, D., Dragomir, A., Kobayashi, K., Akay, Y. M., & Akay, M. (2011) · Journal of NeuroEngineering and Rehabilitation · doi:10.1186/1743-0003-8-58 · Cited by 10 · see citing works
Postnikova, T. Y., Griflyuk, A. V., Ergina, J. L., Zubareva, O. E., & Zaitsev, A. V. (2020) · Pharmaceuticals · doi:10.3390/ph13030048 · Cited by 9 · see citing works
McCool, B. A., & McGinnis, M. M. (2019) · Handbook of experimental pharmacology · doi:10.1007/164_2019_296 · Cited by 8 · see citing works
Dienel, S. J., Bazmi, H. H., & Lewis, D. A. (2017) · Neurobiology of Disease · doi:10.1016/j.nbd.2017.05.016 · Cited by 8 · see citing works
Hoftman, G. D., Bazmi, H. H., Ciesielski, A. J., Dinka, L. A., Chen, K., & Lewis, D. A. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa342 · Cited by 8 · see citing works
González‐Burgos, G., Miyamae, T., Reddy, N., Dawkins, S., Chen, C., Hill, A., Enwright, J. F., Ermentrout, B., & Lewis, D. A. (2023) · Cerebral Cortex · doi:10.1093/cercor/bhad077 · Cited by 7 · see citing works
Adolescent Maturation of Cortical Dopamine
O’Donnell, P. (2010) · Springer eBooks · doi:10.1007/978-1-4614-0785-0_11 · Cited by 7 · see citing works
González‐Burgos, G., Miyamae, T., Nishihata, Y., Krimer, O. L., & Lewis, D. A. (2023) · Biological Psychiatry · doi:10.1016/j.biopsych.2023.01.019 · Cited by 6 · see citing works
Simulation-based inference of developmental EEG maturation with the spectral graph model
Bernardo, D., Xie, X., Verma, P., Kim, J., Liu, V., Numis, A. L., Wu, Y., Glass, H. C., Yap, P., Nagarajan, S. S., et al. (2024) · Communications Physics · doi:10.1038/s42005-024-01748-w · Cited by 4 · see citing works
Saberi, A., Wischnewski, K. J., Jung, K., Lotter, L. D., Schaare, H. L., Banaschewski, T., Barker, G. J., Bokde, A. L. W., Desrivières, S., Flor, H., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.06.18.599509 · Cited by 4 · see citing works
Synapse-associated neuropathological markers in Alzheimer's disease
Barrantes, F. J. (2026) · Brain · doi:10.1093/brain/awag117 · Cited by 2 · see citing works
González‐Burgos, G., Miyamae, T., Nishihata, Y., Krimer, O. L., Wade, K., Fish, K. N., Arion, D., Cai, Z., Xue, M., Stauffer, W. R., et al. (2024) · Journal of Neurophysiology · doi:10.1152/jn.00326.2024 · Cited by 1 · see citing works
King, D. P., Khan, M., Majewska, A. K., Cameron, J. L., & Fudge, J. L. (2026) · Journal of Neuroscience · doi:10.1523/jneurosci.0017-26.2026 · Cited by 1 · see citing works
Kirk, R. W., Liwei, S., Xiao, R., Clark, E., & Nelson, S. B. (2026) · eLife · doi:10.1101/2025.02.07.636951 · Cited by 1 · see citing works
Kirk, R. W., Liwei, S., Xiao, R., Clark, E., & Nelson, S. B. (2025) · eLife · doi:10.7554/elife.106510.1 · Cited by 1 · see citing works
Kirk, R. W., Liwei, S., Xiao, R., Clark, E., & Nelson, S. B. (2025) · eLife · doi:10.7554/elife.106510 · Cited by 1 · see citing works
Lifespan Trajectories of Alpha Rhythm: Dynamic Shifts in Neural Excitation-Inhibition BalancePreprint
Han, C., Cheung, V. C. K., & Chan, R. H. M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.14.653960 · Cited by 2 · see citing works
Keshavan, M. S., Medical, B. I. D., & Lau, J. Y. F. (2014)
González‐Burgos, G., Fish, K. N., & Lewis, D. A. (2011)
Role of ErbB4 splicing in parvalbumin interneuron maturation and schizophrenia
Chung, D. W. (2016) · D-Scholarship@Pitt (University of Pittsburgh)
Network mechanisms of working memory: the role of neuronal nonlinearitiesPreprint
Suarez-Perez, A., Harish, O., & Hansel, D. (2021) · arXiv (Cornell University) · doi:10.48550/arxiv.2112.05091
Benes, F. M., & Konopaske, G. T. (2012) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.716598020.792302857
González‐Burgos, G., Miyamae, T., Reddy, N., Dawkins, S., Chen, C., Hill, A., Enwright, J. F., Ermentrout, B., & Lewis, D. A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.26.489470
Adolescent Maturation of Cortical Dopamine
O’Donnell, P. (2013) · Springer eBooks · doi:10.1007/978-1-4614-7264-3_13
King, D. P., Khan, M., Majewska, A. K., Cameron, J. L., & Fudge, J. L. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.06.697965
Nadei, O. V., & Prokopenko, E. S. (2026) · Journal of Molecular Neuroscience · doi:10.1007/s12031-026-02491-3
Diversity of Layer 3 Pyramidal Neuron Properties Across Areas of the Primate Neocortex
González‐Burgos, G., Benavides‐Piccione, R., Neef, A., Inoue, W., Muller, L., Jimenez-Sosa, M. S., Staiger, J. F., Medalla, M., & Luebke, J. I. (2026) · Biological Psychiatry · doi:10.1016/j.biopsych.2026.08.015
Kirk, R. G., Liwei, S., Xiao, R., Clark, E., & Nelson, S. B. (2026) · eLife · doi:10.7554/elife.106510.2
- Authors
- Gonzalez-Burgos, G., Kroener, S., Zaitsev, A. V., Povysheva, N. V., Krimer, L. S., Barrionuevo, G., & Lewis, D. A.
- Affiliations
- Medical University of South Carolina (US)
- University of Pittsburgh (US)
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-06-24
- Volume
- 18
- Issue
- 3
- Pages
- 626-637
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- OpenAlex
- W2102786824
- Cited by
- 95
- References
- 86
- Citations by year
- 2026: 7 · 2025: 4 · 2024: 3 · 2023: 2 · 2022: 2 · 2021: 3 · 2020: 5 · 2019: 4 · 2018: 3 · 2017: 2 · 2016: 4 · 2015: 5 · 2014: 5 · 2013: 4 · 2012: 9
- FWCI
- 2.91
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cerebral Cortex (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH 45156, P50MH045156)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- excitatory synapses, synapse maturation, dorsolateral prefrontal cortex, postnatal development, adolescence, synaptic pruning, AMPA/NMDA ratio, NMDA receptor, NR2B subunit, ifenprodil, release probability, primate brain development
- MeSH terms
- Animals, Animals, Newborn, Female, Macaca mulatta, Primates, Synapses, Prefrontal Cortex, Pyramidal Cells, Excitatory Postsynaptic Potentials, Dendritic Spines
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review