Selective Changes in Thin Spine Density and Morphology in Monkey Prefrontal Cortex Correlate with Aging-Related Cognitive Impairment
Open accessAbstract
Age-associated memory impairment (AAMI) occurs in many mammalian species, including humans. In contrast to Alzheimer's disease (AD), in which circuit disruption occurs through neuron death, AAMI is due to circuit and synapse disruption in the absence of significant neuron loss and thus may be more amenable to prevention or treatment. We have investigated the effects of aging on pyramidal neurons and synapse density in layer III of area 46 in dorsolateral prefrontal cortex of young and aged, male and female rhesus monkeys ( Macaca mulatta ) that were tested for cognitive status through the delayed non-matching-to-sample (DNMS) and delayed response tasks. Cognitive tests revealed an age-related decrement in both acquisition and performance on DNMS. Our morphometric analyses revealed both an age-related loss of spines (33%, p < 0.05) on pyramidal cells and decreased density of axospinous synapses (32%, p < 0.01) in layer III of area 46. In addition, there was an age-related shift in the distribution of spine types reflecting a selective vulnerability of small, thin spines, thought to be particularly plastic and linked to learning. While both synapse density and the overall spine size average of an animal were predictive of number of trials required for acquisition of DNMS (i.e., learning the task), the strongest correlate of behavior was found to be the head volume of thin spines, with no correlation between behavior and mushroom spine size or density. No synaptic index correlated with memory performance once the task was learned.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Decreases in both thin and mushroom spine types have been reported in animal models of cognitive decline.
“Decreases in both spine types have been reported in animal models of cognitive decline [54], [55].”
From Arf4 Determines Dentate Gyrus-Mediated Pattern Separation by Regulating Dendritic Spine Development (2012) · cites this paper as [54]
The Results (Effects of aging on dendritic spine morphology) report a 45.6% decrease in thin spine density but no statistically significant difference in mushroom spine density. The Discussion (Synaptic basis for cognitive aging) explicitly says mushroom spine density was unchanged in aged versus young monkeys, contrary to the claim that both types decreased. (LLM, conf=0.90)
Checked by a reasoning model — may be wrong.
Experimental — accuracy not yet measuredLoss of thin spines in monkey PFC is selectively correlated with age-related cognitive impairment.
“The loss of thin spines in monkey PFC, which are particularly plastic and linked to learning, is selectively correlated with age-related cognitive impairment 241.”
From Mechanisms of synaptic transmission dysregulation in the prefrontal cortex: pathophysiological implications (2022) · cites this paper as [241]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
The unbiased estimation of number and sizes of arbitrary particles using the disector
Sterio, D. C. (1984) · Journal of Microscopy · doi:10.1111/j.1365-2818.1984.tb02501.x · Cited by 2,533 · see citing works
Fuster, J. M. (1997) · Cited by 2,095 · see citing works
Matsuzaki, M., Ellis-Davies, G. C. R., Nemoto, T., Miyashita, Y., Iino, M., & Kasai, H. (2001) · Nature Neuroscience · doi:10.1038/nn736 · Cited by 1,563 · cited 2× · see citing works
“…that small spines are NMDA receptor (NMDAR) dominated, highly motile, and capable of expanding and stabilizing or retracting, whereas large spines are highly stable and AMPAR dominated (Matsuzaki et al., 2001; Kasai et al., 2003; Zuo et al., 2005; Holtmaat et al., 2006; Bourne and Harris, 2007).”
BackgroundLife and Death of Neurons in the Aging Brain
Morrison, J. H., & Hof, P. R. (1997) · Science · doi:10.1126/science.278.5337.412 · Cited by 1,344 · see citing works
Self-citationLong-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 · cited 1× · see citing works
“Thus it is unlikely that filopodia [long and thin protrusions without spine heads (Grutzendler et al., 2002)] contributed to the spine density and size measurements.”
BackgroundStably maintained dendritic spines are associated with lifelong memories
Yang, G., Pan, F., & Gan, W.-B. (2009) · Nature · doi:10.1038/nature08577 · Cited by 1,182 · see citing works
Harris, K., & Stevens, J. (1989) · The Journal of Neuroscience · doi:10.1523/jneurosci.09-08-02982.1989 · Cited by 1,073 · see citing works
Harris, K. M., Jensen, F. E., & Tsao, B. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-07-02685.1992 · Cited by 990 · see citing works
Structure-stability-function relationships of dendritic spines
Kasai, H., Matsuzaki, M., Noguchi, J., Yasumatsu, N., & Nakahara, H. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00162-0 · Cited by 847 · see citing works
Do thin spines learn to be mushroom spines that remember?
Bourne, J., & Harris, K. M. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.04.009 · Cited by 843 · see citing works
Structural dynamics of dendritic spines in memory and cognition
Kasai, H., Fukuda, M., Watanabe, S., Hayashi-Takagi, A., & Noguchi, J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.001 · Cited by 804 · 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
Different modes of expression of AMPA and NMDA receptors in hippocampal synapses
Takumi, Y., Ramírez-León, V., Laake, P., Rinvik, E., & Ottersen, O. P. (1999) · Nature Neuroscience · doi:10.1038/10172 · Cited by 675 · 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
Rodriguez, A., Ehlenberger, D. B., Dickstein, D. L., Hof, P. R., & Wearne, S. L. (2008) · PLoS ONE · doi:10.1371/journal.pone.0001997 · Cited by 571 · see citing works
Environmental Influences on Cognitive and Brain Plasticity During Aging
Kramer, A. F., Bherer, L., Colcombe, S. J., Dong, W., & Greenough, W. T. (2004) · The Journals of Gerontology Series A · doi:10.1093/gerona/59.9.m940 · Cited by 498 · see citing works
Impaired Recognition Memory in Monkeys after Damage Limited to the Hippocampal Region
Zola, S. M., Squire, L. R., Teng, E., Stefanacci, L., Buffalo, E. A., & Clark, R. E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00451.2000 · Cited by 477 · see citing works
Sorra, K. E., & Harris, K. M. (2000) · Hippocampus · doi:10.1002/1098-1063(2000)10:5 · Cited by 456 · see citing works
Murray, E. A., & Mishkin, M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-16-06568.1998 · Cited by 434 · see citing works
THE USE OF ANIMAL MODELS TO STUDY THE EFFECTS OF AGING ON COGNITION
Gallagher, M., & Rapp, P. R. (1997) · Annual Review of Psychology · doi:10.1146/annurev.psych.48.1.339 · Cited by 430 · see citing works
Self-citationThe prefrontal cortex: categories, concepts and cognition
Miller, E. K., Freedman, D. J., & Wallis, J. D. (2002) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2002.1099 · Cited by 414 · see citing works
Anatomy of the Prefrontal Cortex
Fuster, J. M. (2008) · The Prefrontal Cortex · doi:10.1016/b978-0-12-373644-4.00002-5 · Cited by 364 · see citing works
Cyclic Estrogen Replacement Improves Cognitive Function in Aged Ovariectomized Rhesus Monkeys
Rapp, P. R., Morrison, J. H., & Roberts, J. A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05708.2003 · Cited by 352 · see citing works
Self-citationAge-related Dendritic and Spine Changes in Corticocortically Projecting Neurons in Macaque Monkeys
Duan, H. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.9.950 · Cited by 317 · see citing works
Principles of Long-Term Dynamics of Dendritic Spines
Yasumatsu, N., Matsuzaki, M., Miyazaki, T., Noguchi, J., & Kasai, H. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0603-08.2008 · Cited by 314 · see citing works
(1984) · Cerebral cortex · doi:10.1007/978-1-4615-6610-6 · Cited by 289 · see citing works
Evidence for task-dependent memory dysfunction in the aged monkey
Rapp, P. R., & Amaral, D. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-10-03568.1989 · Cited by 277 · see citing works
Self-citationAging and the myelinated fibers in prefrontal cortex and corpus callosum of the monkey
Peters, A., & Sethares, C. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.10099 · Cited by 274 · see citing works
Synapses are lost during aging in the primate prefrontal cortex
Peters, A., Sethares, C., & Luebke, J. I. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.014 · Cited by 268 · see citing works
Aged monkeys exhibit behavioral deficits indicative of widespread cerebral dysfunction
Bachevalier, J., Landis, L. S., Walker, L. C., Brickson, M., Mishkin, M., Price, D. L., & Cork, L. C. (1991) · Neurobiology of Aging · doi:10.1016/0197-4580(91)90048-o · Cited by 264 · 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
Self-citationFeature article: are neurons lost from the primate cerebral cortex during normal aging?
Peters, A. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.4.295 · Cited by 245 · see citing works
Different modes of hippocampal plasticity in response to estrogen in young and aged female rats
Adams, M. M., Shah, R. A., Janssen, W. G. M., & Morrison, J. H. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.141215898 · Cited by 222 · see citing works
Self-citationRodriguez, A., Ehlenberger, D. B., Hof, P. R., & Wearne, S. L. (2006) · Nature Protocols · doi:10.1038/nprot.2006.313 · Cited by 193 · see citing works
Baxter, M. G., & Murray, E. A. (2001) · Hippocampus · doi:10.1002/1098-1063(2001)11:1 · Cited by 186 · see citing works
Hao, J., Rapp, P. R., Janssen, W. G. M., Lou, W. Y. W., Lasley, B. L., Hof, P. R., & Morrison, J. H. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704757104 · Cited by 176 · see citing works
Self-citationThe effects of aging on layer 1 in area 46 of prefrontal cortex in the rhesus monkey
Peters, A. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.8.671 · Cited by 167 · see citing works
Rapp, P. R., & Amaral, D. G. (1991) · Neurobiology of Aging · doi:10.1016/0197-4580(91)90077-w · Cited by 144 · see citing works
Self-citationChang, Y. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh144 · Cited by 139 · see citing works
Bussire, T., Gold, G., Kvari, E., Giannakopoulos, P., Bouras, C., Perl, D. P., Morrison, J. H., & Hof, P. R. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00942-9 · Cited by 122 · see citing works
Self-citationFrontal connections and cognitive changes in normal aging rhesus monkeys: A DTI study.
Makris, N., Papadimitriou, G. M., van der Kouwe, A., Kennedy, D. N., Hodge, S. M., Dale, A. M., Benner, T., Wald, L. L., Wu, O., Tuch, D. S., et al. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.07.005 · Cited by 115 · see citing works
Zola, S. M., & Squire, L. R. (2001) · Hippocampus · doi:10.1002/hipo.1027 · Cited by 90 · see citing works
A critical evaluation of methods for estimating the numerical density of synapses
de Groot, D. M. G., & Bierman, E. P. B. (1986) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(86)90113-5 · Cited by 83 · see citing works
Shamy, J. L., Buonocore, M. H., Makaron, L., Amaral, D. G., Barnes, C. A., & Rapp, P. R. (2005) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.07.019 · Cited by 77 · see citing works
Self-citationPreservation of Prefrontal Cortical Volume in Behaviorally Characterized Aged Macaque Monkeys
O'Donnell, K. A., Rapp, P. R., & Hof, P. R. (1999) · Experimental Neurology · doi:10.1006/exnr.1999.7192 · Cited by 68 · see citing works
Self-citationIn aging, is it gray or white?
Peters, A., & Rosene, D. L. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10715 · Cited by 62 · see citing works
Tigges, J., Herndon, J. G., & Rosene, D. L. (1996) · Cells Tissues Organs · doi:10.1159/000147867 · Cited by 46 · see citing works
Expertise and aging: maintaining skills through the lifespan
Horton, S., Baker, J. R., & Schorer, J. (2008) · European Review of Aging and Physical Activity · doi:10.1007/s11556-008-0034-5 · Cited by 35 · see citing works
Age-Related Cognitive Decline in the Rhesus Monkey
Moss, M. B., Killiany, R., & Herndon, J. G. (1999) · Cerebral cortex · doi:10.1007/978-1-4615-4885-0_2 · Cited by 31 · see citing works
Kopec, C. D., & Malinow, R. (2006) · Science · doi:10.1126/science.1137595 · Cited by 27 · see citing works
Chapter 33 The “psychic cell” of Ramón y Cajal
Goldman‐Rakic, P. S. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)36035-7 · Cited by 24 · see citing works
Theory and Application of Fluorescence Microscopy
Coling, D., & Kachar, B. (1997) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0201s00 · Cited by 19 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Hallmarks of Brain Aging: Adaptive and Pathological Modification by Metabolic States
Mattson, M. P., & Arumugam, T. V. (2018) · Cell Metabolism · doi:10.1016/j.cmet.2018.05.011 · Cited by 1,242 · see citing works
The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course
McEwen, B. S., & Morrison, J. H. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.028 · Cited by 1,079 · see citing works
Self-citationThe ageing cortical synapse: hallmarks and implications for cognitive decline
Morrison, J. H., & Baxter, M. G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3200 · Cited by 965 · see citing works
Self-citationStress weakens prefrontal networks: molecular insults to higher cognition
Arnsten, A. F. T. (2015) · Nature Neuroscience · doi:10.1038/nn.4087 · Cited by 752 · see citing works
Dendritic spine pathology in schizophrenia
Glausier, J. R., & Lewis, D. A. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.04.044 · Cited by 581 · see citing works
Arnsten, A. F. T., Wang, M. J., & Paspalas, C. D. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.038 · Cited by 538 · see citing works
Wang, M., Yang, Y., Wang, C.-J., Gamo, N. J., Jin, L. E., Mazer, J. A., Morrison, J. H., Wang, X.-J., & Arnsten, A. F. T. (2013) · Neuron · doi:10.1016/j.neuron.2012.12.032 · Cited by 489 · see citing works
Self-citationNeuronal basis of age-related working memory decline
Wang, M., Gamo, N. J., Yang, Y., Jin, L. E., Wang, X.-J., Laubach, M., Mazer, J. A., Lee, D., & Arnsten, A. F. T. (2011) · Nature · doi:10.1038/nature10243 · Cited by 485 · see citing works
A role for synaptic plasticity in the adolescent development of executive function
Selemon, L. D. (2013) · Translational Psychiatry · doi:10.1038/tp.2013.7 · Cited by 439 · see citing works
“Furthermore, mGluR LTD at postsynaptic sites in the hippocampus has been associated with large spines containing an abundance of AMPAR.128 Unlike the hippocampus where large mushroom spines are in the majority, thin, filopodial spines predominate in the PFC.129 Thus, strong evidence for mGluR in plasticity related to…”
BackgroundInfluentialCentral mechanisms of pain revealed through functional and structural MRI
Davis, K. D., & Moayedi, M. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-012-9386-8 · Cited by 376 · see citing works
Structural and synaptic plasticity in stress-related disorders
Christoffel, D. J., Golden, S. A., & Russo, S. J. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.044 · Cited by 334 · see citing works
Yan, Z., & Rein, B. (2022) · Molecular Psychiatry · doi:10.1038/s41380-021-01092-3 · Cited by 300 · see citing works
“The loss of thin spines in monkey PFC, which are particularly plastic and linked to learning, is selectively correlated with age-related cognitive impairment [241].”
BackgroundDendritic spine changes associated with normal aging
Dickstein, D. L., Weaver, C. M., Luebke, J. I., & Hof, P. R. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.09.077 · Cited by 289 · see citing works
Evidence for reduced experience-dependent dendritic spine plasticity in the aging prefrontal cortex
Bloss, E. B., Janssen, W. G., Ohm, D. T., Yuk, F. J., Wadsworth, S., Saardi, K. M., McEwen, B. S., & Morrison, J. H. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.0839-11.2011 · Cited by 219 · see citing works
Self-citationMorphological changes in nerve cells during normal aging
Pannese, E. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0308-y · Cited by 205 · see citing works
Altered synaptic dynamics during normal brain aging.
Mostany, R., Anstey, J. E., Crump, K. L., Maco, B., Knott, G., & Portera-Cailliau, C. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4825-12.2013 · Cited by 179 · see citing works
Ferrer, I. (2012) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.03.005 · Cited by 174 · see citing works
Kulijewicz‐Nawrot, M., Verkhratsky, A., Chvátal, A., Syková, E., & Rodríguez, J. J. (2012) · Journal of Anatomy · doi:10.1111/j.1469-7580.2012.01536.x · Cited by 160 · see citing works
Remodeling of axo-spinous synapses in the pathophysiology and treatment of depression
Licznerski, P., & Duman, R. S. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2012.09.057 · Cited by 157 · see citing works
Sustained remission from depressive-like behavior depends on hippocampal neurogenesis
Mateus-Pinheiro, A., Pinto, L., Bessa, J. M., Morais, M., Alves, N. D., Monteiro, S., Patrício, P., Almeida, O. F. X., & Sousa, N. (2013) · Translational Psychiatry · doi:10.1038/tp.2012.141 · Cited by 149 · see citing works
BDNF signaling during the lifetime of dendritic spines
Zagrebelsky, M., Tacke, C., & Korte, M. (2020) · Cell and Tissue Research · doi:10.1007/s00441-020-03226-5 · Cited by 147 · see citing works
A review of the structural alterations in the cerebral hemispheres of the aging rhesus monkey
Peters, A., & Kemper, T. (2012) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2011.11.015 · Cited by 135 · see citing works
Oligomeric Aβ in the monkey brain impacts synaptic integrity and induces accelerated cortical aging
Beckman, D., Ott, S., Donis-Cox, K., Janssen, W. G., Bliss-Moreau, E., Rudebeck, P. H., Baxter, M. G., & Morrison, J. H. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1902301116 · Cited by 111 · see citing works
Self-citationLongevity factor klotho enhances cognition in aged nonhuman primates
Castner, S. A., Gupta, S., Wang, D., Moreno, A. J., Park, C., Chen, C., Poon, Y., Groen, A., Greenberg, K., David, N., et al. (2023) · Nature Aging · doi:10.1038/s43587-023-00441-x · Cited by 114 · see citing works
Pereira, A. C., Lambert, H. K., Grossman, Y. S., Dumitriu, D., Waldman, R., Jannetty, S. K., Calakos, K., Janssen, W. G., McEwen, B. S., & Morrison, J. H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421285111 · Cited by 116 · see citing works
Self-citationAerobic glycolysis in the primate brain: Reconsidering the implications for growth and maintenance
Bauernfeind, A. L., Barks, S. K., Duka, T., Grossman, L. I., Hof, P. R., & Sherwood, C. C. (2014) · Brain Structure and Function · doi:10.1007/s00429-013-0662-z · Cited by 105 · see citing works
Dendritic Spines: Mediators of Cognitive Resilience in Aging and Alzheimer’s Disease
Walker, C. K., & Herskowitz, J. H. (2021) · The Neuroscientist · doi:10.1177/1073858420945964 · Cited by 86 · see citing works
Galvin, V. C., Yang, S. T., Paspalas, C. D., Yang, Y., Jin, L. E., Datta, D., Morozov, Y. M., Lightbourne, T. C., Lowet, A. S., Rakic, P., et al. (2020) · Neuron · doi:10.1016/j.neuron.2020.02.030 · Cited by 79 · see citing works
Datta, D., Leslie, S. N., Morozov, Y. M., Duque, A., Rakic, P., van Dyck, C. H., Nairn, A. C., & Arnsten, A. F. T. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-019-1683-1 · Cited by 76 · see citing works
Neural ageing and synaptic plasticity: prioritizing brain health in healthy longevity
Navakkode, S., & Kennedy, B. K. (2024) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2024.1428244 · Cited by 75 · see citing works
Molecular and cellular aspects of age-related cognitive decline and Alzheimer’s disease
Hullinger, R., & Puglielli, L. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2016.05.008 · Cited by 68 · see citing works
Three-dimensional synaptic Organization of Layer III of the human temporal neocortex
Cano-Astorga, N., DeFelipe, J., & Alonso-Nanclares, L. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab120 · Cited by 49 · see citing works
Arf4 Determines Dentate Gyrus-Mediated Pattern Separation by Regulating Dendritic Spine Development
Jain, S., Yoon, S. Y., Zhu, L., Brodbeck, J., Dai, J., Walker, D., & Huang, Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0046340 · Cited by 43 · see citing works
Bello-Medina, P. C., Prado-Alcalá, R. A., & Rivas-Arancibia, S. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.01.018 · Cited by 29 · see citing works
Masitinib for the Treatment of Alzheimer’s Disease
Ettcheto, M., Cano, A., Sanchez-López, E., Verdaguer, E., Folch, J., Auladell, C., & Camins, A. (2021) · Neurodegenerative Disease Management · doi:10.2217/nmt-2021-0019 · Cited by 28 · see citing works
Functional alterations of the prefrontal circuit underlying cognitive aging in mice
Chong, H. R., Ranjbar-Slamloo, Y., Ho, M. Z. H., Ouyang, X., & Kamigaki, T. (2023) · Nature Communications · doi:10.1038/s41467-023-43142-0 · Cited by 19 · see citing works
Chen, J.-R., Lim, S. H., Chung, S.-C., Lee, Y.-F., Wang, Y.-J., Tseng, G.-F., & Wang, T.-J. (2017) · Experimental Animals · doi:10.1538/expanim.16-0061 · Cited by 14 · see citing works
- Authors
- Dumitriu, D., Hao, J., Hara, Y., Kaufmann, J., Janssen, W. G. M., Lou, W., Rapp, P. R., & Morrison, J. H.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Hebei Medical University (CN)
- University of Toronto (CA)
- National Institutes of Health (US)
- Mount Sinai Hospital (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-06-02
- Volume
- 30
- Issue
- 22
- Pages
- 7507-7515
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2892969
- OpenAlex
- W2070524933
- Cited by
- 439
- References
- 53
- Citations by year
- 2026: 19 · 2025: 29 · 2024: 22 · 2023: 35 · 2022: 23 · 2021: 28 · 2020: 25 · 2019: 34 · 2018: 28 · 2017: 20 · 2016: 30 · 2015: 23 · 2014: 26 · 2013: 26 · 2012: 43
- FWCI
- 12.53
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute on Aging (AG 016765, AG 006647, R37AG010606, R01AG006647, P01AG016765, R01AG010606, AG010606, R37AG006647)
- National Institute of Mental Health (F30MH083402)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- age-associated memory impairment, aging, prefrontal cortex, dendritic spine morphology, synaptic density, pyramidal neurons, rhesus monkeys, area 46, delayed nonmatching-to-sample, delayed response, memory acquisition, synaptic plasticity, sex differences
- MeSH terms
- Age Factors, Aging, Animals, Cognition Disorders, Female, Macaca mulatta, Male, Neurons, Neuropsychological Tests, Reaction Time, Synapses, Linear Models, Prefrontal Cortex, Recognition, Psychology, Microscopy, Electron, Transmission, 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