Shades of gray in human white matter.

NADPH-d subcortical subplate white matter neurons

Journal

The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041

Informations de publication

Date de publication:
27 Jun 2023
Historique:
revised: 22 05 2023
received: 20 02 2023
accepted: 31 05 2023
pubmed: 28 6 2023
medline: 28 6 2023
entrez: 28 6 2023
Statut: aheadofprint

Résumé

Anatomists have long expressed interest in neurons of the white matter, which is by definition supposed to be free of neurons. Hypotheses regarding their biochemical signature and physiological function are mainly derived from animal models. Here, we investigated 15 whole-brain human postmortem specimens, including cognitively normal cases and those with pathologic Alzheimer's disease (AD). Quantitative and qualitative methods were used to investigate differences in neuronal size and density, and the relationship between neuronal processes and vasculature. Double staining was used to evaluate colocalization of neurochemicals. Two topographically distinct populations of neurons emerged: one appearing to arise from developmental subplate neurons and the other embedded within deep, subcortical white matter. Both populations appeared to be neurochemically heterogeneous, showing positive reactivity to acetylcholinesterase (AChE) [but not choline acetyltransferase (ChAT)], neuronal nuclei (NeuN), nicotinamide adenine dinucleotide phosphate-diaphorase (NADPH-d), microtubule-associated protein 2 (MAP-2), somatostatin (SOM), nonphosphorylated neurofilament protein (SMI-32), and calcium-binding proteins calbindin-D

Identifiants

pubmed: 37376715
doi: 10.1002/cne.25512
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIA NIH HHS
ID : F31AG07631
Pays : United States
Organisme : NIA NIH HHS
ID : P30AG072977
Pays : United States
Organisme : NIA NIH HHS
ID : R01AG062566
Pays : United States
Organisme : NINDS NIH HHS
ID : T32NS047987
Pays : United States
Organisme : NIA NIH HHS
ID : F31AG07631
Pays : United States
Organisme : NIA NIH HHS
ID : P30AG072977
Pays : United States
Organisme : NIA NIH HHS
ID : R01AG062566
Pays : United States
Organisme : NINDS NIH HHS
ID : T32NS047987
Pays : United States

Informations de copyright

© 2023 The Authors. The Journal of Comparative Neurology published by Wiley Periodicals LLC.

Références

Ascoli, G. A., Alonso-Nanclares, L., Anderson, S. A., Barrionuevo, G., Benavides-Piccione, R., Burkhalter, A., Buzsáki, G., Cauli, B., Defelipe, J., Fairén, A., Feldmeyer, D., Fishell, G., Fregnac, Y., Freund, T. F., Gardner, D., Gardner, E. P., Goldberg, J. H., Helmstaedter, M., Hestrin, S., … Yuste, R. (2008). Petilla terminology: Nomenclature of features of GABAergic interneurons of the cerebral cortex. Nature Reviews Neuroscience, 9(7), 557-568. https://doi.org/10.1038/nrn2402
Balasubramanian, A. B., Kawas, C. H., Peltz, C. B., Brookmeyer, R., & Corrada, M. M. (2012). Alzheimer disease pathology and longitudinal cognitive performance in the oldest-old with no dementia. Neurology, 79(9), 915-921. https://doi.org/10.1212/WNL.0b013e318266fc77
Bankhead, P., Loughrey, M. B., Fernández, J. A., Dombrowski, Y., McArt, D. G., Dunne, P. D., McQuaid, S., Gray, R. T., Murray, L. J., Coleman, H. G., James, J. A., Salto-Tellez, M., & Hamilton, P. W. (2017). QuPath: Open source software for digital pathology image analysis. Scientific Reports, 7(1), 16878. https://doi.org/10.1038/s41598-017-17204-5
Barbaresi, P., Fabri, M., & Mensà, E. (2014). Characterization of NO-producing neurons in the rat corpus callosum. Brain and Behavior, 4(3), 317-336. https://doi.org/10.1002/brb3.218
Barbaresi, P., Mensà, E., Lariccia, V., Desiato, G., Fabri, M., & Gratteri, S. (2015). Intracallosal neuronal nitric oxide synthase neurons colocalize with neurokinin 1 substance P receptor in the rat. Journal of Comparative Neurology, 523(4), 589-607. https://doi.org/10.1002/cne.23695
Blottner, D., Grozdanovic, Z., & Gossrau, R. (1995). Histochemistry of nitric oxide synthase in the nervous system. Histochemical Journal, 27(10), 785-811.
Braak, H., & Braak, E. (1995). Staging of Alzheimer's disease-related neurofibrillary changes. Neurobiology of Aging, 16(3), 271-278. discussion 278-284. https://doi.org/10.1016/0197-4580(95)00021-6
Bu, J., Sathyendra, V., Nagykery, N., & Geula, C. (2003). Age-related changes in calbindin-D28k, calretinin, and parvalbumin-immunoreactive neurons in the human cerebral cortex. Experimental Neurology, 182(1), 220-231. https://doi.org/10.1016/s0014-4886(03)00094-3
Cebada-Sánchez, S., Marcos Rabal, P., Insausti, A. M., & Insausti, R. (2018). Postnatal development of NPY and somatostatin-28 peptidergic populations in the human angular bundle. Frontiers in Neuroanatomy, 12, 116. https://doi.org/10.3389/fnana.2018.00116
Chun, J. J., & Shatz, C. J. (1989). Interstitial cells of the adult neocortical white matter are the remnant of the early generated subplate neuron population. Journal of Comparative Neurology, 282(4), 555-569. https://doi.org/10.1002/cne.902820407
DeRuiter, M. C., Poelmann, R. E., VanMunsteren, J. C., Mironov, V., Markwald, R. R., & Gittenberger-de Groot, A. C. (1997). Embryonic endothelial cells transdifferentiate into mesenchymal cells expressing smooth muscle actins in vivo and in vitro. Circulation Research, 80(4), 444-451. https://doi.org/10.1161/01.res.80.4.444
Estrada, C., & DeFelipe, J. (1998). Nitric oxide-producing neurons in the neocortex: Morphological and functional relationship with intraparenchymal microvasculature. Cerebral Cortex, 8(3), 193-203. https://doi.org/10.1093/cercor/8.3.193
Estrada, C., Mengual, E., & González, C. (1993). Local NADPH-diaphorase neurons innervate pial arteries and lie close or project to intracerebral blood vessels: A possible role for nitric oxide in the regulation of cerebral blood flow. Journal of Cerebral Blood Flow and Metabolism, 13(6), 978-984. https://doi.org/10.1038/jcbfm.1993.122
Garcia-Marin, V., Blazquez-Llorca, L., Rodriguez, J. R., Gonzalez-Soriano, J., & DeFelipe, J. (2010). Differential distribution of neurons in the gyral white matter of the human cerebral cortex. Journal of Comparative Neurology, 518(23), 4740-4759. https://doi.org/10.1002/cne.22485
Geula, C., Mesulam, M. M., Saroff, D. M., & Wu, C. K. (1998). Relationship between plaques, tangles, and loss of cortical cholinergic fibers in Alzheimer disease. Journal of Neuropathology and Experimental Neurology, 57(1), 63-75. https://doi.org/10.1097/00005072-199801000-00008
Geula, C., Schatz, C. R., & Mesulam, M. M. (1993). Differential localization of NADPH-diaphorase and calbindin-D28k within the cholinergic neurons of the basal forebrain, striatum and brainstem in the rat, monkey, baboon and human. Neuroscience, 54(2), 461-476. https://doi.org/10.1016/0306-4522(93)90266-i
Gonchar, Y., Wang, Q., & Burkhalter, A. (2007). Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Frontiers in Neuroanatomy, 1, 3. https://doi.org/10.3389/neuro.05.003.2007
Gorno-Tempini, M. L., Hillis, A. E., Weintraub, S., Kertesz, A., Mendez, M., Cappa, S. F., Ogar, J. M., Rohrer, J. D., Black, S., Boeve, B. F., Manes, F., Dronkers, N. F., Vandenberghe, R., Rascovsky, K., Patterson, K., Miller, B. L., Knopman, D. S., Hodges, J. R., Mesulam, M. M., & Grossman, M. (2011). Classification of primary progressive aphasia and its variants. Neurology, 76(11), 1006-1014. https://doi.org/10.1212/WNL.0b013e31821103e6
Judaš, M., Sedmak, G., Pletikos, M., & Jovanov-Milošević, N. (2010). Populations of subplate and interstitial neurons in fetal and adult human telencephalon. Journal of Anatomy, 217(4), 381-399. https://doi.org/10.1111/j.1469-7580.2010.01284.x
Judas, M., Sestan, N., & Kostović, I. (1999). Nitrinergic neurons in the developing and adult human telencephalon: Transient and permanent patterns of expression in comparison to other mammals. Microscopy Research and Technique, 45(6), 401-419. https://doi.org/10.1002/(sici)1097-0029(19990615)45:6<401::Aid-jemt7>3.0.Co;2-q
Kim, E. J., Brown, J. A., Deng, J., Hwang, J. L., Spina, S., Miller, Z. A., DeMay, M. G., Valcour, V., Karydas, A., Ramos, E. M., Coppola, G., Miller, B. L., Rosen, H. J., Seeley, W. W., & Grinberg, L. T. (2018). Mixed TDP-43 proteinopathy and tauopathy in frontotemporal lobar degeneration: Nine case series. Journal of Neurology, 265(12), 2960-2971. https://doi.org/10.1007/s00415-018-9086-2
Kostovic, I., & Rakic, P. (1980). Cytology and time of origin of interstitial neurons in the white matter in infant and adult human and monkey telencephalon. Journal of Neurocytology, 9(2), 219-242. https://doi.org/10.1007/BF01205159
Kostović, I., Stefulj-Fucić, A., Mrzljak, L., Jukić, S., & Delalle, I. (1991). Prenatal and perinatal development of the somatostatin-immunoreactive neurons in the human prefrontal cortex. Neuroscience Letters, 124(2), 153-156. https://doi.org/10.1016/0304-3940(91)90082-5
Kowall, N. W., & Beal, M. F. (1988). Cortical somatostatin, neuropeptide Y, and NADPH diaphorase neurons: Normal anatomy and alterations in Alzheimer's disease. Annals of Neurology, 23(2), 105-114. https://doi.org/10.1002/ana.410230202
Lamerand, S., Shahidehpour, R., Ayala, I., Gefen, T., Mesulam, M. M., Bigio, E., & Geula, C. (2020). Calbindin-D(28K), parvalbumin, and calretinin in young and aged human locus coeruleus. Neurobiology of Aging, 94, 243-249. https://doi.org/10.1016/j.neurobiolaging.2020.06.006
Mesulam, M., & Geula, C. (1991). Differential distribution of a neurofilament protein epitope in acetylcholinesterase-rich neurons of human cerebral neocortex. Brain Research, 544(1), 169-173. https://doi.org/10.1016/0006-8993(91)90901-7
Mesulam, M., Shaw, P., Mash, D., & Weintraub, S. (2004). Cholinergic nucleus basalis tauopathy emerges early in the aging-MCI-AD continuum. Annals of Neurology, 55(6), 815-828. https://doi.org/10.1002/ana.20100
Mesulam, M. M. (2003). Primary progressive aphasia: A language-based dementia. The New England Journal of Medicine, 349(16), 1535-1542. https://doi.org/10.1056/NEJMra022435
Mesulam, M. M., & Geula, C. (1988). Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: Observations based on the distribution of acetylcholinesterase and choline acetyltransferase. Journal of Comparative Neurology, 275(2), 216-240. https://doi.org/10.1002/cne.902750205
Meyer, G., Wahle, P., Castaneyra-Perdomo, A., & Ferres-Torres, R. (1992). Morphology of neurons in the white matter of the adult human neocortex. Experimental Brain Research, 88(1), 204-212. https://doi.org/10.1007/BF02259143
Meynert, T. (1867). Der Bau der Gross-Hirnrinde und seine örtlichen Verschiedenheiten, nebst einem pathologisch-anatomischen Corollarium: Separat-Abdruck aus der“ Vierteljahrsschrift für Psychiatrie etc.” Heuser.
Montine, T. J., Phelps, C. H., Beach, T. G., Bigio, E. H., Cairns, N. J., Dickson, D. W., Duyckaerts, C., Frosch, M. P., Masliah, E., Mirra, S. S., Nelson, P. T., Schneider, J. A., Thal, D. R., Trojanowski, J. Q., Vinters, H. V., & Hyman, B. T. (2012). National Institute on Aging-Alzheimer's Association guidelines for the neuropathologic assessment of Alzheimer's disease: A practical approach. Acta Neuropathologica, 123(1), 1-11. https://doi.org/10.1007/s00401-011-0910-3
Mortazavi, F., Romano, S. E., Rosene, D. L., & Rockland, K. S. (2017). A survey of white matter neurons at the gyral crowns and sulcal depths in the rhesus monkey. Frontiers in Neuroanatomy, 11, 69. https://doi.org/10.3389/fnana.2017.00069
Mortazavi, F., Wang, X., Rosene, D. L., & Rockland, K. S. (2016). White matter neurons in young adult and aged rhesus monkey. Frontiers in Neuroanatomy, 10, 15. https://doi.org/10.3389/fnana.2016.00015
Nassif, C., Kawles, A., Ayala, I., Minogue, G., Gill, N. P., Shepard, R. A., Zouridakis, A., Keszycki, R., Zhang, H., Mao, Q., Flanagan, M. E., Bigio, E. H., Mesulam, M. M., Rogalski, E., Geula, C., & Gefen, T. (2022). Integrity of neuronal size in the entorhinal cortex is a biological substrate of exceptional cognitive aging. Journal of Neuroscience, 42(45), 8587-8594. https://doi.org/10.1523/jneurosci.0679-22.2022
Rockland, K. S., & Nayyar, N. (2012). Association of type I neurons positive for NADPH-diaphorase with blood vessels in the adult monkey corpus callosum. Frontiers in Neural Circuits, 6, 4. https://doi.org/10.3389/fncir.2012.00004
Sedmak, G., & Judaš, M. (2019). The total number of white matter interstitial neurons in the human brain. Journal of Anatomy, 235(3), 626-636. https://doi.org/10.1111/joa.13018
Sedmak, G., & Judaš, M. (2021). White matter interstitial neurons in the adult human brain: 3% of cortical neurons in quest for recognition. Cells, 10(1), 190. https://doi.org/10.3390/cells10010190
Selden, N., Geula, C., Hersh, L., & Mesulam, M. M. (1994). Human striatum: Chemoarchitecture of the caudate nucleus, putamen and ventral striatum in health and Alzheimer's disease. Neuroscience, 60(3), 621-636. https://doi.org/10.1016/0306-4522(94)90491-x
Smiley, J. F., Levey, A. I., & Mesulam, M. M. (1998). Infracortical interstitial cells concurrently expressing m2-muscarinic receptors, acetylcholinesterase and nicotinamide adenine dinucleotide phosphate-diaphorase in the human and monkey cerebral cortex. Neuroscience, 84(3), 755-769. https://doi.org/10.1016/s0306-4522(97)00524-1
Suarez-Sola, M. L., Gonzalez-Delgado, F. J., Pueyo-Morlans, M., Medina-Bolivar, O. C., Hernandez-Acosta, N. C., Gonzalez-Gomez, M., & Meyer, G. (2009). Neurons in the white matter of the adult human neocortex. Frontiers in Neuroanatomy, 3, 7. https://doi.org/10.3389/neuro.05.007.2009
Tao, Z., Van Gool, D., Lammens, M., & Dom, R. (1999). NADPH-diaphorase-containing neurons in cortex, subcortical white matter and neostriatum are selectively spared in Alzheimer's disease. Dementia and Geriatric Cognitive Disorders, 10(6), 460-468. https://doi.org/10.1159/000017190
Wood, J., & Garthwaite, J. (1994). Models of the diffusional spread of nitric oxide: Implications for neural nitric oxide signalling and its pharmacological properties. Neuropharmacology, 33(11), 1235-1244. https://doi.org/10.1016/0028-3908(94)90022-1

Auteurs

Antonia Zouridakis (A)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Ivan Ayala (I)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Grace Minogue (G)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Allegra Kawles (A)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Rachel Keszycki (R)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Alyssa Macomber (A)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Eileen H Bigio (EH)

Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Changiz Geula (C)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
Department of Cell and Developmental Biology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Marek-Marsel Mesulam (MM)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Tamar Gefen (T)

Mesulam Center for Cognitive Neurology and Alzheimer's Disease, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.
Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, Chicago, Illinois, USA.

Classifications MeSH