Cited by 1,153Point processes and geometric inequalitiesMemory and Neural MechanismsClassical Anatomy and Histology

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Unbiased stereological estimation of the number of neurons in the human hippocampus

West, Mark J., Gundersen, H. J. G.·1990·Journal of Comparative Neurology

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Abstract

The total numbers of neurons in five subdivisions of human hippocampi were estimated using unbiased Stereological principles and systematic sampling techniques. The method addresses the problems associated with the results and conclusions of previous quantitative studies, virtually all of which have been based on biased estimates of neuron densities. For each subdivision, the total number of neurons was calculated as the product of the estimate of the volume of the neuron‐containing layers and the estimate of the numerical density of neurons in the layers. Each hippocampus was cut into 3‐mm‐thick slabs, transverse to the rostrocaudal axis. One 70‐μUm‐thick section from each slab was used in the analysis. The volumes of the layers containing neurons in five major subdivisions of the hippocampus (granule cell layer, hilus, CA3–2, CA1, and subiculum) were estimated with point‐counting techniques after delineation of the layers on each section. The numerical densities of neurons in each subdivision were estimated on the same sections with optical directors. The sampling used in both estimates was performed systematically in all three dimensions. In an example of five hippocampi, the mean numbers of neurons (CV = SD/mean) in the different subdivisions were as follows: granule cells 15 × 10 6 (0.28), hilus 2.0 × 10 6 (0.16), CA3‐2 2.7 × 10 6 (0.22), CA1 16 × 10 6 (0.32), subiculum 4.5 × 10 6 (0.19). The stereological measurements contributed approximately 25% of the observed variance. Among the five subjects there was a significant inverse relationship between age (which ranged from 47 to 85 years) and the total number of neurons in CA1 (which ranged from 24 to 11 × 10 6). An optimized sampling scheme for studies of the number of neurons in the human hippocampus has been designed on the basis of an analysis of variance of the estimates at different levels of the sampling scheme. Counting neurons in the five subdivisions of the human hippocampus with the optimized sampling scheme takes less than 4 hours.

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Background
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Method
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Background
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Background
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“10 (West and Gundersen, 1990).”
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Method
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Method
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Self-citation
Huntington's Disease (HD): Neurodegeneration of Brodmann's Primary Visual Area 17 (BA17)
Rüb, U., Seidel, K., Vonsattel, J. P., Lange, H. W., Eisenmenger, W., Götz, M., Turco, D. D., Bouzrou, M., Korf, H., & Heinsen, H. (2014) · Brain Pathology · doi:10.1111/bpa.12237 · Cited by 30
Asymmetric Direct Reciprocal Connections Between Primary Visual and Somatosensory Cortices of the Mouse
Massé, I. O., Ross, S., Bronchti, G., & Boire, D. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw239 · Cited by 31
Mitochondrial Complex I Reversible S-Nitrosation Improves Bioenergetics and Is Protective in Parkinson's Disease
Milanese, C., Tapias, V., Gabriels, S., Cerri, S., Levandis, G., Blandini, F., Tresini, M., Shiva, S., Greenamyre, J. T., Gladwin, M. T., et al. (2017) · Antioxidants and Redox Signaling · doi:10.1089/ars.2017.6992 · Cited by 27
“The coefficient of error was calculated according to West and Gundersen as described earlier, and values were 0.10 in all cases.”
MethodInfluential
Life and Death of Immature Neurons in the Juvenile and Adult Primate Amygdala
Chareyron, L. J., Lavenex, P. B., Amaral, D. G., & Lavenex, P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22136691 · Cited by 27
“We estimated the volume of the amygdala nuclei (lateral, basal, and paralaminar) according to the Cavalieri principle on Nissl-stained sections [90,91].”
Method
Functional deficits and morphological changes in the neurogenic bladder match the severity of spinal cord compression
Özsoy, Ö., Özsoy, U., Stein, G., Semler, O., Skouras, E., Schempf, G., Wellmann, K., Wirth, F., Angelova, S. K., Ankerne, J., et al. (2012) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-2012-110203 · Cited by 28
“The total lesion volume was calculated using the Cavalieri method (Gundersen and Jensen, 1987; Gundersen, 1988; West and Gundersen, 1990).”
Method
The hippocampus of the eastern rock sengi: cytoarchitecture, markers of neuronal function, principal cell numbers, and adult neurogenesis
Slomianka, L., Drenth, T., Cavegn, N., Menges, D., Lazic, S., Phalanndwa, M., Chimimba, C., & Amrein, I. (2013) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00034 · Cited by 24
“To obtain the estimates, we used the optical fractionator method (West et al., 1991) with StereoInvestigator 10 software (MBF Bioscience, Williston, VT, USA).”
Method
Glutamate and dopamine synaptic terminals in extended amygdala after 14-week chronic alcohol drinking in inbred alcohol-preferring rats
Zhou, F., Sahr, R. N., Sari, Y., & Behbahani, K. (2006) · Alcohol · doi:10.1016/j.alcohol.2006.06.013 · Cited by 28
Taxonomic Separation of Hippocampal Networks: Principal Cell Populations and Adult Neurogenesis
van Dijk, R. M., Huang, S., Slomianka, L., & Amrein, I. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00022 · Cited by 27
“Ki67- and DCX-positive cells were quantified under a x63 oilimmersion lens and either counted manually and exhaustively (Ki67) but avoiding cells in the top focal plane of the section or by using the optical Fractionator (DCX).”
MethodInfluential
Neuroprotective effects of Nigella sativa extract upon the hippocampus in PTU-induced hypothyroidism juvenile rats: A stereological study
Asiaei, F., Fazel, A., Rajabzadeh, A., Hosseini, M., Beheshti, F., & Seghatoleslam, M. (2017) · Metabolic Brain Disease · doi:10.1007/s11011-017-0025-1 · Cited by 28
“Volumemeasurements as well as, TUNEL positive cell and dark neuron estimation were performed in the right hippocampus of rats using the unbiased stereological principles (West and Gundersen 1990; Pourzaki et al. 2017).”
Method
A concise review of optical, physical and isotropic fractionator techniques in neuroscience studies, including recent developments
Deniz, Ö. G., Altun, G., Kaplan, A. A., Yurt, K. K., von Bartheld, C. S., & Kaplan, S. (2018) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2018.07.012 · Cited by 28
“Additionally, the sampling strategy is a combination of the area-sampling fraction (asf), which is obtained from the x- and y-axis movement of the counting frame on the areas of the section sampling fraction (ssf) and the thickness-sampling fraction (tsf) (West and Gundersen, 1990).”
BackgroundMethodInfluential
D2 Dopamine receptor blockade results in sprouting of DA axons in the intact animal but prevents sprouting following nigral lesions
Tripanichkul, W., Stanić, D., Drago, J., Finkelstein, D. I., & Horne, M. K. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02547.x · Cited by 28
Call type-specific differences in vocalization-related afferents to the periaqueductal gray of squirrel monkeys (Saimiri sciureus)
Gruber-Dujardin, E., & Jürgens, U. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.10.006 · Cited by 30
Intramuscular Injection of Hypertonic Saline: In vitro and in vivo Muscle Tissue Toxicity and Spinal Neurone c‐fos Expression
Svendsen, O., Edwards, C. N., Lauritzen, B., & Rasmussen, A. D. (2005) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2005.pto_97108.x · Cited by 28
Sex difference in the 24-h acetylcholine release profile in the premotor/supplementary motor area of behaving rats
Takase, K., Mitsushima, D., Funabashi, T., & Kimura, F. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.001 · Cited by 29
Developmental Alcohol Exposure Alters Light‐Induced Phase Shifts of the Circadian Activity Rhythm in Rats
Farnell, Y. Z., West, J. R., Chen, W. A., Allen, G. C., & Earnest, D. J. (2004) · Alcoholism Clinical and Experimental Research · doi:10.1097/01.alc.0000130807.21020.1b · Cited by 28
“The Vref was determined by point counting and application of Cavalieri’s principle (Gundersen et al., 1988), and SCN neuronal density was determined by using the optical disector method (Gundersen et al., 1988; West and Gundersen, 1990).”
Method
Experimental Models of Partial Lesion of Rat Spinal Cord to Investigate Neurodegeneration, Glial Activation, and Behavior Impairments
Chadi, G., de Andrade, M. S. R., Leme, R. J. D. A., & Gomide, V. C. (2001) · International Journal of Neuroscience · doi:10.3109/00207450108994227 · Cited by 28
Compensatory regulation of striatal neuropeptide gene expression occurs before changes in metabolic activity of basal ganglia nuclei
Meissner, W. G., Doveró, S., Bioulac, B. H., Gross, C. E., & Bézard, E. (2003) · Neurobiology of Disease · doi:10.1016/s0969-9961(03)00011-1 · Cited by 28
“Unbiased stereological techniques were used to estimate cell number in the SNc (Gundersen et al., 1988; West and Gundersen, 1990; West, 1999) as previously described (Gross et al.”
Method
Changes in spatial memory mediated by experimental variation in food supply do not affect hippocampal anatomy in mountain chickadees (Poecile gambeli)
Витальевич, П. В., Lavenex, P., & Clayton, N. S. (2002) · Journal of Neurobiology · doi:10.1002/neu.10045 · Cited by 28
“In accordance with the Cavalieri principle (Gundersen and Jensen, 1987; West and Gundersen, 1990), we chose the first section randomly from the first four sections containing the hippocampus.”
Mechanisms of Neuron Loss in Alzheimer’s Disease
Mukhin, V. N., Pavlov, K. I., & Klimenko, V. M. (2017) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-017-0427-x · Cited by 27
Inducible knockout of Mef2a, ‐c, and ‐d from nestin‐expressing stem/progenitor cells and their progeny unexpectedly uncouples neurogenesis and dendritogenesis in vivo
Latchney, S. E., Jiang, Y., Petřík, D., Eisch, A. J., & Hsieh, J. (2015) · The FASEB Journal · doi:10.1096/fj.15-275651 · Cited by 27
“Because the raw counts (before multiplication) for immunopositive cells counted were low according to dissector/fractionator standards (22, 23), we used an area sampling fraction of 1, as is commonly used for countingrare cell populations(13,24).”
Method
Genetic and pharmacological evidence that endogenous nociceptin/orphanin FQ contributes to dopamine cell loss in Parkinson's disease
Arcuri, L., Viaro, R., Bido, S., Longo, F., Calcagno, M., Fernagut, P., Zaveri, N. T., Calò, G., Bézard, E., & Morari, M. (2016) · Neurobiology of Disease · doi:10.1016/j.nbd.2016.01.016 · Cited by 27
Conditional Deletion of PDK1 in the Forebrain Causes Neuron Loss and Increased Apoptosis during Cortical Development
Xu, C., Yu, L., Hou, J., Jackson, R. J., Wang, H., Huang, C., Liu, T., Wang, Q., Zou, X., Morris, R., et al. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00330 · Cited by 29
“It was based on an unbiased stereological neuron counting technique (West and Gundersen, 1990).”
Method
A detailed anatomical and mathematical model of the hippocampal formation for the generation of sharp-wave ripples and theta-nested gamma oscillations
Aussel, A., Buhry, L., Tyvaert, L., & Ranta, R. (2018) · Journal of Computational Neuroscience · doi:10.1007/s10827-018-0704-x · Cited by 30
Effect of Local Anaesthesia on Neuronal c-fos Expression in the Spinal Dorsal Horn and Hypothalamic Paraventricular Nucleus after Surgery in Rats
Stenberg, C., Ovlisen, K., Svendsen, O., & Lauritzen, B. (2005) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2005.pto_07.x · Cited by 27
Matrix metalloproteinase 9 regulates cell death following pilocarpine-induced seizures in the developing brain
Hoehna, Y., Uckermann, O., Luksch, H., Stefovska, V. G., Marzahn, J., Theil, M., Górkiewicz, T., Gawlak, M., Wilczynski, G. M., Kaczmarek, L., et al. (2012) · Neurobiology of Disease · doi:10.1016/j.nbd.2012.06.023 · Cited by 27
Testosterone metabolites differentially maintain adult morphology in a sexually dimorphic neuromuscular system
Verhovshek, T., Buckley, K. M., Sergent, M. A., & Sengelaub, D. R. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20780 · Cited by 27
“Estimates of the total number of labeled SNB motoneurons were obtained using the optical disector method outlined by Coggeshall (1992) and a procedure similar to that of West and Gundersen (1990).”
Method
Relative neuron loss in hippocampal sclerosis of aging and Alzheimer's disease
Ihara, R., Vincent, B. D., Baxter, M. R., Franklin, E. E., Hassenstab, J. J., Xiong, C., Morris, J. C., & Cairns, N. J. (2018) · Annals of Neurology · doi:10.1002/ana.25344 · Cited by 28
“The “disector” probe was used to estimate neuron numbers.(21,22) The boundary between CA1 and the subiculum was operationalized by using a line perpendicular to a line connecting both termini of the dentate gyrus and through the apex of the curve of CA2 and CA3.”
Method
Hippocampal expression of cell‐adhesion glycoprotein neuroplastin is altered in Alzheimer's disease
Ilić, K., Mlinac, K., Milošević, N. J., Šimić, G., Habek, N., Bogdanović, N., & Bognar, S. K. (2018) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13998 · Cited by 27
“Left hippocampi were cut in rostrocaudal direction, with a random position for the first cut within the first rostral 3 mm, as previously described.(17) Twelve micrometers thick sections were used for both Nissl staining and immunohistochemistry.”
Method
Nonvolatile Memory and Artificial Synapse Based on the Cu/P(VDF-TrFE)/Ni Organic Memtranstor
Lu, P., Shen, J., Shang, D., & Sun, Y. (2020) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.9b19510 · Cited by 27
Alcohol exposure on postnatal day 5 induces Purkinje cell loss and evidence of Purkinje cell degradation in lobule I of rat cerebellum
Lee, Y., Rowe, J. H., Eskue, K., West, J. R., & Maier, S. E. (2008) · Alcohol · doi:10.1016/j.alcohol.2008.01.010 · Cited by 27
AIDS does not alter the total number of neurons in the hippocampal formation but induces cell atrophy: a stereological study
Sá, M. J., Madeira, M. D., Ruela, C., Volk, B., Mota‐Miranda, A., Lecour, H., Gonçalves, V., & Paula-Barbosa, M. M. (2000) · Acta Neuropathologica · doi:10.1007/s004010051175 · Cited by 27
“The boundaries of the layers, defined on the basis of their cytoarchitectonic organization [ 44 , 46], were outlined with the help of a camera lucida attachment and a 〈 3 objective lens.”
MethodResultInfluential
Nerve cell loss in the thalamic mediodorsal nucleus in Huntington's disease. II. Optimization of a stereological estimation procedure
Schmitz, C., Rüb, U., Korr, H., & Heinsen, H. (1999) · Acta Neuropathologica · doi:10.1007/s004010051038 · Cited by 27
“Concerning the latter method, it is important to take into account that balancing of random errors of estimated total numbers of particles (i.e., CEs) against interindividual variabilities of true total numbers of particles (i.e., CVs) requires a precise prediction of CE. However, the predicting methods described in […”
Influential
Prenatal development of the retinohypothalamic pathway and the suprachiasmatic nucleus in the sheep
Torrealba, F., Parraguez, V. H., Reyes, T. P., Valenzuela, G. J., & Serón‐Ferré, M. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903380212 · Cited by 27
Repression of proinflammatory cytokine and inducible nitric oxide synthase (NOS2) gene expression in activated microglia by N-acetyl-O-methyldopamine: Protein kinase a-dependent mechanism
Cho, S., Kim, Y., Cruz, M. O., Park, E., Chu, C. K., Song, G., & JOH, T. H. (2001) · Glia · doi:10.1002/1098-1136(20010315)33:4 · Cited by 39
Viral-based rodent and nonhuman primate models of multiple system atrophy: Fidelity to the human disease
Marmion, D. J., Rutkowski, A., Chatterjee, D., Hiller, B. M., Werner, M. H., Bézard, E., Kirik, D., McCown, T. J., Gray, S. J., & Kordower, J. H. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105184 · Cited by 26
“Stereology: Unbiased stereological counting methods [102] using the Stereo Investigator”
Method
Prolonged release of VEGF and Ang1 from intralesionally implanted hydrogel promotes perilesional vascularization and functional recovery after experimental ischemic stroke
Yanev, P. G., van Tilborg, G. A. F., van der Toorn, A., Kong, X., Stowe, A. M., & Dijkhuizen, R. M. (2022) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1177/0271678x211069927 · Cited by 26
“The optical fractionator design was used to estimate the numbers (N) of NeuN-positive cells and vessel branching points.(55) Each ROI was systematically, uniformly and randomly sampled in the section plane (the x-y plane) and across the thickness of the sections (the z-axis), superimposing a grid of 3D optical dissect…”
Method

Authors: West, M. J., & Gundersen, H. J. G.
Affiliations: Aarhus University (DK)
Corresponding author: West, Mark J.
ORCID: West, Mark J.
Venue: Journal of Comparative Neurology
Publisher: Wiley
Published: 1990-06
Volume: 296
Issue: 1
Pages: 1-22
ISSN: 0021-9967 (ISSN-L)
1096-9861
DOI: 10.1002/cne.902960102
OpenAlex: W2014892312
Cited by: 1,153
References: 47
Citations by year: 2026: 7 · 2025: 13 · 2024: 10 · 2023: 17 · 2022: 24 · 2021: 22 · 2020: 24 · 2019: 19 · 2018: 40 · 2017: 27 · 2016: 32 · 2015: 30 · 2014: 38 · 2013: 40 · 2012: 41
FWCI: 46.01
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 5244 d)
Locations: The Journal of Comparative Neurology (publishedVersion)
PubMed (publishedVersion)
Funders: Sundhed og Sygdom, Det Frie Forskningsråd
Topics: Physical Sciences › Mathematics › Applied Mathematics › Point processes and geometric inequalities
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Health Sciences › Medicine › Anatomy › Classical Anatomy and Histology
Keywords: human hippocampus, neuron number estimation, neuronal density, unbiased stereology, optical disector, point counts, CA1, CA3, subiculum, granular layer, hilus, age-related neuronal loss
MeSH terms: Aged, Aged, 80 and over, Cell Count, Hippocampus, Humans, Middle Aged

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Unbiased stereological estimation of the number of neurons in the human hippocampus

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