Cellular components of the human medial amygdaloid nucleus
Open accessAbstract
The medial nucleus (Me) is a superficial component of the amygdaloid complex. Here we assessed the density and morphology of the neurons and glial cells, the glial fibrillary acidic protein (GFAP) immunoreactivity, and the ultrastructure of the synaptic sites in the human Me. The optical fractionator method was applied. The Me presented an estimated mean neuronal density of 1.53 × 10 5 neurons/mm 3(greater in the left hemisphere), more glia (72% of all cells) than neurons, and a nonneuronal:neuronal ratio of 2.7. Golgi‐impregnated neurons had round or ovoid, fusiform, angular, and polygonal cell bodies (10–30 μm in diameter). The length of the dendrites varied, and pleomorphic spines were found in sparsely spiny or densely spiny cells (1.5–5.2 spines/dendritic μm). The axons in the Me neuropil were fine or coarsely beaded, and fibers showed simple or notably complex collateral terminations. The protoplasmic astrocytes were either isolated or formed small clusters and showed GFAP‐immunoreactive cell bodies and multiple branches. Furthermore, we identified both asymmetrical (with various small, clear, round, electron‐lucent vesicles and, occasionally, large, dense‐core vesicles) and symmetrical (with small, flattened vesicles) axodendritic contacts, also including multisynaptic spines. The astrocytes surround and may compose tripartite or tetrapartite synapses, the latter including the extracellular matrix between the pre‐ and the postsynaptic elements. Interestingly, the terminal axons exhibited a glomerular‐like structure with various asymmetrical contacts. These new morphological data on the cellular population and synaptic complexity of the human Me can contribute to our knowledge of its role in health and pathological conditions. J. Comp. Neurol. 521:589–611, 2013. © 2012 Wiley Periodicals, Inc.
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In adulthood, mature PNNs regulate synaptic functions representing the fourth element of the 'tetrapartite' synapse.
“In adulthood, mature PNNs regulate synaptic functions representing the fourth element of what has been termed the ‘tetrapartite' synapse.85, 86”
From Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala (2015) · cites this paper as [85]
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“Different technical reasons have prevented the unanimous, precise localization of the borders and subdivisions of the primate Me (see, e.g., Sims and Williams, 1990; Martin et al., 1991; Sorvari et al., 1995; Gloor, 1997; Carlo et al., 2010; Yilmazer-Hanke, 2012).”
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“Our descriptions of these neurons will have to be compared with those reported by other authors (Sims and Williams, 1990; Gloor, 1997; de Olmos, 2004).”
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“It is worth mentioning that the estimated mean neuronal density found in the Me is compatible with the corresponding values in the human central amygdaloid nucleus (1.04 105 neurons/mm3; Schumann and Amaral, 2005; Chareyron et al., 2011).”
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“Different technical reasons have prevented the unanimous, precise localization of the borders and subdivisions of the primate Me (see, e.g., Sims and Williams, 1990; Martin et al., 1991; Sorvari et al., 1995; Gloor, 1997; Carlo et al., 2010; Yilmazer-Hanke, 2012).”
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“The former was identified by the presence of vesicle accumulation in close proximity to the presynaptic density (S€atzler et al., 2002; Ribeiro et al., 2005) in both asymmetrical and symmetrical contacts.”
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BackgroundCalbindin-D28k-immunoreactive cells and fibres in the human amygdaloid complex
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“These neurons resemble the aforementioned calretinin-immunoreactive cells (Sorvari et al., 1996b) and might represent different populations of inhibitory neurons (Sorvari et al., 1995, 1996a; Carney et al., 2010).”
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“Samples from four cases were used for GFAP immunohistochemistry (cases 1–4; Table 1), adapting the methods described in previous reports (Xavier et al., 2005; Martinez et al., 2006; de Castilhos et al., 2009).”
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Self-citationPrimate evolution and the amygdala
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“In rats, the Me multipolar neurons have been classified as bitufted (with an ovoid or fusiform soma) or stellate cells (see, e.g., Rasia-Filho et al., 1999, 2012b; Cooke et al., 2007; Marcuzzo et al., 2007; Dall’Oglio et al., 2008a,b; Arpini et al., 2010) after previous descriptions (Valverde,…”
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“Unfortunately, when studying some neuroanatomical aspects of large structures in human brains, it is not feasible to use approaches that produce little shrinkage such as the inclusion of tissue in durcupan or epoxy resins (Tang and Nyengaard, 1997; Lopez et al, 2005; Hermel et al., 2006a,b).”
Methodde Olmos, J. S. (2004) · Elsevier eBooks · doi:10.1016/b978-012547626-3/50023-5 · Cited by 39 · cited 13× · see citing works
“The locations of the Me in both left and right brain hemispheres were identified according to the descriptions and recommendations in the literature (Gloor, 1997; Sorvari, 1997; de Olmos, 2004).”
BackgroundMethodResultInfluentialEffects of gonadal hormones on the morphology of neurons from the medial amygdaloid nucleus of rats.
Rasia-Filho, A., Londero, R., & Achaval, M. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00160-9 · Cited by 39 · cited 3× · see citing works
“In rats, the Me multipolar neurons have been classified as bitufted (with an ovoid or fusiform soma) or stellate cells (see, e.g., Rasia-Filho et al., 1999, 2012b; Cooke et al., 2007; Marcuzzo et al., 2007; Dall’Oglio et al., 2008a,b; Arpini et al., 2010) after previous descriptions (Valverde,…”
BackgroundSelf-citationDendritic spines in the posterodorsal medial amygdala after restraint stress and ageing in rats
Marcuzzo, S., Dall’Oglio, A., Ribeiro, M. F. M., Achaval, M., & Rasia‐Filho, A. A. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.07.019 · Cited by 39 · cited 2× · see citing works
“…have been classified as bitufted (with an ovoid or fusiform soma) or stellate cells (see, e.g., Rasia-Filho et al., 1999, 2012b; Cooke et al., 2007; Marcuzzo et al., 2007; Dall’Oglio et al., 2008a,b; Arpini et al., 2010) after previous descriptions (Valverde, 1962; de Olmos et al., Human medial…”
BackgroundSelf-citationCarlo, C. N., Stefanacci, L., Semendeferi, K., & Stevens, C. F. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22264 · Cited by 38 · see citing works
Rodrigues, G. J., Restini, C. B. A., Lunardi, C. N., Moreira, J. E., de Lima, R. G., da Silva, R. S., & Bendhack, L. M. (2007) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.107.127241 · Cited by 36 · cited 1× · see citing works
“Ultrastructural observations were carried out in two subjects (cases 7 and 8; Table 1), following the procedures detailed by Moreira et al. (1996), Hermel et al. (2006a), and Rodrigues et al. (2007).”
MethodSelf-citationDall’Oglio, A., Gehlen, G., Achaval, M., & Rasia‐Filho, A. A. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2007.10.051 · Cited by 32 · see citing works
Self-citationBenzing, W. C., Mufson, E. J., Jennes, L., Stopa, E. G., & Armstrong, D. M. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903170306 · Cited by 31 · cited 1× · see citing works
“…technique (Gabbott and Somogyi, 1984; Rasia-Filho et al., 2004; de Castilhos et al., 2008; Arpini et al., 2010), according to the modifications proposed by Izzo et al. (1987) and Bolam (1992), and used the methodology specific for human nervous tissue recently described by Dall’Oglio et al. (2010).”
MethodMiddeldorp, J., van den Berge, S. A., Aronica, E., Speijer, D., & Hol, E. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007663 · Cited by 31 · cited 2× · see citing works
“It stained a pattern of cellular morphology and distribution in the human Me that is identical to that described in previous reports (Middeldorp et al., 2009).”
BackgroundResultPopov, V. I., & Stewart, M. G. (2009) · Synapse · doi:10.1002/syn.20613 · Cited by 30 · cited 1× · see citing works
“Although they were not commonly observed in local synapses, both specializations offer insight into the strength and complexity of the synaptic transmission and processing in the Me (see parallel comments in Peters el al., 1991; Popov and Stewart, 2009).”
BackgroundDescriptive findings on the morphology of dendritic spines in the rat medial amygdala
Brusco, J., Dall’Oglio, A., Rocha, L. B., Rossi, M. A., Moreira, J. E., & Rasia‐Filho, A. A. (2010) · Neuroscience Letters · doi:10.1016/j.neulet.2010.07.083 · Cited by 28 · cited 2× · see citing works
“Spinules emerged from the larger mushroom-like spines (Brusco et al., 2010; data not shown).”
BackgroundSelf-citationDall’Oglio, A., Gehlen, G., Achaval, M., & Rasia‐Filho, A. A. (2008) · Neuroscience Letters · doi:10.1016/j.neulet.2008.05.025 · Cited by 27 · see citing works
Self-citationThe “single-section” Golgi method adapted for formalin-fixed human brain and light microscopy
Dall’Oglio, A., Ferme, D., Brusco, J., Moreira, J. E., & Rasia‐Filho, A. A. (2010) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2010.03.018 · Cited by 20 · cited 2× · see citing works
“This method allows us to study neurons and glial cells in brains that have been kept in simple and routine fixative solutions (Dall’Oglio et al., 2010).”
MethodSelf-citationMatsuda, S., Kobayashi, Y., & Ishizuka, N. (2004) · Neuroscience Research · doi:10.1016/j.neures.2004.03.002 · Cited by 19 · cited 1× · see citing works
“The synapse was classified as being inhibitory, when more than 20% of the electron-lucid vesicles on a synaptic terminal were flattened, and the pre- and postsynaptic membranes of the terminal were symmetrical (Matsuda et al., 2004; Hermel et al., 2006a).”
BackgroundMoreira, J. E., Reese, T. S., & Kachar, B. (1996) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(19960215)33:3 · Cited by 17 · see citing works
Self-citationArpini, M., Menezes, I. C., Dall’Oglio, A., & Rasia‐Filho, A. A. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.11.076 · Cited by 17 · see citing works
Self-citationHermel, É. D. E. S., Faccioni-Heuser, M. C., Marcuzzo, S., Rasia‐Filho, A. A., & Achaval, M. (2006) · Journal of Anatomy · doi:10.1111/j.1469-7580.2006.00559.x · Cited by 16 · see citing works
Self-citationDendritic spines observed by extracellular DiI dye and immunolabeling under confocal microscopy
Rasia‐Filho, A. A. (2010) · Protocol Exchange · doi:10.1038/nprot.2010.153 · Cited by 16 · cited 1× · see citing works
“Experiments may also require the carbocyanine fluorescent dye DiI in lightly fixed tissue and confocal microscopy (Rasia-Filho et al., 2010; Brusco et al., 2010).”
BackgroundSelf-citationMolecular and functional properties of neurons in the human lateral amygdala
Hüttmann, K., Yilmazer‐Hanke, D., Seifert, G., Schramm, J., Pape, H., & Steinhäuser, C. (2005) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.09.011 · Cited by 13 · cited 1× · see citing works
“Electrophysiological recordings and other neuroanatomical techniques will be needed to characterize the interneurons and projecting neurons (see Huttmann et al., 2006; Lanciego and Wounterlood, 2011).”
BackgroundUrban, S., & Yilmazer‐Hanke, D. (1999) · PubMed · Cited by 7 · see citing works
Sex differences in NADPH-diaphorase activity in the rat posterodorsal medial amygdala
de Castilhos, J., Rigon, P., Xavier, L. L., Rasia‐Filho, A. A., & Achaval, M. (2009) · Brain Research · doi:10.1016/j.brainres.2009.09.110 · Cited by 5 · cited 1× · see citing works
“Samples from four cases were used for GFAP immunohistochemistry (cases 1–4; Table 1), adapting the methods described in previous reports (Xavier et al., 2005; Martinez et al., 2006; de Castilhos et al., 2009).”
MethodSelf-citation
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1 of the 91 references couldn’t be matched to a known paper.
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Pantazopoulos, H., Markota, M., Jaquet, F., Ghosh, D., Wallin, A., Santos, A., Caterson, B., & Berretta, S. (2015) · Translational Psychiatry · doi:10.1038/tp.2014.128 · Cited by 153 · see citing works
“85,86 PNNs control the lateral mobility of cell surface molecules including glutamatergic receptors, thus regulating their availability on the postsynaptic membrane specialization, modulate L-type voltage-dependent calcium channels and voltage-gated potassium channels and affect the local…”
Brusco, J., Merlo, S., Ikeda, E. T., Petralia, R. S., Kachar, B., Rasia‐Filho, A. A., & Moreira, J. E. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23518 · Cited by 36 · see citing works
“Synaptic vesicles with lengths twice as much as their widths were considered flattened (Uchizono, 1965; Matsuda et al., 2004; Dall’Oglio et al., 2013).”
BackgroundSelf-citationThe human medial amygdala: structure, diversity, and complexity of dendritic spines
Dall’Oglio, A., Dutra, A. C. L., Moreira, J. E., & Rasia‐Filho, A. A. (2015) · Journal of Anatomy · doi:10.1111/joa.12358 · Cited by 36 · see citing works
“The definitive subdivision of the human Me has not as yet been established (Dall’Oglio et al. 2013 and references therein).”
BackgroundMethodInfluentialSelf-citationStructure and function of the medial amygdala
(2020) · Handbook of Behavioral Neuroscience · doi:10.1016/b978-0-12-815134-1.00002-7 · Cited by 29 · see citing works
Reberger, R., Dall’Oglio, A., Jung, C. R., & Rasia‐Filho, A. A. (2017) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2017.09.001 · Cited by 21 · see citing works
Self-citationNeuronal types of the human cortical amygdaloid nucleus
Vásquez, C. E., Reberger, R., Dall’Oglio, A., Calcagnotto, M. E., & Rasia‐Filho, A. A. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24527 · Cited by 21 · see citing works
“One or multiple axon terminals usually form asymmetric contacts with a dendritic spine (Arellano et al., 2007b; Brusco et al., 2014; Dall'Oglio et al., 2013; Dall'Oglio et al., 2015; Peters, Palay, & Webster, 1991).”
BackgroundMethodInfluentialSelf-citationRasia‐Filho, A. A., Guerra, K. T. K., Vásquez, C. E., Dall’Oglio, A., Reberger, R., Jung, C. R., & Calcagnotto, M. E. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.616607 · Cited by 24 · see citing works
Self-citationGlial Cell Modulation of Dendritic Spine Structure and Synaptic Function
Rasia‐Filho, A. A., Calcagnotto, M. E., & Halbach, O. V. B. U. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-36159-3_6 · Cited by 21 · see citing works
Self-citationDendritic and Spine Heterogeneity of von Economo Neurons in the Human Cingulate Cortex
Correa-Júnior, N. D., Renner, J., Fuentealba-Villarroel, F., Hilbig, A., & Rasia‐Filho, A. A. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.00025 · Cited by 18 · see citing works
Self-citationLoss, C. M., Rosa, N. S., Mestriner, R. G., Xavier, L. L., & de Oliveira, D. L. (2019) · NeuroToxicology · doi:10.1016/j.neuro.2019.01.002 · Cited by 15 · see citing works
“The evidence points to absence of sexual dimorphism in NMDAR expression and composition in PND16 (the period we subject the animals to SE) or even around this stage of brain development (second and third postnatal weeks) (Damborsky and Winzer-Serhan, 2012; Tavassoli et al., 2013).”
BackgroundSelf-citationMorphological Features of Human Dendritic Spines
Renner, J., & Rasia‐Filho, A. A. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-36159-3_9 · Cited by 16 · see citing works
Self-citationSpindle-Shaped Neurons in the Human Posteromedial (Precuneus) Cortex
Fuentealba-Villarroel, F., Renner, J., Hilbig, A., Bruton, O. J., & Rasia‐Filho, A. A. (2022) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.769228 · Cited by 13 · see citing works
“0 software (Media Cybernetics, United States) during the acquisition process (Dall’Oglio et al., 2013; Reberger et al., 2018).”
MethodSelf-citationGuerra, K. T. K., Renner, J., Vásquez, C. E., & Rasia‐Filho, A. A. (2022) · The Journal of Comparative Neurology · doi:10.1002/cne.25430 · Cited by 11 · see citing works
Self-citationThe medial amygdala’s neural circuitry: Insights into social processing and sex differences
Ignacio, B., Baeza, J., Ruiz, B., Romero, J. P., Yáñez, P., Ramírez, C., Caprile, T., Farkas, C., & Recabal, A. (2025) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2025.101190 · Cited by 9 · see citing works
“Still, the left amygdala contains 18 % more neurons than the right (Dall ’ Oglio, 2013), whose morphology is mainly multipolar, similar to the MeA in rats.”
Horn, Â. C. M., & Rasia‐Filho, A. A. (2017) · The Anatomical Record · doi:10.1002/ar.23699 · Cited by 10 · see citing works
“The same precautionary procedure was done previously for the delineation of the subnuclei of the MeA in rats and humans (Dall’Oglio et al., 2013; Salazar et al., 2014).”
MethodSelf-citationIntroduction: What Are Dendritic Spines?
Rasia‐Filho, A. A., Calcagnotto, M. E., & Halbach, O. V. B. U. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-36159-3_1 · Cited by 9 · see citing works
Self-citationRasia‐Filho, A. A. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2022.831568 · Cited by 5 · see citing works
Self-citationVargas‐Barroso, V., & Larriva-Sahd, J. A. (2013) · The Anatomical Record · doi:10.1002/ar.22753 · Cited by 5 · see citing works
Renner, J., Rasia‐Filho, A. A., González-Tapia, D., & González‐Burgos, I. (2026) · Journal of Anatomy · doi:10.1111/joa.70124 · Cited by 4 · see citing works
Self-citationMorphological heterogeneity of neurons in the human central amygdaloid nucleus
Vásquez, C. E., Guerra, K. T. K., Renner, J., & Rasia‐Filho, A. A. (2024) · Journal of Neuroscience Research · doi:10.1002/jnr.25319 · Cited by 4 · see citing works
Self-citationHuman Neocortex Layer Features Evaluated by PIXE, STIM, and STXM Techniques
Jobim, P. F. C., dos Santos, C. E. I., Dias, J. F., Kelemen, M., Pelicon, P., Vogel‐Mikuš, K., Pascolo, L., Gianoncelli, A., Bedolla, D. E., & Rasia‐Filho, A. A. (2022) · Biological Trace Element Research · doi:10.1007/s12011-022-03182-x · Cited by 3 · see citing works
Self-citationThe Human Amygdaloid Complex: Cellular Architecture and Dopaminergic Innervation
García-Amado, M., & Prensa, L. (2017) · InTech eBooks · doi:10.5772/intechopen.68391 · Cited by 3 · see citing works
Renner, J., da Silva, B. L. R., & Rasia-Filho, A. (2026) · Neuroscience · doi:10.1016/j.neuroscience.2026.04.022 · Cited by 2 · see citing works
Self-citationRasia‐Filho, A. A., Renner, J., & da Silva, B. R. (2026) · SSRN Electronic Journal · doi:10.2139/ssrn.6019303
Self-citation
- Authors
- Dall'Oglio, A., Xavier, L. L., Hilbig, A., Ferme, D., Moreira, J. E., Achaval, M., & Rasia‐Filho, A. A.
- Affiliations
- Pontifícia Universidade Católica do Rio Grande do Sul (BR)
- Universidade Federal de Ciências da Saúde de Porto Alegre (BR)
- Universidade de São Paulo (BR)
- Universidade Federal do Rio Grande do Sul (BR)
- Corresponding author
- Rasia‐Filho, Alberto A.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2012-12-17
- Volume
- 521
- Issue
- 3
- Pages
- 589-611
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W2035509750
- Cited by
- 24
- References
- 91
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 1 · 2020: 2 · 2019: 1 · 2018: 1 · 2017: 3 · 2015: 2 · 2013: 2
- FWCI
- 0.53
- Type
- journal article
- Language
- en
- Open access
- green
- hdl.handle.net
- Licence
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Lume (Universidade Federal do Rio Grande do Sul) (submittedVersion, cc-by-nc-sa)
- Funders
- Universidade de São Paulo
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Anatomy › Medical and Biological Sciences
- Keywords
- medial amygdala, human amygdala, neuronal density, glial cells, astrocytes, GFAP immunoreactivity, synaptic ultrastructure, dendritic spines, axodendritic synapses, tripartite synapse, hemispheric lateralization
- MeSH terms
- Aged, Aged, 80 and over, Amygdala, Astrocytes, Axons, Cell Count, Dendrites, Coloring Agents, Glial Fibrillary Acidic Protein, Humans, Male, Middle Aged, Neurons, Phenothiazines, Synapses, Synaptic Vesicles, Silver Staining, Cell Shape, Dendritic Spines
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