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Stereological Analysis of Amygdala Neuron Number in Autism
Open accessAbstract
The amygdala is one of several brain regions suspected to be pathological in autism. Previously, we found that young children with autism have a larger amygdala than typically developing children. Past qualitative observations of the autistic brain suggest increased cell density in some nuclei of the postmortem autistic amygdala. In this first, quantitative stereological study of the autistic brain, we counted and measured neurons in several amygdala subdivisions of 9 autism male brains and 10 age-matched male control brains. Cases with comorbid seizure disorder were excluded from the study. The amygdaloid complex was outlined on coronal sections then partitioned into five reliably defined subdivisions: (1) lateral nucleus, (2) basal nucleus, (3) accessory basal nucleus, (4) central nucleus, and (5) remaining nuclei. There is no difference in overall volume of the amygdala or in individual subdivisions. There are also no changes in cell size. However, there are significantly fewer neurons in the autistic amygdala overall and in its lateral nucleus. In conjunction with the findings from previous magnetic resonance imaging studies, the autistic amygdala appears to undergo an abnormal pattern of postnatal development that includes early enlargement and ultimately a reduced number of neurons. It will be important to determine in future studies whether neuron loss in the amygdala is a consistent characteristic of autism and whether cell loss occurs in other brain regions as well.
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“Neuronal densities are higher in layers I-III of area 24a in the left hemisphere, neuronal size is reduced in all layers of area 24b, and neuronal packing density is reduced in layers V-VI in area 24c, consistent with previously reported reductions in neuronal density in the FG and amygdala [318, 362].”
From Autism spectrum disorder: neuropathology and animal models (2017) · cites this paper as [318]
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Advances in nonhuman primate models of autism: Integrating neuroscience and behavior
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“abnormalities in individuals with ASD [117-121], complete amygdala lesions in an animal model clearly do not represent findings in the clinical population.”
Self-citationRubinow, M. J., Mahajan, G., May, W., Overholser, J. C., Jurjus, G., Dieter, L., Herbst, N. P., Steffens, D. C., Miguel-Hidalgo, J. J., Rajkowska, G., et al. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0900-z · Cited by 76
“Unlike disorders including autism (Schumann and Amaral 2006), schizophrenia (Kreczmanski et al.”
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“Moreover, age-related variation in the amygdala (54) and the dorsal prefrontal cortex (2) has been noted in autism.”
BackgroundStructural connectivity of the amygdala in young adults with autism spectrum disorder
Gibbard, C. R., Ren, J., Skuse, D., Clayden, J. D., & Clark, C. A. (2017) · Human Brain Mapping · doi:10.1002/hbm.23915 · Cited by 76
“Contrary to this, reduced neuronal density has been reported in the lateral nucleus of the amygdala in ASD (Schumann & Amaral, 2006; Wegiel et al., 2014).”
BackgroundAnder, B. P., Barger, N., Stamova, B. S., Sharp, F. R., & Schumann, C. M. (2015) · Molecular Autism · doi:10.1186/s13229-015-0029-9 · Cited by 72
“abnormalities in ASD brain [33, 51, 61–67].”
Self-citationNeuropathology and Animal Models of Autism: Genetic and Environmental Factors
Gadad, B. S., Hewitson, L. C., Young, K. A., & German, D. C. (2013) · Autism Research and Treatment · doi:10.1155/2013/731935 · Cited by 72
“Several studies have shown a 13–16% enlargement of the amygdala in young autistic cases (3–5 years of age) [37, 46].”
BackgroundInfluentialAltered Amygdala Development and Fear Processing in Prematurely Born Infants
Cismaru, A. L., Gui, L., Vasung, L., Lejeune, F., Barisnikov, K., Truttmann, A. C., Tolsa, C. B., & Hüppi, P. S. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00055 · Cited by 68
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“en in the �rst quantitative stereological study of the autistic brain, neurons in several amygdala subdivisions of nine autism male brains were counted and measured and compared to the counts from ten age-matched male control brains [62].”
MethodEvans, T. A., Siedlak, S. L., Lu, L., Fu, X., Wang, Z., McGinnis, W. R., Fakhoury, E., Castellani, R. J., Hazen, S. L., Walsh, W. J., et al. (2008) · American journal of biochemistry & biotechnology/American journal of biochemistry and biotechnology · doi:10.3844/ajbbsp.2008.61.72 · Cited by 68
“Significantly fewer neurons in the autistic amygdala overall and in its lateral nucleus are noted([18]), suggesting neuronal loss occurs in more than one brain area.”
BackgroundKleinhans, N. M., Reiter, M. A., Neuhaus, E., Pauley, G., Martin, N., Dager, S. R., & Estes, A. M. (2015) · Autism Research · doi:10.1002/aur.1589 · Cited by 71
“A postmortem study reported evidence that the lateral nucleus of the amygdala, which is crucial for socioemotional processing, is the most consistently impacted in ASD [Schumann & Amaral, 2006].”
BackgroundResultMoseley, R. L., Юрьевич, Ш. Ю., Mohr, B., Lombardo, M. V., Baron‐Cohen, S., & Friedemann Pulvermüller, A. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.09.046 · Cited by 72
“In addition to the aforementioned abnormalities of corticalmotor systems, peoplewith ASC also show atypical activity and structure in many of these limbic regions (Bauman and Kemper, 1994; Raymond et al., 1995; Haznedar et al., 1997, 2000; Aylward et al., 1999; Howard et al., 2000; Ohnishi et al., 2000; Salmond et al.…”
BackgroundThe Limbic and Sensorimotor Pathways of the Human Amygdala: A Structural Connectivity Study
Rizzo, G., Milardi, D., Bertino, S., Basile, G. A., Mauro, D. D., Calamuneri, A., Chillemi, G., Silvestri, G., Anastasi, G., Bramanti, A., et al. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.05.051 · Cited by 69
Barger, N., Stefanacci, L., Schumann, C. M., Sherwood, C. C., Annese, J., Allman, J. M., Buckwalter, J. A., V, Hof, P. R., & Semendeferi, K. (2012) · The Journal of Comparative Neurology · doi:10.1002/cne.23118 · Cited by 65
“Autistic adults exhibit considerable reductions in the number of neurons only in the lateral nucleus (Schumann and Amaral, 2006), and volumetric reduction of the lateral nucleus has been suggested to be a feature of Williams syndrome (Galaburda and Bellugi, 2000).”
BackgroundSelf-citationTager-Flusberg, H. B., Skwerer, D. P., & Joseph, R. M. (2006) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsl035 · Cited by 65
“…this proposal, especially as it is consistent with evidence of structural abnormalities of the amygdala in both postmortem (Bauman and Kemper, 1985; Schumann and Amaral, 2006) and in vivo MRI studies (Schumann et al., 2004; Nacewicz et al., in press), there is little consensus on the scope of the…”
Stereological Analysis of Neuron, Glial and Endothelial Cell Numbers in the Human Amygdaloid Complex
García‐Amado, M., & Prensa, L. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038692 · Cited by 65
“However, neuron densities estimated by Schuman and Amaral [7] or Berreta et al.”
MethodInfluentialPersistence of megalencephaly in a subgroup of young boys with autism spectrum disorder
Libero, L. E., Nordahl, C. W., Li, D. D., Ferrer, E. E., Rogers, S. J., & Amaral, D. G. (2016) · Autism Research · doi:10.1002/aur.1643 · Cited by 70
“Both increased [Bailey et al., 1998; Courchesne et al., 2011b] and decreased [Bailey et al., 1998; Bauman, 1991; Schumann & Amaral, 2006] neuron counts have been reported in studies using postmortem tissue of individuals with ASD.”
ResultSelf-citationThe mouse Engrailed genes: A window into autism
KUEMERLE, B., GULDEN, F., CHEROSKY, N., WILLIAMS, E., & HERRUP, K. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2006.09.009 · Cited by 60
Malformation of the superior olivary complex in an animal model of autism
Lukose, R., Schmidt, E., Wolski, T. P., Murawski, N. J., & Kulesza, R. J. (2011) · Brain Research · doi:10.1016/j.brainres.2011.05.013 · Cited by 59
The Current View on the Paradox of Pain in Autism Spectrum Disorders
Bogdanova, O. V., Bogdanov, V. B., Pizano, A., Bouvard, M. P., Cazalets, J., Mellen, N. M., & Amestoy, A. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.910824 · Cited by 70
“For example, the amygdala in individuals with ASD show both microscopic (112) and macroscopic structural regional abnormalities.”
BackgroundDifferential serotonergic innervation of the amygdala in bonobos and chimpanzees
Stimpson, C. D., Barger, N., Taglialatela, J. P., Gendron‐Fitzpatrick, A., Hof, P. R., Hopkins, W. D., & Sherwood, C. C. (2015) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsv128 · Cited by 60
“…a number of cognitive disorders that affect social behavior, such as autism, schizophrenia and extreme chronic aggression (Reynolds, 1992; Adolphs, 1999; Davidson, 2000; Dalton et al., 2005; Meyer-Lindenberg et al., 2006; Schumann and Amaral, 2006; Kennedy and Adolphs, 2012; Markota et al., 2014).”
BackgroundAutism as early neurodevelopmental disorder: evidence for an sAPPα-mediated anabolic pathway
Lahiri, D. K., Sokol, D. K., Erickson, C. A., Ray, B., Ho, C. Y., & Maloney, B. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00094 · Cited by 63
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 67
Fereshetyan, K., Chavushyan, V. A., Danielyan, M., & Yenkoyan, K. B. (2021) · Scientific Reports · doi:10.1038/s41598-021-02994-6 · Cited by 58
Barrett, C., Hennessey, T., Gordon, K. M., Ryan, S. J., McNair, M. L., Ressler, K. J., & Rainnie, D. G. (2017) · Molecular Autism · doi:10.1186/s13229-017-0160-x · Cited by 60
“Amygdala abnormalities in structure [11–13], neuronal density [14, 15], and functional MRI activity during social tasks [16–22] have been reported in patients with ASD.”
BackgroundWang, C.-C., Lin, H., Chan, Y., Gean, P., Yang, Y. K., & Chen, P. S. (2013) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145713000473 · Cited by 59
“In addition, post-mortem studies of individuals with ASD have shown cyto-architectural and neuronal organization changes within the amygdala (Bailey et al., 1998; Schumann and Amaral, 2006).”
BackgroundOlde Loohuis, N. F. M., Kole, K., Glennon, J. C., Karel, P., Van der Borg, G., Van Gemert, Y., Van den Bosch, D., Meinhardt, J., Kos, A., Shahabipour, F., et al. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.05.006 · Cited by 54
“Previously, it has been suggested that gene defects inherent to ASD result in the development of a larger and more active amygdala (Schumann and Amaral, 2006).”
BackgroundNo reduction of spindle neuron number in frontoinsular cortex in autism
Kennedy, D. P., Semendeferi, K., & Courchesne, E. (2007) · Brain and Cognition · doi:10.1016/j.bandc.2007.01.007 · Cited by 55
“These Nissl-stained coronal sections were 100 microns thick (for complete tissue processing details, see Schumann & Amaral, 2005, 2006).”
BackgroundCope, E. C., Briones, B. A., Brockett, A. T., Martinez, S., Vigneron, P.-A., Opendak, M. M., Wang, S. S. ‐., & Gould, E. (2016) · eNeuro · doi:10.1523/eneuro.0196-16.2016 · Cited by 57
“Our findings leave open the possibility that more subtle changes in morphology may occur in ASD as well as in other brain regions that are not explored here but are implicated in ASD (Schumann and Amaral, 2006; Dichter et al., 2012; Wang et al., 2014).”
BackgroundAutism and the amygdala: An endocrine hypothesis
Schulkin, J. A. (2007) · Brain and Cognition · doi:10.1016/j.bandc.2006.02.009 · Cited by 57
Wills, S., Rossi, C. C., Bennett, J., Martínez‐Cerdeño, V., Ashwood, P., Amaral, D. G., & de Water, J. V. (2011) · Molecular Autism · doi:10.1186/2040-2392-2-5 · Cited by 53
“While a decreased number of neurons has been reported in the amygdala [77] and in the fusiform gyrus [78] of postmortem cases of autism, it is not yet clear whether there is a preferential loss of any particular category of neurons, such as GABAergic interneurons.”
BackgroundSelf-citationNeuropathology of the Anterior Midcingulate Cortex in Young Children With Autism
Uppal, N., Wicinski, B., Buxbaum, J. D., Heinsen, H., Schmitz, C., & Hof, P. R. (2014) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/nen.0000000000000108 · Cited by 52
“The amygdala and fusiform gyrus also have reduced neuron density in autism, as reported by Simms et al (19), van Kooten et al (70), and Schumann and Amaral (71).”
MethodSynaptic reorganization in scaled networks of controlled size.
Wilson, N. R., Ty, M. T., Ingber, D. E., Sur, M., & Liu, G. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.3863-07.2007 · Cited by 52
“…synaptic scaling and reconfiguration as a result of neuron loss could contribute to known age-related deficits in synaptic plasticity (Rosenzweig and Barnes, 2003) or impact specific regions during diseases where neuron number is suspected to change, such as in autism (Schumann and Amaral, 2006).”
BackgroundDendritic Integration Dysfunction in Neurodevelopmental Disorders
Nelson, A. D., & Bender, K. J. (2021) · Developmental Neuroscience · doi:10.1159/000516657 · Cited by 54
Serotonin, pregnancy and increased autism prevalence: Is there a link?
Hadjikhani, N. K. (2009) · Medical Hypotheses · doi:10.1016/j.mehy.2009.11.015 · Cited by 51
“Several anatomical studies have found abnormalities in the amygdala of autistic subjects, although their results do not allow any conclusion regarding an increase or a decrease of amygdala volume in autism [55–61].”
BackgroundAutism: A review of biological bases, assessment, and intervention.
Volker, M. A., & Lopata, C. J. (2008) · School Psychology Quarterly · doi:10.1037/1045-3830.23.2.258 · Cited by 56
“…this, recent research has indicated that in male subjects with autism and no history of seizures, the amygdala demonstrated an abnormal pattern of development characterized by enlargement in childhood (Schumann et al., 2004) and a decreased number of neurons in adulthood (Schumann & Amaral, 2006).”
BackgroundSex Differences in the Amygdala Resting-State Connectome of Children With Autism Spectrum Disorder
Lee, J. K., Amaral, D. G., Solomon, M., Rogers, S. J., Ozonoff, S. J., & Nordahl, C. W. (2019) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.08.004 · Cited by 49
“Postmortem research has reported differences in the number of amygdala neurons in ASD (2, 4), volumetric MRI research has reported amygdala enlargement in ASD (2, 8–11), and functional neuroimaging research has reported altered amygdala response and habituation to socio-emotional stimuli in ASD (12, 13).”
BackgroundSelf-citationAutism spectrum disorder, but not amygdala lesions, impairs social attention in visual search
Wang, S., Xu, J., Jiang, M. X., Zhao, Q., Hurlemann, R., & Adolphs, R. (2014) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2014.09.002 · Cited by 53
Comparing social attention in autism and amygdala lesions: Effects of stimulus and task condition
Birmingham, E., Cerf, M., & Adolphs, R. (2011) · Social Neuroscience · doi:10.1080/17470919.2011.561547 · Cited by 56
“For instance, morphometric studies of postmortem brains have shown that the amygdala is structurally abnormal in ASD (Kemper & Bauman, 1993 ; Schumann & Amaral, 2006 ).”
Micheau, J., Vimeney, A., Normand, E., Mulle, C., & Riedel, G. (2014) · Hippocampus · doi:10.1002/hipo.22290 · Cited by 43
Wegiel, J., Flory, M., Kuchna, I., Nowicki, K., Ma, S. Y., Imaki, H., Wegiel, J., Frackowiak, J., Kolecka, B. M., Wierzba-Bobrowicz, T., et al. (2015) · Acta Neuropathologica Communications · doi:10.1186/s40478-015-0183-5 · Cited by 47
“This result is similar to the result of averaging of the neuronal size in the amygdala of 10- to 44-year-old autistic subjects [56], when the difference is masked by an increase in the neuronal volume in autistic subjects and a decrease in the neuronal volume in control subjects.”
ResultActivation of basolateral amygdala in juvenile C57BL/6J mice during social approach behavior
Ferri, S. L., Kreibich, A. S., Torre, M., Piccoli, C. T., Dow, H. C., Pallathra, A. A., Li, H., Bilker, W. B., Gur, R. C., Abel, T. G., et al. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.08.006 · Cited by 48
“Researchers have demonstrated changes in cell number and size (Kemper and Bauman, 1993; Schumann and Amaral, 2006), volume (Abell et al., 1999; Howard et al., 2000; Sparks et al., 2002; Munson et al., 2006), gray matter volume (Abell et al., 1999; Waiter et al., 2004), and activity during social…”
Chmielewski, W. X., & Beste, C. (2014) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2014.11.002 · Cited by 51
Boll, S., Gamer, M., Kalisch, R., & Büchel, C. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2011.02.021 · Cited by 51
“Based on a stereological analysis its size in the human brain is approximately 430 mm3 (SD=± 50 mm3) (Schumann and Amaral, 2006).”
BackgroundInfluentialAbnormal Neural Activation to Faces in the Parents of Children with Autism
Yucel, G., Belger, A., Bizzell, J., Parlier, M., Adolphs, R., & Piven, J. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu147 · Cited by 50
Maternal Obesity and Gut Microbiota Are Associated with Fetal Brain Development
Basak, S., Das, R. K., Banerjee, A., Paul, S., Pathak, S., & Duttaroy, A. K. (2022) · Nutrients · doi:10.3390/nu14214515 · Cited by 55
“The structural and functional alterations of the amygdala are associated with neuropsychiatric and developmental disorders ranging from anxiety [139] to autism spectrum disorder [140].”
BackgroundRecent developments in neuropathology of autism spectrum disorders
Polšek, D., Jagatic, T., Cepanec, M., Hof, P. R., & Šimić, G. (2011) · Translational Neuroscience · doi:10.2478/s13380-011-0024-3 · Cited by 49
Dystrophic Serotonin Axons in Postmortem Brains from Young Autism Patients
Azmitia, E. C., Singh, J. S., Hou, X. P., & Węgiel, J. (2011) · The Anatomical Record · doi:10.1002/ar.21243 · Cited by 46
“…increase of white matter volume in the cerebellum (Courchesne et al., 2001), whereas another study found a larger amygdala volume in autistic children than in controls, though this changed with time and no difference was observed after adolescence (Schumann et al., 2004; Schumann and Amaral, 2006).”
BackgroundMurphy, C. M., Deeley, Q., Daly, E. M., Ecker, C., O'Brien, F. M., Hallahan, B., Loth, E., Toal, F., Reed, S., Hales, S., et al. (2012) · Autism Research · doi:10.1002/aur.227 · Cited by 63
“In the only postmortem stereological investigation of amygdala in autism, no differences were detected in amygdala volume or cell size, but a significant reduction in number of neurons was noted [Schumann & Amaral, 2006].”
BackgroundHanson, J. L., & Nacewicz, B. M. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.624705 · Cited by 50
Primary olfactory cortex in autism and epilepsy: increased glial cells in autism
Menassa, D. A., Sloan, C., & Chance, S. A. (2016) · Brain Pathology · doi:10.1111/bpa.12415 · Cited by 45
“Neighbouring regions of the PiC are affected in autism: the amygdala has 12% fewer neurons (12), the hippocampus has increased cell-packing density and decreased neuronal size in the cornu ammonis (CA1) region (13) and the fusiform gyrus has layer-specific decreases in neuronal numbers and densities (14).”
BackgroundIdentification of amygdala-expressed genes associated with autism spectrum disorder
Herrero, M. J., Velmeshev, D., Hernandez‐Pineda, D., Sethi, S., Sorrells, S. F., Banerjee, P., Sullivan, C. A. W., Gupta, A. R., Kriegstein, A. R., & Corbin, J. G. (2020) · Molecular Autism · doi:10.1186/s13229-020-00346-1 · Cited by 45
Lukose, R., Beebe, K., & Kulesza, R. J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.11.033 · Cited by 42
Lossi, L., Castagna, C., Granato, A., & Merighi, A. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8122088 · Cited by 43
Altered Dynamics of the fMRI Response to Faces in Individuals with Autism
Kleinhans, N. M., Richards, T. L., Greenson, J., Dawson, G., & Aylward, E. (2015) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-015-2565-8 · Cited by 48
“Abnormal habituation might be related to amygdalar abnormalities such as reduced numbers of neurons (Schumann and Amaral 2006), volumetric deviations from agematched controls (Schumann et al.”
BackgroundGadad, B. S., Li, W., Yazdani, U., Grady, S., Johnson, T., Hammond, J., Gunn, H. C., Curtis, B., English, C. N., Yutuc, V., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500968112 · Cited by 41
“For instance, Schumann and Amaral (20) reported a 14% decrease in amygdala lateral 4 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1500968112 Gadad et al. D ow nl oa de d by g ue st o n Ju ly 1 0, 2 02 0 nucleus cell number in postmortem ASD brains.”
BackgroundInfluentialHall, G. B., Doyle, K. A. R., Goldberg, J., West, D., & Szatmári, P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010804 · Cited by 39
“However, a recent study failed to replicate differences in cell packing, but instead identified fewer neurons in the amygdalae of individuals with autism [23].”
ResultHajisoltani, R., Karimi, S. A., Rahdar, M., Davoudi, S., Borjkhani, M., Hosseinmardi, N., Behzadi, G., & Janahmadi, M. (2018) · Brain Research · doi:10.1016/j.brainres.2018.12.011 · Cited by 40
Weston, C. S. E. (2019) · Brain Sciences · doi:10.3390/brainsci9060130 · Cited by 48
“Further, studies of sensory system disruptions may cast light on the causation of the amygdala cellular abnormalities that chiefly affect the lateral amygdaloid nucleus, which receives the heaviest sensory inputs [49,182,183].”
BackgroundSciara, A., Beasley, B., Crawford, J. D., Anderson, E. P., Carrasco, T., Zheng, S., Ordway, G. A., & Chandley, M. (2020) · Autism Research · doi:10.1002/aur.2284 · Cited by 42
“In the amygdala, neuronal numbers are reduced overall but in particular in the lateral nucleus [Schumann & Amaral, 2006] while the microglia marker IBA-1 was increased in the region [Morgan, Barger, Amaral, & Schumann, 2014].”
Liu, X., Bautista, J., Liu, E., & Zikopoulos, B. (2020) · Molecular Autism · doi:10.1186/s13229-020-00390-x · Cited by 41
Does bilateral damage to the human amygdala produce autistic symptoms?
Paul, L. K., Corsello, C. M., Tranel, D., & Adolphs, R. (2010) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-010-9056-1 · Cited by 41
“For instance, abnormal cell packing density has been reported in modern stereological studies (Schumann and Amaral 2006), and morphometric studies have found an abnormal developmental trajectory of amygdala volume in autism using structural MRI (Mosconi et al. 2009; Nacewicz et al. 2006; Schumann…”
BackgroundNeural correlates to seen gaze-direction and head orientation in the macaque monkey amygdala
Tazumi, T., Hori, E., Maior, R. S., Ono, T., & Nishijo, H. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.04.028 · Cited by 39
Neuroimaging in autism spectrum disorders: 1H-MRS and NIRS study
Mori, K., Toda, Y., Ito, H., Mori, T., Mori, K., Goji, A., Hashimoto, H., Tani, H., Miyazaki, M., Harada, M., et al. (2015) · The Journal of Medical Investigation · doi:10.2152/jmi.62.29 · Cited by 40
Chen, Y.-W., Lin, H., Ng, M.-C., Hsiao, Y., Wang, C.-C., Gean, P., & Chen, P. S. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00219 · Cited by 40
“ORIGINAL RESEARCH ARTICLE published: 17 June 2014 doi: 10.3389/fnbeh.2014.00219 Activation of mGluR2/3 underlies the effects of”
BackgroundInfluentialCarlo, C. N., Stefanacci, L., Semendeferi, K., & Stevens, C. F. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22264 · Cited by 38
Sweigert, J., John, T. S., Begay, K. K., Davis, G. E., MUNSON, J. A., Shankland, E. G., Estes, A. M., Dager, S. R., & Kleinhans, N. M. (2020) · Brain Sciences · doi:10.3390/brainsci10060362 · Cited by 43
“Among individuals with autism, structural and functional alterations have been identified in some of these regions, including the piriform cortex [12], the orbitofrontal cortex [21], and the amygdala [22,23].”
BackgroundAutism and EMF? Plausibility of a pathophysiological link – Part I
Herbert, M. R., & Sage, C. (2013) · Pathophysiology · doi:10.1016/j.pathophys.2013.08.001 · Cited by 37
“[135] C.”
Unruh, K. E., Martin, L. E., Magnon, G. C., Vaillancourt, D. E., Sweeney, J. A., & Mosconi, M. W. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00286.2019 · Cited by 34
Cory‐Slechta, D. A., Sobolewski, M., & Oberdörster, G. (2020) · Atmosphere · doi:10.3390/atmos11101098 · Cited by 36
“Hypothesized mechanisms of these disorders, such as mitochondrial dysfunction, have been reported in all NDDs, particularly in SCZ [276,277,283,285,286,288,289,291], and could be related to alterations in neuronal fate [371,372].”
BackgroundSéguin, D., Pac, S., Wang, J., Nicolson, R., Martínez-Trujillo, J., & Duerden, E. G. (2021) · Brain and Behavior · doi:10.1002/brb3.2299 · Cited by 37
“Findings are supported by recent studies examining cellular differences in amygdala subnuclei revealed throughpost-mortemanalysis of brain tissue acquired in individuals with ASD (Schumann & Amaral 2006).”
BackgroundMethodResultInfluentialPrenatal valproic acid exposure disrupts tonotopic c-Fos expression in the rat brainstem
Dubiel, A., & Kulesza, R. J. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.10.043 · Cited by 35
“…et al., 1988; Arin et al., 1991; Piven et al., 1992; Hashimoto et al., 1993; Raymond et al., 1996; Fatemi et al., 2002b; Palmen et al., 2004; Schumann and Amaral, 2006; Kulesza and Mangunay, 2008; Whitney et al., 2008; Weigiel et al., 2010; Kulesza et al., 2011; Stoner et al., 2014; Wegiel…”
The association between perceived social support and amygdala structure
Sato, W., Kochiyama, T., Kubota, Y., Uono, S., Sawada, R., Yoshimura, S., & Toichi, M. (2016) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2016.03.036 · Cited by 35
“…a human stereological study that detected structural problems only in these subregions in autistic individuals with impaired social interactions (Schumann & Amaral, 2006), and comparative anatomical studies that revealed an volume increase in these, but not the centromedial, regions in…”
BackgroundCheng, Y., Chou, K., Fan, Y., & Lin, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018905 · Cited by 34
“Moreover, the autistic amygdala demonstrated an abnormal pattern of development with early enlargement in childhood followed by a reduction beginning from adolescence [22].”
BackgroundA revisit of the amygdala theory of autism: Twenty years after
Wang, S., & Li, X. (2023) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2023.108519 · Cited by 38
Trutzer, I. M., García‐Cabezas, M. Á., & Zikopoulos, B. (2019) · Acta Neuropathologica Communications · doi:10.1186/s40478-019-0684-8 · Cited by 33
Ahadullah, Yau, S., Lu, H., Lee, T. M. C., Guo, H., & Chan, C. C. H. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.06.043 · Cited by 33
Aitken, K. J. (2008) · The Keio Journal of Medicine · doi:10.2302/kjm.57.15 · Cited by 33
Sosa-Díaz, N., Bringas, M. E., Atzori, M., & Flores, G. (2014) · Synapse · doi:10.1002/syn.21759 · Cited by 31
O'Brien, F. M., Page, L., Tuura, R., Bolton, P., Sharma, A. K., Baird, G., Daly, E., Hallahan, B. P., Conroy, R. M., Foy, C., et al. (2010) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2010.08.007 · Cited by 32
“On the other hand, this hypothesis is not supported by a recent study (and the first to use quantitative stereological methods) which reported reduced neuronal density in people with autism (Schumann and Amaral, 2006) and consistent with other MRS studies of ASD reporting reduced NAA concentrations in the AHC (Otsuka…”
BackgroundResultMori, K., Toda, Y., Ito, H., Mori, T., Goji, A., Fujii, E., Miyazaki, M., Harada, M., & Kagami, S. (2012) · Brain and Development · doi:10.1016/j.braindev.2012.09.016 · Cited by 32
“Furthermore, Schumann and Amaral reported significantly fewer neurons in the bilateral amygdalae of the postmortem autistic brain [14].”
BackgroundMalisza, K. L., Clancy, C., Shiloff, D., Holden, J., Jones, C., Paulson, K., Yu, D. C. T., Summers, R., & Chudley, A. E. (2011) · ijamh · doi:10.1515/ijamh.2011.055 · Cited by 32
“Recently, postmortem studies have shown that subjects with ASD have signifi cantly fewer neurons in the amygdala compared to typical control subjects (39) , which could contribute to the reduced functional activity.”
BackgroundRestriction Spectrum Imaging As a Potential Measure of Cortical Neurite Density in Autism
Carper, R. A., Treiber, J. M., White, N. S., Kohli, J. S., & Müller, R. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00610 · Cited by 29
“Increased cell packing density has been found in anterior cingulate, hippocampus and amygdala (Kemper and Bauman, 1998; Schumann and Amaral, 2006), and in prefrontal cortex by some (Bailey et al.”
BackgroundResultMiller, M. W. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm024 · Cited by 31
“This difference largely resulted from the dramatic and significant (P 0.05) increase in the nonsomatic volume in the Group A/B monkeys relative to the Group C/D macaques (+37.8”
ResultInfluentialNeuroanatomy and Neuropathology of Autism Spectrum Disorder in Humans
Ecker, C., Schmeißer, M. J., Loth, E., & Murphy, D. (2017) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-319-52498-6_2 · Cited by 32
From Loci to Networks and Back Again
Müller, R. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1416.014 · Cited by 30
“…such as reduced neuronal size and increased cell packing density (Bauman & Kemper, 1994; Raymond et al., 1996) or reduced numbers of neurons (Schumann & Amaral, 2006) in the medial temporal lobe (amygdala, hippocampus, etc.) and possibly in the anterior cingulate gyrus (Bauman & Kemper,…”
BackgroundQuantification of the Stapedial Reflex Reveals Delayed Responses in Autism
Lukose, R., Brown, K., Barber, C. M., & Kulesza, R. J. (2013) · Autism Research · doi:10.1002/aur.1297 · Cited by 30
“…& Kuroda, 1993; Kulesza and Mangunay, 2008; Kulesza, Lukose, & Stevens, 2011; Palmen, van Engeland, Hof, & Schmitz, 2004; Piven, Nehme, & Simon, 1992; Raymond, Bauman, & Kemper, 1989; Ritvo et al., 1986; Schumann & Amaral, 2006; Wegiel et al., 2010; Whitney, Kemper, Bauman, Rosene, & Blatt, 2008].”
Morphofunctional Alterations of the Hypothalamus and Social Behavior in Autism Spectrum Disorders
Carìa, A., Ciringione, L., & de Falco, S. (2020) · Brain Sciences · doi:10.3390/brainsci10070435 · Cited by 31
Altered Development of Amygdala-Connected Brain Regions in Males and Females with Autism
Lee, J. K., Andrews, D. S., Öztürk, A., Solomon, M., Rogers, S. J., Amaral, D. G., & Nordahl, C. W. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.0053-22.2022 · Cited by 32
Self-citationNguyen, M. N., Nishijo, M., Nguyen, A. T. N., Bor, A., Nakamura, T., Hori, E., Nakagawa, H., Ono, T., & Nishijo, H. (2013) · Toxicology · doi:10.1016/j.tox.2013.09.005 · Cited by 30
Lynch, G. T. F., James, S., & VanDam, M. (2017) · Autism Research · doi:10.1002/aur.1888 · Cited by 29
“…ASD neuropathology reveal structural change and a reduction in the number of neurons within the amygdala later in development, although it is not known whether this neuropathology is unique to the amygdala or reflects a more generalized condition of atrophy across regions [Schumann & Amaral, 2006].”
BackgroundSome assessments of the amygdala role in suprahypothalamic neuroendocrine regulation: a minireview.
Talarovičová, A., Kršková, L., & Kiss, A. (2007) · PubMed · Cited by 29
Functional brain abnormalities associated with comorbid anxiety in autism spectrum disorder
Bartolotti, J., Sweeney, J. A., & Mosconi, M. W. (2020) · Development and Psychopathology · doi:10.1017/s0954579420000772 · Cited by 30
A neuronal social trait space for first impressions in the human amygdala and hippocampus
Cao, R., Lin, C., Hodge, J., Li, X., Todorov, A. T., Brandmeir, N. J., & Wang, S. (2022) · Molecular Psychiatry · doi:10.1038/s41380-022-01583-x · Cited by 27
“A specific neural structure hypothesized to underlie deficits in face processing in ASD is the amygdala, a brain structure that has long been implicated in autism [22, 31].”
BackgroundInfluentialMetabolite alterations in the hippocampus of high-functioning adult subjects with autism
Suzuki, K., Nishimura, K., Sugihara, G., Nakamura, K., Tsuchiya, K. J., Matsumoto, K., Takebayashi, K., Isoda, H., Sakahara, H., Sugiyama, T., et al. (2009) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709990952 · Cited by 27
“Received 12 April 2009 ; Reviewed 2 June 2009 ; Revised 13 June 2009 ; Accepted 8 October 2009 ; First published online 9 November 2009 Key words : Aggression, autism, hippocampus, magnetic resonance spectroscopy.”
BackgroundLactobacillus reuteri normalizes altered fear memory in male Cntnap4 knockout mice
Zhang, W., Huang, J., Gao, F., You, Q.-L., Ding, L., Gong, J., Zhang, M., Ma, R., Zheng, S., Sun, X., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104323 · Cited by 29
Kleinhans, N. M., Richards, T. L., Weaver, K. E., Liang, O., Dawson, G., & Aylward, E. (2009) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-009-0707-6 · Cited by 26
“…of the biochemical alterations in the amygdala– hippocampal region (Endo et al. 2007; Gabis et al. 2008; Otsuka et al. 1999; Page et al. 2006) and a quantitative postmortem study that reported reduced numbers of neurons in the amygdala (Schumann and Amaral 2006), and may be due to a lack of power.”
BackgroundAutism and EMF? Plausibility of a pathophysiological link part II
Herbert, M. R., & Sage, C. (2013) · Pathophysiology · doi:10.1016/j.pathophys.2013.08.002 · Cited by 28
Merali, Z., Presti-Torres, J., MacKay, J. C., Johnstone, J., Du, L., St-Jean, A., Levesque, D., Kent, P., Schwartsmann, G., Roesler, R., et al. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.008 · Cited by 25
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“In addition to the abnormal developmental trajectory of the amygdala, there is a concomitant early overgrowth in ASD.”
BackgroundDługosz, A., Wróblewski, M., Błaszak, B., & Szulc, J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26020808 · Cited by 30
“Neuronal loss has been observed in the cerebellum [127], and stereological studies have also indicated significant losses in the amygdala area [128].”
Metadata
- Authors
- Schumann, C. M., & Amaral, D. G.
- Affiliations
- University of California, Davis (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-07-19
- Volume
- 26
- Issue
- 29
- Pages
- 7674-7679
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6674270
- OpenAlex
- W2087838692
- Cited by
- 413
- References
- 35
- Citations by year
- 2026: 3 · 2025: 11 · 2024: 12 · 2023: 18 · 2022: 19 · 2021: 20 · 2020: 20 · 2019: 16 · 2018: 17 · 2017: 25 · 2016: 26 · 2015: 25 · 2014: 31 · 2013: 26 · 2012: 23
- FWCI
- 10.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Miami
- National Institutes of Health (MH41479)
- National Institute of Mental Health (MH-41479)
- National Institute of Child Health and Human Development
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Keywords
- autism spectrum disorder, amygdala, neuron number, neuronal loss, lateral nucleus, central nucleus, postnatal brain development, brain volume, postmortem brain
- MeSH terms
- Adolescent, Adult, Amygdala, Autistic Disorder, Cadaver, Cell Count, Child, Humans, Male, Neurons, Case-Control Studies
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