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Acta Neuropathologica

, Volume 134, Issue 4, pp 537–566 | Cite as

Autism spectrum disorder: neuropathology and animal models

  • Merina Varghese
  • Neha Keshav
  • Sarah Jacot-Descombes
  • Tahia Warda
  • Bridget Wicinski
  • Dara L. Dickstein
  • Hala Harony-Nicolas
  • Silvia De Rubeis
  • Elodie Drapeau
  • Joseph D. Buxbaum
  • Patrick R. Hof
Review

Abstract

Autism spectrum disorder (ASD) has a major impact on the development and social integration of affected individuals and is the most heritable of psychiatric disorders. An increase in the incidence of ASD cases has prompted a surge in research efforts on the underlying neuropathologic processes. We present an overview of current findings in neuropathology studies of ASD using two investigational approaches, postmortem human brains and ASD animal models, and discuss the overlap, limitations, and significance of each. Postmortem examination of ASD brains has revealed global changes including disorganized gray and white matter, increased number of neurons, decreased volume of neuronal soma, and increased neuropil, the last reflecting changes in densities of dendritic spines, cerebral vasculature and glia. Both cortical and non-cortical areas show region-specific abnormalities in neuronal morphology and cytoarchitectural organization, with consistent findings reported from the prefrontal cortex, fusiform gyrus, frontoinsular cortex, cingulate cortex, hippocampus, amygdala, cerebellum and brainstem. The paucity of postmortem human studies linking neuropathology to the underlying etiology has been partly addressed using animal models to explore the impact of genetic and non-genetic factors clinically relevant for the ASD phenotype. Genetically modified models include those based on well-studied monogenic ASD genes (NLGN3, NLGN4, NRXN1, CNTNAP2, SHANK3, MECP2, FMR1, TSC1/2), emerging risk genes (CHD8, SCN2A, SYNGAP1, ARID1B, GRIN2B, DSCAM, TBR1), and copy number variants (15q11-q13 deletion, 15q13.3 microdeletion, 15q11-13 duplication, 16p11.2 deletion and duplication, 22q11.2 deletion). Models of idiopathic ASD include inbred rodent strains that mimic ASD behaviors as well as models developed by environmental interventions such as prenatal exposure to sodium valproate, maternal autoantibodies, and maternal immune activation. In addition to replicating some of the neuropathologic features seen in postmortem studies, a common finding in several animal models of ASD is altered density of dendritic spines, with the direction of the change depending on the specific genetic modification, age and brain region. Overall, postmortem neuropathologic studies with larger sample sizes representative of the various ASD risk genes and diverse clinical phenotypes are warranted to clarify putative etiopathogenic pathways further and to promote the emergence of clinically relevant diagnostic and therapeutic tools. In addition, as genetic alterations may render certain individuals more vulnerable to developing the pathological changes at the synapse underlying the behavioral manifestations of ASD, neuropathologic investigation using genetically modified animal models will help to improve our understanding of the disease mechanisms and enhance the development of targeted treatments.

Keywords

Autism spectrum disorder Cerebral cortex Genetically modified animal models Neuronal morphology Synapse Idiopathic autism models 

Abbreviations

ASD

Autism spectrum disorders

PFC

Prefrontal cortex

FG

Fusiform gyrus

CA1

Cornu ammonis 1

GABA

γ-Aminobutyric acid

VEN

von Economo neuron

FI

Frontoinsular

ACC

Anterior cingulate cortex

aMCC

Anterior midcingulate cortex

PCC

Posterior cingulate cortex

PIOTG

Postero-inferior occipitotemporal gyrus

CNVs

Copy number variations

NLGN

Neuroligins

MRI

Magnetic resonance imaging

KO

Knockout

KI

Knock-in

PSD

Postsynaptic density

AMPA

α-Amino-3-hydroxyl-5-methyl-4-isoxazole-propionic acid

NMDA

N-Methyl-d-aspartic acid

NRXN

Neurexins

WT

Wild type

CNTNAP2

Contactin associated protein-like 2

SHANK

SH3 and multiple ankyrin repeat domains protein

MECP2

Methyl-CpG-binding protein 2

FMR1

Fragile X mental retardation 1

FMRP

Fragile X mental retardation protein

UBE3A

E6AP-E3 ubiquitin protein ligase

TSC

Tuberous sclerosis

mTOR

Mammalian target of rapamycin

CHD8

Chromodomain helicase DNA-binding protein 8

SCN2A

Sodium channel, voltage-gated, type II alpha subunit

SYNGAP1

Synaptic GTPase activating protein 1

ARID1B

AT-rich interactive domain containing protein 1B

GRIN2B

Glutamate receptor ionotropic, NMDA 2B

DSCAM

Down syndrome cell adhesion molecule

TBR1

T-brain-1

VPA

Sodium valproate

MIA

Maternal immune activation

Notes

Acknowledgements

We are indebted to all of the families for generously donating postmortem brain specimens. Our work on autism is supported by the Seaver Foundation (to JDB and PRH), the Simons Foundation (Grant FA #345922 from Foundation Associates, LLC, to PRH), Autism Speaks (the Autism Celloidin Library Project to PRH), the Foundation for Prader–Willi Research (to PRH and MV) and the National Institutes of Health (Grants MH093725 and MH101584 to JDB and PRH). SDR is a Seaver fellow.

Author contributions

MV and NK wrote the manuscript; SJ-D, HH-N, TW, BW, DLD, SDR, ED, JDB, and PRH provided content and revised the manuscript; all authors read and approved the final version.

Compliance with ethical standards

Funding

This study was supported by the Seaver Foundation (JDB, PRH), the Simons Foundation Grant FA #345922 (PRH), Autism Speaks and the Autism Celloidin Library Project (PRH), the Foundation for Prader–Willi Research (to PRH and MV), and the National Institutes of Health Grants R01 MH093725 (JDB, PRH) and R01 MH101584 (JDB, PRH). SDR is a Seaver Fellow.

Conflict of interest

The authors declare that they have no conflict of interest.

Disclaimer

The opinions expressed herein are those of the authors and are not necessarily representative of those of the Uniformed Services University of the Health Sciences, the Department of Defense; or, the United States Army, Navy, or Air Force (DLD).

Supplementary material

401_2017_1736_MOESM1_ESM.pdf (532 kb)
Supplementary material 1 (PDF 532 kb)

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Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Merina Varghese
    • 1
    • 2
  • Neha Keshav
    • 1
    • 2
    • 3
  • Sarah Jacot-Descombes
    • 1
    • 2
    • 5
  • Tahia Warda
    • 1
    • 2
  • Bridget Wicinski
    • 1
    • 2
  • Dara L. Dickstein
    • 1
    • 2
    • 6
  • Hala Harony-Nicolas
    • 3
    • 4
  • Silvia De Rubeis
    • 3
    • 4
  • Elodie Drapeau
    • 3
    • 4
  • Joseph D. Buxbaum
    • 1
    • 2
    • 3
    • 4
  • Patrick R. Hof
    • 1
    • 2
    • 3
  1. 1.Fishberg Department of NeuroscienceIcahn School of Medicine at Mount SinaiNew YorkUSA
  2. 2.Friedman Brain InstituteIcahn School of Medicine at Mount SinaiNew YorkUSA
  3. 3.Seaver Autism Center for Research and TreatmentIcahn School of Medicine at Mount SinaiNew YorkUSA
  4. 4.Department of PsychiatryIcahn School of Medicine at Mount SinaiNew YorkUSA
  5. 5.Unit of Psychiatry, Department of Children and TeenagersUniversity Hospitals and School of MedicineGenevaSwitzerland
  6. 6.Department of PathologyUniformed Services University of the Health SciencesBethesdaUSA

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