Advances in Nonhuman Primate Models of Autism: Integrating Neuroscience and Behavior

Overview

Journal Exp Neurol

Specialty Neurology

Date 2017 Aug 5

PMID 28774750

Citations 39

Authors

M D Bauman

C M Schumann

Affiliations

Soon will be listed here.

Abstract

Given the prevalence and societal impact of autism spectrum disorders (ASD), there is an urgent need to develop innovative preventative strategies and treatments to reduce the alarming number of cases and improve core symptoms for afflicted individuals. Translational efforts between clinical and preclinical research are needed to (i) identify and evaluate putative causes of ASD, (ii) determine the underlying neurobiological mechanisms, (iii) develop and test novel therapeutic approaches and (iv) ultimately translate basic research into safe and effective clinical practices. However, modeling a uniquely human brain disorder, such as ASD, will require sophisticated animal models that capitalize on unique advantages of diverse species including drosophila, zebra fish, mice, rats, and ultimately, species more closely related to humans, such as the nonhuman primate. Here we discuss the unique contributions of the rhesus monkey (Macaca mulatta) model to ongoing efforts to understand the neurobiology of the disorder, focusing on the convergence of brain and behavior outcome measures that parallel features of human ASD.

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References

Schumann C, Hamstra J, Goodlin-Jones B, Lotspeich L, Kwon H, Buonocore M . The amygdala is enlarged in children but not adolescents with autism; the hippocampus is enlarged at all ages. J Neurosci. 2004; 24(28):6392-401. PMC: 6729537. DOI: 10.1523/JNEUROSCI.1297-04.2004. View

Goines P, Croen L, Braunschweig D, Yoshida C, Grether J, Hansen R . Increased midgestational IFN-γ, IL-4 and IL-5 in women bearing a child with autism: A case-control study. Mol Autism. 2011; 2:13. PMC: 3170586. DOI: 10.1186/2040-2392-2-13. View

Silverman J, Yang M, Lord C, Crawley J . Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci. 2010; 11(7):490-502. PMC: 3087436. DOI: 10.1038/nrn2851. View

Estes M, Kimberley McAllister A . Immune mediators in the brain and peripheral tissues in autism spectrum disorder. Nat Rev Neurosci. 2015; 16(8):469-86. PMC: 5650494. DOI: 10.1038/nrn3978. View

Paukner A, Simpson E, Ferrari P, Mrozek T, Suomi S . Neonatal imitation predicts how infants engage with faces. Dev Sci. 2014; 17(6):833-40. PMC: 4211944. DOI: 10.1111/desc.12207. View

Green J, Hollander E . Autism and oxytocin: new developments in translational approaches to therapeutics. Neurotherapeutics. 2010; 7(3):250-7. PMC: 5084228. DOI: 10.1016/j.nurt.2010.05.006. View

t Hart B . Reverse translation of failed treatments can help improving the validity of preclinical animal models. Eur J Pharmacol. 2015; 759:14-8. DOI: 10.1016/j.ejphar.2015.03.030. View

Abdallah M, Larsen N, Grove J, Norgaard-Pedersen B, Thorsen P, Mortensen E . Amniotic fluid chemokines and autism spectrum disorders: an exploratory study utilizing a Danish Historic Birth Cohort. Brain Behav Immun. 2011; 26(1):170-6. DOI: 10.1016/j.bbi.2011.09.003. View

Kinnally E, Karere G, Lyons L, Mendoza S, Mason W, Capitanio J . Serotonin pathway gene-gene and gene-environment interactions influence behavioral stress response in infant rhesus macaques. Dev Psychopathol. 2010; 22(1):35-44. PMC: 3170845. DOI: 10.1017/S0954579409990241. View

10.

Capitanio J, Widaman K . Confirmatory factor analysis of personality structure in adult male rhesus monkeys (Macaca mulatta). Am J Primatol. 2005; 65(3):289-94. DOI: 10.1002/ajp.20116. View

11.

Gadad B, Li W, Yazdani U, Grady S, Johnson T, Hammond J . Administration of thimerosal-containing vaccines to infant rhesus macaques does not result in autism-like behavior or neuropathology. Proc Natl Acad Sci U S A. 2015; 112(40):12498-503. PMC: 4603476. DOI: 10.1073/pnas.1500968112. View

12.

Boksa P . Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav Immun. 2010; 24(6):881-97. DOI: 10.1016/j.bbi.2010.03.005. View

13.

Ruhela R, Prakash A, Medhi B . An urgent need for experimental animal model of autism in drug development. Ann Neurosci. 2015; 22(1):44-9. PMC: 4410529. DOI: 10.5214/ans.0972.7531.220210. View

14.

Chareyron L, Banta Lavenex P, Amaral D, Lavenex P . Stereological analysis of the rat and monkey amygdala. J Comp Neurol. 2011; 519(16):3218-39. PMC: 4342351. DOI: 10.1002/cne.22677. View

15.

Modabbernia A, Velthorst E, Reichenberg A . Environmental risk factors for autism: an evidence-based review of systematic reviews and meta-analyses. Mol Autism. 2017; 8:13. PMC: 5356236. DOI: 10.1186/s13229-017-0121-4. View

16.

Lord C, Risi S, Lambrecht L, Cook Jr E, Leventhal B, DiLavore P . The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. J Autism Dev Disord. 2000; 30(3):205-23. View

17.

Raper J, Stephens S, Henry A, Villarreal T, Bachevalier J, Wallen K . Neonatal amygdala lesions lead to increased activity of brain CRF systems and hypothalamic-pituitary-adrenal axis of juvenile rhesus monkeys. J Neurosci. 2014; 34(34):11452-60. PMC: 4138348. DOI: 10.1523/JNEUROSCI.0269-14.2014. View

18.

Nestler E, Hyman S . Animal models of neuropsychiatric disorders. Nat Neurosci. 2010; 13(10):1161-9. PMC: 3750731. DOI: 10.1038/nn.2647. View

19.

Semendeferi K, Lu A, Schenker N, Damasio H . Humans and great apes share a large frontal cortex. Nat Neurosci. 2002; 5(3):272-6. DOI: 10.1038/nn814. View

20.

Insel T . A neurobiological basis of social attachment. Am J Psychiatry. 1997; 154(6):726-35. DOI: 10.1176/ajp.154.6.726. View