Subregional differences in intrinsic amygdala hyperconnectivity and hypoconnectivity in autism spectrum disorder

Autism Research

Volumn 9, Issue 7, 2016, Pages 760-772

  Kleinhans, Natalia M ^a,b   Reiter, Maya A ^a,b   Neuhaus, Emily ^b   Pauley, Greg ^a,b   Martin, Nathalie ^a   Dager, Stephen ^a,b   Estes, Annette ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

amygdala; anxiety; autism; centromedial; depression; laterobasal; resting state fMRI; superficial

Indexed keywords

ADOLESCENT; ADULT; AMYGDALA; ANXIETY; ARTICLE; AUTISM; AUTISM DIAGNOSTIC INTERVIEW REVISED; AUTISM DIAGNOSTIC OBSERVATION SCHEDULE; BECK ANXIETY INVENTORY; BECK DEPRESSION INVENTORY; BRAIN REGION; CLINICAL ARTICLE; COMORBIDITY; CONTROLLED STUDY; DEPRESSION; DISEASE SEVERITY; FEMALE; FUNCTIONAL ANATOMY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL STATUS; HUMAN; MALE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SOCIAL DISABILITY; SYMPTOM;

EID: 84978857994     PISSN: 19393792     EISSN: 19393806     Source Type: Journal    
DOI: 10.1002/aur.1589     Document Type: Article

References (53)

1. Amunts, K., Kedo, O., Kindler, M., Pieperhoff, P., Mohlberg, H., Shah, N. J., … Zilles, K. (2005). Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: Intersubject variability and probability maps. Anatomy and Embryology (Berl), 210(5-6), 343–352.
2. Assaf, M., Hyatt, C. J., Wong, C. G., Johnson, M. R., Schultz, R. T., Hendler, T., & Pearlson, G. D. (2013). Mentalizing and motivation neural function during social interactions in autism spectrum disorders. Neuroimage Clinical, 3, 321–331.
3. Banks, S. J., Eddy, K. T., Angstadt, M., Nathan, P. J., & Phan, K. L. (2007). Amygdala-frontal connectivity during emotion regulation. Social Cognitive and Affective Neuroscience, 2(4), 303–312.
4. Birn, R. M., Diamond, J. B., Smith, M. A., & Bandettini, P. A. (2006). Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage, 31(4), 1536–1548.
5. Bzdok, D., Laird, A. R., Zilles, K., Fox, P. T., & Eickhoff, S. B. (2013). An investigation of the structural, connectional, and functional subspecialization in the human amygdala. Humand Brain Mapping, 34(12), 3247–3266.
6. Cerliani, L., Mennes, M., Thomas, R. M., Di Martino, A., Thioux, M., & Keysers, C. (2015). Increased Functional Connectivity Between Subcortical and Cortical Resting-State Networks in Autism Spectrum Disorder. JAMA Psychiatry, 72(8), 767–777 doi: 10.1001/jamapsychiatry.2015.0101
7. Courchesne, E., Yeung-Courchesne, R., Press, G. A., Hesselink, J. R., & Jernigan, T. L. (1988). Hypoplasia of cerebellar vermal lobules VI and VII in autism. The New England Journal of Medicine, 318(21), 1349–1354. doi: 10.1056/nejm198805263182102
8. Dawson, G. (2008). Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder. Development and Psychopathology, 20(3), 775–803.
9. Dawson, G., Webb, S. J., & McPartland, J. (2005). Understanding the nature of face processing impairment in autism: Insights from behavioral and electrophysiological studies. Developmental Neuropsychology, 27(3), 403–424.
10. Delmonte, S., Gallagher, L., O'Hanlon, E., McGrath, J., & Balsters, J. H. (2013). Functional and structural connectivity of frontostriatal circuitry in Autism Spectrum Disorder. Frontiers in Human Neuroscience, 7, 430.
11. Desikan, R. S., Segonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., … Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31(3), 968–980.
12. Di Martino, A., Yan, C. G., Li, Q., Denio, E., Castellanos, F. X., Alaerts, K., … Milham, M. P. (2014). The autism brain imaging data exchange: Towards a large-scale evaluation of the intrinsic brain architecture in autism. Molecular Psychiatry, 19(6), 659–667. doi: 10.1038/mp.2013.78
13. Drevets, W., Price, J., & Furey, M. (2008). Brain structural and functional abnormalities in mood disorders: Implications for neurocircuitry models of depression. Brain Structure and Function, 213(1-2), 93–118.
14. Esbensen, A., Greenberg, J., Seltzer, M., & Aman, M. (2009). A longitudinal investigation of psychotropic and non-psychotropic medication use among adolescents and adults with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(9), 1339–1349.
15. Gaffrey, M. S., Kleinhans, N. M., Haist, F., Akshoomoff, N., Campbell, A., Courchesne, E., & Muller, R. A. (2007). Atypical [corrected] participation of visual cortex during word processing in autism: An fMRI study of semantic decision. Neuropsychologia, 45(8), 1672–1684.
16. Glover, G. H., Li, T. Q., & Ress, D. (2000). Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magnetic Resonance in Medical Sciences, 44(1), 162–167.
17. Grijalva, C. V., Levin, E. D., Morgan, M., Roland, B., & Martin, F. C. (1990). Contrasting effects of centromedial and basolateral amygdaloid lesions on stress-related responses in the rat. Physiology and Behavior, 48(4), 495–500.
18. Hashimoto, T., Tayama, M., Murakawa, K., Yoshimoto, T., Miyazaki, M., Harada, M., & Kuroda, Y. (1995). Development of the brainstem and cerebellum in autistic patients. Journal of Autism and Developmental Disorders, 25(1), 1–18.
19. Hilton, C. L., Harper, J. D., Kueker, R. H., Lang, A. R., Abbacchi, A. M., Todorov, A., & LaVesser, P. D. (2010). Sensory responsiveness as a predictor of social severity in children with high functioning autism spectrum disorders. Journal of Autism and Developmental Disorders, 40(8), 937–945.
20. Kana, R. K., Liu, Y., Williams, D. L., Keller, T. A., Schipul, S. E., Minshew, N. J., & Just, M. A. (2013). The local, global, and neural aspects of visuospatial processing in autism spectrum disorders. Neuropsychologia, 51(14), 2995–3003. doi: 10.1016/j.neuropsychologia.2013.10.013
21. Kaufmann, W. E., Cooper, K. L., Mostofsky, S. H., Capone, G. T., Kates, W. R., Newschaffer, C. J., … Lanham, D. C. (2003). Specificity of cerebellar vermian abnormalities in autism: A quantitative magnetic resonance imaging study. Journal of Child Neurology, 18(7), 463–470.
22. Keehn, B., Brenner, L., Palmer, E., Lincoln, A. J., & Muller, R. A. (2008). Functional brain organization for visual search in ASD. Journal of the International Neuropsychological Society, 14(6), 990–1003. doi: 10.1017/s1355617708081356
23. Kim, J. A., Szatmari, P., Bryson, S. E., Streiner, D. L., & Wilson, F. J. (2000). The prevalence of anxiety and mood problems among children with autism and asperger syndrome. Autism, 4(2), 117–132. doi: 10.1177/1362361300004002002
24. Kim, J. E., Lyoo, I. K., Estes, A. M., Renshaw, P. F., Shaw, D. W., Friedman, S. D., … Dager, S. R. (2010). Laterobasal amygdalar enlargement in 6- to 7-year-old children with autism spectrum disorder. Archives of General Psychiatry, 67(11), 1187–1197.
25. Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., & Aylward, E. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. American Journal of Psychiatry, 166(4), 467–475.
26. Kleinhans, N. M., Richards, T., Johnson, L. C., Weaver, K. E., Greenson, J., Dawson, G., & Aylward, E. (2011). fMRI evidence of neural abnormalities in the subcortical face processing system in ASD. Neuroimage, 54(1), 697–704.
27. Kleinhans, N. M., Richards, T., Sterling, L., Stegbauer, K. C., Mahurin, R., Johnson, L. C., … Aylward, E. (2008). Abnormal functional connectivity in autism spectrum disorders during face processing. Brain, 131(Pt 4), 1000–1012.
28. Kleinhans, N. M., Richards, T., Weaver, K., Johnson, L. C., Greenson, J., Dawson, G., & Aylward, E. (2010). Association between amygdala response to emotional faces and social anxiety in autism spectrum disorders. Neuropsychologia, 48(12), 3665–3670.
29. Lemieux, L., Salek-Haddadi, A., Lund, T. E., Laufs, H., & Carmichael, D. (2007). Modelling large motion events in fMRI studies of patients with epilepsy. Magnetic Resonance Imaging., 25(6), 894–901.
30. Mandell, D. S., Morales, K. H., Marcus, S. C., Stahmer, A. C., Doshi, J., & Polsky, D. E. (2008). Psychotropic medication use among medicaid-enrolled children with autism spectrum disorders. Pediatrics, 121(3), e441–e448. doi: 10.1542/peds.2007-0984
31. Mazefsky, C. A., Borue, X., Day, T. N., & Minshew, N. J. (2014). Emotion regulation patterns in adolescents with high-functioning autism spectrum disorder: Comparison to typically developing adolescents and association with psychiatric symptoms. Autism Research, 7(3), 344–354. doi: 10.1002/aur.1366.
32. Mazefsky, C. A., Folstein, S. E., & Lainhart, J. E. (2008). Overrepresentation of mood and anxiety disorders in adults with autism and their first-degree relatives: What does it mean? Autism Research, 1(3), 193–197.
33. McDonald, A. J. (1991). Topographical organization of amygdaloid projections to the caudatoputamen, nucleus accumbens, and related striatal-like areas of the rat brain. Neuroscience, 44(1), 15–33.
34. Mosher, C. P., Zimmerman, P. E., & Gothard, K. M. (2010). Response characteristics of basolateral and centromedial neurons in the primate amygdala. Journal of Neuroscience, 30(48), 16197–16207. doi: 10.1523/JNEUROSCI.3225-10.2010
35. Muller, R. A. (2007). The study of autism as a distributed disorder. Mental Retardation and Developmental Disabilities Research Reviews, 13(1), 85–95.
36. Muller, R. A., Shih, P., Keehn, B., Deyoe, J. R., Leyden, K. M., & Shukla, D. K. (2011). Underconnected, but how? A survey of functional connectivity mri studies in autism spectrum disorders. Cerebral Cortex, 21(10), 2233–2243.
37. Myers-Schulz, B., & Koenigs, M. (2012). Functional anatomy of ventromedial prefrontal cortex: Implications for mood and anxiety disorders. Molecular Psychiatry, 17(2), 132–141.
38. Oler, J. A., Fox, A. S., Shelton, S. E., Rogers, J., Dyer, T. D., Davidson, R. J., … Kalin, N. H. (2010). Amygdalar and hippocampal substrates of anxious temperament differ in their heritability. Nature, 466(7308), 864–868. doi: 10.1038/nature09282
39. Ramasubbu, R., Konduru, N., Cortese, F., Bray, S., Gaxiola-Valdez, I., & Goodyear, B. (2014). Reduced intrinsic connectivity of amygdala in adults with major depressive disorder. Frontiers in Psychiatry, 5, 17. doi: 10.3389/fpsyt.2014.00017
40. Richey, J. A., Damiano, C. R., Sabatino, A., Rittenberg, A., Petty, C., Bizzell, J., … Dichter, G. S. (2015). Neural mechanisms of emotion regulation in autism spectrum disorder. Journal of Autism and Developmental Disorders, 45(11), 3409–3423 doi: 10.1007/s10803-015-2359-z
41. Roy, A. K., Fudge, J. L., Kelly, C., Perry, J. S., Daniele, T., Carlisi, C., … Ernst, M. (2013). Intrinsic functional connectivity of amygdala-based networks in adolescent generalized anxiety disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 52(3), 290–299.e292. doi: 10.1016/j.jaac.2012.12.010
42. Rubinow, M. J., Mahajan, G., May, W., Overholser, J. C., Jurjus, G. J., Dieter, L., … Stockmeier, C. A. (2014). Basolateral amygdala volume and cell numbers in major depressive disorder: A postmortem stereological study. Brain Structure & Function. doi: 10.1007/s00429-014-0900-z. [Epub ahead of print]
43. Sah, P., Faber, E. S., Lopez De Armentia, M., & Power, J. (2003). The amygdaloid complex: Anatomy and physiology. Physiological Reviews, 83(3), 803–834.
44. Sahyoun, C. P., Belliveau, J. W., Soulieres, I., Schwartz, S., & Mody, M. (2010). Neuroimaging of the functional and structural networks underlying visuospatial vs. linguistic reasoning in high-functioning autism. Neuropsychologia, 48(1), 86–95. doi: 10.1016/j.neuropsychologia.2009.08.013
45. Schmitz, N., Rubia, K., van Amelsvoort, T., Daly, E., Smith, A., & Murphy, D. G. (2008). Neural correlates of reward in autism. The British Journal of Psychiatry, 192(1), 19–24.
46. Schumann, C. M., & Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. Journal of Neuroscience, 26(29), 7674–7679.
47. Scott-Van Zeeland, A. A., Dapretto, M., Ghahremani, D. G., Poldrack, R. A., & Bookheimer, S. Y. (2010). Reward processing in autism. Autism Research, 3(2), 53–67.
48. Shmueli, K., van Gelderen, P., de Zwart, J. A., Horovitz, S. G., Fukunaga, M., Jansma, J. M., & Duyn, J. H. (2007). Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal. Neuroimage, 38(2), 306–320.
49. Siegel, M., & Beaulieu, A. (2012). Psychotropic medications in children with autism spectrum disorders: A systematic review and synthesis for evidence-based practice. Journal of Autism and Developmental Disorders, 42(8), 1592–1605.
50. Sterling, L., Dawson, G., Estes, A., & Greenson, J. (2008). Characteristics associated with presence of depressive symptoms in adults with autism spectrum disorder. Journal of Autism and Developmental Disorders, 38(6), 1011–1018.
51. Venkataraman, A., Duncan, J. S., Yang, D. Y., & Pelphrey, K. A. (2015). An unbiased Bayesian approach to functional connectomics implicates social-communication networks in autism. NeuroImage Clinical, 8, 356–366. doi: 10.1016/j.nicl.2015.04.021
52. Vickerstaff, S., Heriot, S., Wong, M., Lopes, A., & Dossetor, D. (2007). Intellectual ability, self-perceived social competence, and depressive symptomatology in children with high-functioning autistic spectrum disorders. Journal of Autism and Developmental Disorders, 37(9), 1647–1664. doi: 10.1007/s10803-006-0292-x
53. Webb, S. J., Sparks, B. F., Friedman, S. D., Shaw, D. W., Giedd, J., Dawson, G., & Dager, S. R. (2009). Cerebellar vermal volumes and behavioral correlates in children with autism spectrum disorder. Psychiatry Research, 172(1), 61–67. doi: 10.1016/j.pscychresns.2008.06.001