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Journal of Autism and Developmental Disorders

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01-10-2014 | Original Paper

Emotion Potentiated Startle in Fragile X Syndrome

Auteurs: Elizabeth C. Ballinger, Lisa Cordeiro, Alyssa D. Chavez, Randi J. Hagerman, David Hessl

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 10/2014

Abstract

Social avoidance and anxiety are prevalent in fragile X syndrome (FXS) and are potentially mediated by the amygdala, a brain region critical for social behavior. Unfortunately, functional brain resonance imaging investigation of the amygdala in FXS is limited by the difficulties experienced by intellectually impaired and anxious participants. We investigated the relationship between social avoidance and emotion-potentiated startle, a probe of amygdala activation, in children and adolescents with FXS, developmental disability without FXS (DD), and typical development. Individuals with FXS or DD demonstrated significantly reduced potentiation to fearful faces than a typically developing control group (p < .05). However, among individuals with FXS, social avoidance correlated positively with fearful-face potentiation (p < .05). This suggests that general intellectual disability blunts amygdalar response, but differential amygdala responsiveness to social stimuli contributes to phenotypic variability among individuals with FXS.

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Adolphs, R. (2010). What does the amygdala contribute to social cognition? Annals of the New York Academy of Sciences, 1191(1), 42–61. doi:10.1111/j.1749-6632.2010.05445.x.PubMedCrossRefPubMedCentral

Aman, M. G., Singh, N. N., Stewart, A. W., & Field, C. J. (1985). The aberrant behavior checklist: A behavior rating scale for the assessment of treatment effects. American Journal of Mental Deficiency, 89(5), 485–491.PubMed

Amaral, D. G. (2002). The primate amygdala and the neurobiology of social behavior: Implications for understanding social anxiety. Biological Psychiatry, 51(1), 11–17.PubMedCrossRef

Angrilli, A., Mauri, A., Palomba, D., Flor, H., Birbaumer, N., Sartori, G., et al. (1996). Startle reflex and emotion modulation impairment after a right amygdala lesion. Brain, 119, 1991–2000.PubMedCrossRef

Baird, A. A., Gruber, S. A., Fein, D. A., Maas, L. C., Steingard, R. J., Renshaw, P. F., et al. (1999). Functional magnetic resonance imaging of facial affect recognition in children and adolescents. Journal of the American Academy of Child and Adolescent Psychiatry, 38(2), 195–199.PubMedCrossRef

Batty, M., & Taylor, M. J. (2006). The development of emotional face processing during childhood. Developmental Science, 9(2), 207–220. doi:10.1111/j.1467-7687.2006.00480.x.PubMedCrossRef

Birbaumer, N., Grodd, W., Diedrich, O., Klose, U., Erb, M., Lotze, M., et al. (1998). fMRI reveals amygdala activation to human faces in social phobics. NeuroReport, 9(6), 1223–1226.PubMedCrossRef

Brown, W. T., Jenkins, E. C., Cohen, I. L., Fisch, G. S., Wolf-Schein, E. G., Gross, A., et al. (1986). Fragile X and autism: A multicenter survey. American Journal of Medical Genetics, 23(1–2), 341–352.PubMedCrossRef

Buchanan, T. W., Tranel, D., & Adolphs, R. (2004). Anteromedial temporal lobe damage blocks startle modulation by fear and disgust. Behavioral Neuroscience, 118(2), 429–437. doi:10.1037/0735-7044.118.2.429.PubMedCrossRef

Buchanan, T. W., Tranel, D., & Adolphs, R. (2009). The human amygdala in social function. In P. J. Whalen & E. A. Phelps (Eds.), The human amygdala (pp. 289–318). New York: The Guilford Press.

Chudley, A. E., & Hagerman, R. J. (1987). Fragile X syndrome. The Journal of Pediatrics, 110(6), 821–831.PubMedCrossRef

Cohen, S., Masyn, K., Mastergeorge, A., & Hessl, D. (2013). Psychophysiological responses to emotional stimuli in children and adolescents with autism and fragile X syndrome. Journal of Clinical Child and Adolescent Psychology. doi:10.1080/15374416.2013.843462.PubMedCentral

Cordeiro, L., Ballinger, E., Hagerman, R. J., & Hessl, D. (2010). Clinical assessment of DSM-IV anxiety disorders in fragile X syndrome: prevalence and characterization. Journal of Neurodevelopmental Disorders. doi:10.1007/s11689-010-9067-y.PubMedPubMedCentral

Cuthbert, B. N., Bradley, M. M., & Lang, P. J. (1996). Probing picture perception: Activation and emotion. Psychophysiology, 33, 103–111.PubMedCrossRef

Davis, M. (1992). The role of the amygdala in fear and anxiety. Annual Review of Neuroscience, 15, 353–375.PubMedCrossRef

Davis, M., Falls, W. A., Campeau, S., & Kim, M. (1993). Fear-potentiated startle: A neural and pharmacological analysis. Behavioural Brain Research, 58, 175–198.PubMedCrossRef

Farzin, F., Rivera, S. M., & Hessl, D. (2009). Brief report: Visual processing of faces in individuals with fragile X syndrome: An eye tracking study. Journal of Autism and Developmental Disorders, 39(6), 946–952. doi:10.1007/s10803-009-0744-1.PubMedCrossRefPubMedCentral

Feng, Y., Absher, D., Eberhart, D. E., Brown, V., Malter, H. E., & Warren, S. T. (1997). FMRP associates with polyribosomes as an mRNP, and the I304 N mutation of severe fragile X syndrome abolishes this association. Molecular Cell, 1(1), 109–118.PubMedCrossRef

Frenkel, T. I., & Bar-Haim, Y. (2011). Neural activation during the processing of ambiguous fearful facial expressions: An ERP study in anxious and nonanxious individuals. Biological Psychology, 88(2–3), 188–195. doi:10.1016/j.biopsycho.2011.08.001.PubMedCrossRef

Freund, L. S., Reiss, A. L., & Abrams, M. T. (1993). Psychiatric disorders associated with fragile X in the young female. Pediatrics, 91, 321–329.PubMed

Funayama, E. S., Grillon, C., Davis, M., & Phelps, E. A. (2001). A double dissociation in the affective modulation of startle in humans: Effects of unilateral temporal lobectomy. Journal of Cognitive Neuroscience, 13(6), 721–729.PubMedCrossRef

Garber, K. B., Visootak, J., & Warren, S. T. (2008). Fragile X syndrome. European Journal of Human Genetics, 16, 666–672. doi:10.1038/ejhg.2008.61.

Gotham, K., Risi, S., Pickles, A., & Lord, C. (2007). The autism diagnostic observation schedule: Revised algorithms for improved diagnostic validity. Journal of Autism and Developmental Disorders, 37(4), 613–627. doi:10.1007/s10803-006-0280-1.PubMedCrossRef

Gothelf, D., Furfaro, J. A., Hoeft, F., Eckert, M. A., Hall, S. S., O’Hara, R., et al. (2008). Neuroanatomy of fragile X syndrome is associated with aberrant behavior and the fragile X mental retardation protein (FMRP). Annals of Neurology, 63(1), 40–51. doi:10.1002/ana.21243.PubMedCrossRefPubMedCentral

Hagan, C. C., Hoeft, F., Mackey, A., Mobbs, D., & Reiss, A. L. (2008). Aberrant neural function during emotion attribution in female subjects with fragile X syndrome. Journal of the American Academy of Child and Adolescent Psychiatry, 47(12), 1443–1454. doi:10.1097/CHI.0b013e3181886e92.PubMedCrossRef

Hagerman, R. J. (1987). Fragile X syndrome. Current problems in pediatrics, 626–674.

Hazlett, H. C., Poe, M. D., Lightbody, A. A., Gerig, G., Macfall, J. R., Ross, A. K., et al. (2009). Teasing apart the heterogeneity of autism: Same behavior, different brains in toddlers with fragile X syndrome and autism. Journal of Neurodevelopmental Disorders, 1(1), 81–90. doi:10.1007/s11689-009-9009-8.PubMedCrossRefPubMedCentral

Hessl, D., Glaser, B., Dyer-Friedman, J., & Reiss, A. L. (2006). Social behavior and cortisol reactivity in children with fragile X syndrome. Journal of Child Psychology and Psychiatry, 47(6), 602–610. doi:10.1111/j.1469-7610.2005.01556.x.PubMedCrossRef

Hessl, D., Rivera, S., Koldewyn, K., Cordeiro, L., Adams, J., Tassone, F., et al. (2007). Amygdala dysfunction in men with the fragile X premutation. Brain, 130(2), 404–416. doi:10.1093/brain/awl338.PubMedCrossRef

Hessl, D., Wang, J. M., Schneider, A., Koldewyn, K., Le, L., Iwahashi, C., et al. (2011). Decreased fragile X mental retardation protein expression underlies amygdala dysfunction in carriers of the fragile X permutation. Biological Psychiatry, 70(9), 859–865. doi:10.1016/j.biopsych.2011.05.033.PubMedCrossRefPubMedCentral

Hitchcock, J., & Davis, M. (1986). Lesions of the amygdala, but not of the cerebellum or red nucleus, block conditioned fear as measured with the potentiated startle paradigm. Behavioral Neuroscience, 100(1), 11–22.PubMedCrossRef

Hoeft, F., Walter, E., Lightbody, A. A., Hazlett, H. C., Chang, C., Piven, J., et al. (2011). Neuroanatomical differences in toddler boys with fragile X syndrome and idiopathic autism. Archives of General Psychiatry, 68(3), 295–305. doi:10.1001/archgenpsychiatry.2010.153.PubMedCrossRef

Kau, A. S. M., Tierney, E., Bukelis, I., Stump, M. H., Kates, W. R., Trescher, W. H., et al. (2004). Social behavior profile in young males with fragile X syndrome: Characteristics and specificity. American Journal of Medical Genetics Part A, 126A(1), 9–17. doi:10.1002/ajmg.a.20218.PubMedCrossRef

Kim, S. Y., Burris, J., Bassal, F., Koldewyn, K., Chattarji, S., Tassone, F., et al. (2012). Fear-specific amygdala function in children and adolescents on the fragile X spectrum: A dosage response of the FMR1 gene. Cerebral Cortex. doi:10.1093/cercor/bhs341.

Koch, M., Schmid, A., & Schnitzler, H.-U. (1996). Pleasure-attenuation of startle is disrupted by lesions of the nucleus accumbens. NeuroReport, 7, 1442–1446.PubMedCrossRef

Koch, M., & Schnitzler, H.-U. (1997). The acoustic startle response in rats-circuits mediating evocation, inhibition and potentiation. Behavioral Brain Research, 89, 35–49.CrossRef

Lachiewicz, A. M. (1992). Abnormal behaviors of young girls with fragile X syndrome. American Journal of Medical Genetics, 43, 72–77.PubMedCrossRef

Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (1999). Autism diagnostic observation schedule-WPS (ADOS-WPS). Los Angeles: Western Psychological Services.

Lord, C., Rutter, M., Goode, S., Heemsbergen, J., Jordan, H., Mawhood, L., et al. (1989). Autism diagnostic observation schedule: A standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19(2), 185–212.PubMedCrossRef

Mazzocco, M. M. M., Freund, L. S., & Baumgardner, T. L. (1995). Neuropsychological and psychosoical effects of the fmr-1 full mutation: Case report of monozygotic twins discordant for the fragile X syndrome. Neuropsychology, 9(4), 470–480.CrossRef

Olmos-Serrano, J. L., Paluszkiewicz, S. M., Martin, B. S., Kaufmann, W. E., Corbin, J. G., & Huntsman, M. M. (2010). Defective GABAergic neurotransmission and pharmacological rescue of neuronal hyperexcitability in the amygdala in a mouse model of fragile X syndrome. Journal of Neuroscience, 30(29), 9929–9938. doi:10.1523/jneurosci.1714-10.2010.PubMedCrossRefPubMedCentral

Paradee, W., Melikian, H. E., Rasmussen, D. L., Kenneson, A., Conn, P. J., & Warren, S. T. (1999). Fragile X mouse: Strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience, 94(1), 185–192.PubMedCrossRef

Phan, K. L., Fitzgerald, D. A., Nathan, P. J., & Tancer, M. E. (2006). Association between amygdala hyperactivity to harsh faces and severity of social anxiety in generalized social phobia. Biological Psychiatry, 59(5), 424–429. doi:10.1016/j.biopsych.2005.08.012.PubMedCrossRef

Pissiota, A., Frans, O., Michelgard, A., Appel, L., Langstrom, B., Flaten, M. A., et al. (2003). Amygdala and anterior cingulate cortex activation during affective startle modulation: A PET study of fear. European Journal of Neuroscience, 18, 1325–1331.PubMedCrossRef

Reiss, A. L., Abrams, M. T., Greenlaw, R., Freund, L. S., & Denckla, M. B. (1995). Neurodevelopmental effects of the FMR-1 full mutation in humans. Nature Medicine, 1(2), 159–167.PubMedCrossRef

Reynolds, C. R., & Kamphaus, R. W. (2004). Behavior assessment system for children, Second Edition. In I. American Guidance Service (Ed.). Circle Pines, MN.

Roberts, J., Weisenfeld, L., Hatton, D., Heath, M., & Kaufmann, W. (2007). Social approach and autistic behavior in children with fragile X syndrome. Journal of Autism and Developmental Disorders, 37(9), 1748–1760. doi:10.1007/s10803-006-0305-9.PubMedCrossRef

Rosen, J. B., & Davis, M. (1988). Enhancement of acoustic startle by electrical stimulation of the amygdala. Behavioral Neuroscience, 102(2), 195–202.PubMedCrossRef

Rousseau, F., Heitz, D., Biancalana, V., Blumenfeld, S., Kretz, C., Boue, J., et al. (1991). Direct diagnosis by DNA analysis of the fragile X syndrome of mental retardation. The New England Journal of Medicine, 325(24), 1673–1681.PubMedCrossRef

Saluto, A., Brussino, A., Tassone, F., Arduino, C., Cagnoli, C., Pappi, P., et al. (2005). An enhanced polymerase chain reaction assay to detect pre- and full mutation alleles of the fragile X mental retardation 1 gene. The Journal of Molecular Diagnostics, 7(5), 605–612.PubMedCrossRefPubMedCentral

Sansone, S. M., Widaman, K. F., Hall, S. S., Reiss, A. L., Lightbody, A., Kaufmann, W. E., et al. (2012). Psychometric study of the aberrant behavior checklist in fragile X syndrome and implications for targeted treatment. Journal of Autism and Developmental Disorders, 42(7), 1377–1392. doi:10.1007/s10803-011-1370-2.PubMedCrossRefPubMedCentral

Shin, L. M., Rauch, S. L., Pitman, R. K., & Whalen, P. J. (2009). The human amygdala in anxiety disorders. In P. J. Whalen & E. A. Phelps (Eds.), The human amygdala (pp. 321–343). New York: The Guilford Press.

Suvrathan, A., & Chattarji, S. (2011). Fragile X syndrome and the amygdala. Current Opinion in Neurobiology, 21(3), 509–515. doi:10.1016/j.conb.2011.04.005.PubMedCrossRef

Suvrathan, A., Hoeffer, C. A., Wong, H., Klann, E., & Chattarji, S. (2010). Characterization and reversal of synaptic defects in the amygdala in a mouse model of fragile X syndrome. Proceedings of the National Academy of Sciences, 107(25), 11591–11596. doi:10.1073/pnas.1002262107.CrossRef

Tassone, F., Iwahashi, C., & Hagerman, P. J. (2004). FMR1 RNA within the intranuclear inclusions of fragile X-associated tremor/ataxia syndrome (FXTAS). RNA Biology, 1(2), 103–105.PubMedCrossRef

Thomas, K. M., Drevets, W. C., Dahl, R. E., Ryan, N. D., Birmaher, B., Eccard, C. H., et al. (2001). Amygdala response to fearful faces in anxious and depressed children. Archives of General Psychiatry, 58(11), 1057–1063.PubMedCrossRef

Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., et al. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168(3), 242–249. doi:10.1016/j.psychres.2008.05.006.PubMedCrossRefPubMedCentral

Verkerk, A. J. M. H., Pieretti, M., Sutcliffe, J. S., Fu, Y.-H., Kuhl, D. P. A., Pizzuti, A., et al. (1991). Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell, 65(5), 905–914.PubMedCrossRef

Vrana, S. R., Spence, E. L., & Lang, P. J. (1988). The startle probe response: A new measure of emotion. Journal of Abnormal Psychology, 97(4), 487–491.PubMedCrossRef

Watson, C., Hoeft, F., Garrett, A. S., Hall, S. S., & Reiss, A. L. (2008). Aberrant brain activation during gaze processing in boys with fragile X syndrome. Archives of General Psychiatry, 65(11), 1315–1323.PubMedCrossRef

Whalen, P. J., Davis, F. C., Oler, J. A., Kim, H., Kim, M. J., & Neta, M. (2009). Human amygdala responses to facial expressions of emotion. In P. J. Whalen & E. A. Phelps (Eds.), The human amygdala (pp. 265–288). New York: The Guilford Press.

Whalen, P. J., Shin, L. M., McInerney, S. C., Fischer, H., Wright, C. I., & Rauch, S. L. (2001). A functional MRI study of human amygdala responses to facial expressions of fear versus anger. Emotion, 1(1), 70–83.PubMedCrossRef

Wolfensberger, S. P. A., Veltman, D. J., Hoogendijk, W. J. G., Boomsma, D. I., & de Geus, E. J. C. (2008). Amygdala responses to emotional faces in twins discordant or concordant for the risk for anxiety and depression. NeuroImage, 41(2), 544–552. doi:10.1016/j.neuroimage.2008.01.053.PubMedCrossRef

Yuhas, J., Cordeiro, L., Tassone, F., Ballinger, E., Schneider, A., Long, J. M., et al. (2011). Brief report: Sensorimotor gating in idiopathic autism and autism associated with fragile X syndrome. Journal of Autism and Developmental Disorders, 41(2), 248–253. doi:10.1007/s10803-010-1040-9.PubMedCrossRefPubMedCentral

Zhao, M. G. (2005). Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. Journal of Neuroscience, 25(32), 7385–7392. doi:10.1523/jneurosci.1520-05.2005.PubMedCrossRef

Titel: Emotion Potentiated Startle in Fragile X Syndrome
Auteurs: Elizabeth C. Ballinger
Lisa Cordeiro
Alyssa D. Chavez
Randi J. Hagerman
David Hessl
Publicatiedatum: 01-10-2014
Uitgeverij: Springer US
Gepubliceerd in: Journal of Autism and Developmental Disorders / Uitgave 10/2014
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI: https://doi.org/10.1007/s10803-014-2125-7

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