Overactive Pattern Separation Memory Associated with Negative Emotionality in Adults Diagnosed with Autism Spectrum Disorder

Journal of Autism and Developmental Disorders

Volumn 45, Issue 11, 2015, Pages 3458-3467

  South, M ^a   Stephenson, K G ^a   Nielson, C A ^a   Maisel, M ^a   Top, D N ^a   Kirwan, C B ^a  

^a BRIGHAM YOUNG UNIVERSITY   (United States)

Author keywords

Anxiety; Autism spectrum disorder; Emotion regulation; Hippocampus; Memory; Pattern separation

Indexed keywords

ACHIEVEMENT; ADOLESCENT; ADULT; AMNESIA; ARTICLE; AUTISM; BRAIN FUNCTION; CLINICAL ARTICLE; COMPULSION; CONTROLLED STUDY; EMOTIONALITY; FEMALE; HIPPOCAMPUS; HUMAN; HYPERACTIVITY; IMPULSIVENESS; MALE; MEMORY; MENTAL TASK; MOTIVATION; PRIORITY JOURNAL; ANXIETY; CASE CONTROL STUDY; COMPLICATION; EMOTION; MEMORY DISORDER; PATTERN RECOGNITION; PSYCHOLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; ANXIETY; AUTISM SPECTRUM DISORDER; CASE-CONTROL STUDIES; EMOTIONS; FEMALE; HUMANS; MALE; MEMORY DISORDERS; MOTIVATION; PATTERN RECOGNITION, VISUAL; YOUNG ADULT;

EID: 84944511688     PISSN: 01623257     EISSN: 15733432     Source Type: Journal    
DOI: 10.1007/s10803-015-2547-x     Document Type: Article

References (65)

1. Aggleton, J. P., & Brown, M. W. (2006). Interleaving brain systems for episodic and recognition memory. Trends in Cognitive Sciences,10(10), 455–463. doi:10.1016/j.tics.2006.08.003.
2. Aimone, J. B., Wiles, J., & Gage, F. H. (2006). Potential role for adult neurogenesis in the encoding of time in new memories. Nature Neuroscience,9(6), 723–727. doi:10.1038/nn1707.
3. Andersen, P. N., Skogli, E. W., Hovik, K. T., Geurts, H., Egeland, J., & Øie, M. (2014). Working memory arrest in children with high-functioning autism compared to children with attention-deficit/hyperactivity disorder: Results from a 2-year longitudinal study. Autism, 19, 443–450.
4. Bakker, A., Kirwan, C. B., Miller, M., & Stark, C. E. L. (2008). Pattern separation in the human hippocampal CA3 and dentate gyrus. Science,319(5870), 1640–1642. doi:10.1126/science.1152882.
5. Barbalat, G., Leboyer, M., & Zalla, T. (2014). A specific impairment in cognitive control in individuals with high-functioning autism. Journal of Psychiatric Research,58, 26–35.
6. Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.
7. Ben Shalom, D. (2003). Memory in autism: Review and synthesis. Cortex; a Journal Devoted to the Study of the Nervous System and Behavior,39(4–5), 1129–1138.
8. Ben Shalom, D. (2009). The medial prefrontal cortex and integration in autism. The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry,15(6), 589–598. doi:10.1177/1073858409336371.
9. Bieling, P. J., Antony, M. M., & Swinson, R. P. (1998). The state-trait anxiety inventory, trait version: Structure and content re-examined. Behaviour Research and Therapy,36(7–8), 777–788. doi:10.1016/S0005-7967(98)00023-0.
10. Bird, G., & Cook, R. (2013). Mixed emotions: The contribution of alexithymia to the emotional symptoms of autism. Translational Psychiatry,3, e285–e285. doi:10.1038/tp.2013.61.
11. Bird, G., Silani, G., Brindley, R., White, S., Frith, U., & Singer, T. (2010). Empathic brain responses in insula are modulated by levels of alexithymia but not autism. Brain: A Journal of Neurology,133(Pt 5), 1515–1525. doi:10.1093/brain/awq060.
12. Biro, S., Alink, L. R. A., van IJzendoorn, M. H., & Bakermans-Kranenburg, M. J. (2014). Infants’ monitoring of social interactions: The effect of emotional cues. Emotion,14(2), 263–271. doi:10.1037/a0035589. (Washington, DC).
13. Boucher, J., Mayes, A., & Bigham, S. (2012). Memory in autistic spectrum disorder. Psychological Bulletin,138(3), 458–496. doi:10.1037/a0026869.
14. Bowler, D. M., Gaigg, S. B., & Gardiner, J. M. (2014). Binding of multiple features in memory by high-functioning adults with autism spectrum disorder. Journal of Autism and Developmental Disorders,44(9), 2355–2362. doi:10.1007/s10803-014-2105-y.
15. Caci, H., Baylé, F. J., Dossios, C., Robert, P., & Boyer, P. (2003). The Spielberger trait anxiety inventory measures more than anxiety. European Psychiatry,18(8), 394–400. doi:10.1016/j.eurpsy.2003.05.003.
16. Carver, C. S., & White, T. S. (1994). Behavioral inhibition, behavioral activation, and affective responses to impending reward and punishment: The BIS/BAS scales. Journal of Personality and Social Psychology,67, 319–333.
17. Childhood Autism Research Group Online—North East. (n.d.). Anxiety Scale for Children—ASD. Retrieved from http://research.ncl.ac.uk/cargo-ne/measures.html.
18. Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D., Fragniere, A., Tyers, P., & Bussey, T. J. (2009). A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation. Science,325(5937), 210–213. doi:10.1126/science.1173215.
19. Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., et al. (2003). Validation of a brief quantitative measure of autistic traits: Comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433. doi:10.1023/A:1025014929212.
20. Cook, R., Brewer, R., Shah, P., & Bird, G. (2013). Alexithymia, not autism, predicts poor recognition of emotional facial expressions. Psychological Science,24(5), 723–732. doi:10.1177/0956797612463582.
21. Cowen, P., & Sherwood, A. C. (2013). The role of serotonin in cognitive function: Evidence from recent studies and implications for understanding depression. Journal of Psychopharmacology,27(7), 575–583. doi:10.1177/0269881113482531. (Oxford, England).
22. 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.
23. Doxey, C. R., & Kirwan, C. B. (2015). Structural and functional correlates of behavioral pattern separation in the hippocampus and medial temporal lobe. Hippocampus,25(4), 524–533. doi:10.1002/hipo.22389.
24. Elsabbagh, M., Fernandes, J., Jane Webb, S., Dawson, G., Charman, T., & Johnson, M. H. (2013). Disengagement of visual attention in infancy is associated with emerging autism in toddlerhood. Biological Psychiatry,74(3), 189–194. doi:10.1016/j.biopsych.2012.11.030.
25. Etherton, M., Földy, C., Sharma, M., Tabuchi, K., Liu, X., Shamloo, M., & Südhof, T. C. (2011). Autism-linked neuroligin-3 R451C mutation differentially alters hippocampal and cortical synaptic function. Proceedings of the National Academy of Sciences,108(33), 13764–13769. doi:10.1073/pnas.1111093108.
26. Fujii, T., Saito, D. N., Yanaka, H. T., Kosaka, H., & Okazawa, H. (2014). Depressive mood modulates the anterior lateral CA1 and DG/CA3 during a pattern separation task in cognitively intact individuals: A functional MRI study. Hippocampus,24(2), 214–224. doi:10.1002/hipo.22216.
27. Gaigg, S. B., & Bowler, D. M. (2008). Free recall and forgetting of emotionally arousing words in autism spectrum disorder. Neuropsychologia,46(9), 2336–2343. doi:10.1016/j.neuropsychologia.2008.03.008.
28. Gaigg, S. B., Bowler, D. M., & Gardiner, J. M. (2014). Episodic but not semantic order memory difficulties in autism spectrum disorder: Evidence from the Historical Figures Task. Memory,22(6), 669–678. doi:10.1080/09658211.2013.811256. (Hove, England).
29. Gilbert, P. E., Kesner, R. P., & DeCoteau, W. E. (1998). Memory for spatial location: Role of the hippocampus in mediating spatial pattern separation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience,18(2), 804–810.
30. Goh, S., & Peterson, B. S. (2012). Imaging evidence for disturbances in multiple learning and memory systems in persons with autism spectrum disorders. Developmental Medicine and Child Neurology,54(3), 208–213. doi:10.1111/j.1469-8749.2011.04153.x.
31. Gomez, R., & Corr, P. J. (2010). Attention-deficit/hyperactivity disorder symptoms: Associations with Gray’s and Tellegen’s models of personality. Personality and Individual Differences,49(8), 902–906. doi:10.1016/j.paid.2010.06.033.
32. Heym, N., Kantini, E., Checkley, H. L. R., & Cassaday, H. J. (2015). Gray’s revised reinforcement sensitivity theory in relation to attention-deficit/hyperactivity and tourette-like behaviors in the general population. Personality and Individual Differences,78, 24–28. doi:10.1016/j.paid.2015.01.012.
33. Hoshino, T., & Tanno, Y. (2014). Trait anxiety and impaired control of reflective attention in working memory. Cognition and Emotion. doi:10.1080/02699931.2014.993597.
34. Huffman, D. J., & Stark, C. E. L. (2014). Multivariate pattern analysis of the human medial temporal lobe revealed representationally categorical cortex and representationally agnostic hippocampus. Hippocampus,24(11), 1394–1403. doi:10.1002/hipo.22321.
35. Jones, W., & Klin, A. (2013). Attention to eyes is present but in decline in 2-6-month-old infants later diagnosed with autism. Nature,504(7480), 427–431. doi:10.1038/nature12715.
36. Kheirbek, M. A., Klemenhagen, K. C., Sahay, A., & Hen, R. (2012). Neurogenesis and generalization: A new approach to stratify and treat anxiety disorders. Nature Neuroscience,15(12), 1613–1620. doi:10.1038/nn.3262.
37. Koolen, S., Vissers, C. T. W. M., Egger, J. I. M., & Verhoeven, L. (2014). How stimulus and task complexity affect monitoring in high-functioning adults with autism spectrum disorder. Journal of Autism and Developmental Disorders,44(10), 2499–2513. doi:10.1007/s10803-014-2119-5.
38. Larson, M. J., South, M., Clayson, P. E., & Clawson, A. (2012). Cognitive control and conflict adaptation in youth with high-functioning autism. Journal of Child Psychology and Psychiatry, and Allied Disciplines,53(4), 440–448. doi:10.1111/j.1469-7610.2011.02498.x.
39. Leary, M. R. (1983). A brief version of the Fear of Negative Evaluation Scale. Personality and Social Psychology Bulletin,9, 371–376.
40. Leutgeb, J. K., Leutgeb, S., Moser, M.-B., & Moser, E. I. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science,315(5814), 961–966. doi:10.1126/science.1135801.
41. Lissek, S., Kaczkurkin, A. N., Rabin, S., Geraci, M., Pine, D. S., & Grillon, C. (2014). Generalized anxiety disorder is associated with overgeneralization of classically conditioned fear. Biological Psychiatry,75(11), 909–915. doi:10.1016/j.biopsych.2013.07.025.
42. Maister, L., Simons, J. S., & Plaisted-Grant, K. (2013). Executive functions are employed to process episodic and relational memories in children with autism spectrum disorders. Neuropsychology,27(6), 615–627. doi:10.1037/a0034492.
43. Mathew, I., Gardin, T. M., Tandon, N., Eack, S., Francis, A. N., Seidman, L. J., & Keshavan, M. S. (2014). Medial temporal lobe structures and hippocampal subfields in psychotic disorders: Findings from the Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP) study. JAMA Psychiatry,71(7), 769–777. doi:10.1001/jamapsychiatry.2014.453.
44. Matson, J. L., Rieske, R. D., & Williams, L. W. (2013). The relationship between autism spectrum disorders and attention-deficit/hyperactivity disorder: An overview. Research in Developmental Disabilities,34(9), 2475–2484. doi:10.1016/j.ridd.2013.05.021.
45. Mazefsky, C. A., Herrington, J., Siegel, M., Scarpa, A., Maddox, B. B., Scahill, L., & White, S. W. (2013). The role of emotion regulation in autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry,52(7), 679–688. doi:10.1016/j.jaac.2013.05.006.
46. McDonald, J. H. (2014). Handbook of biological statistics (3rd ed.). Baltimore, MD: Sparky House Publishing.
47. Meyer, T. J., Miller, M. L., Metzger, R. L., & Borkovec, T. D. (1990). Development and validation of the Penn State Worry Questionnaire. Behaviour Research and Therapy,28(6), 487–495.
48. Minshew, N. J., & Goldstein, G. (2001). The pattern of intact and impaired memory functions in autism. Journal of Child Psychology and Psychiatry and Allied Disciplines,42(8), 1095–1101.
49. Minshew, N. J., Goldstein, G., & Siegel, D. J. (1997). Neuropsychologic functioning in autism: Profile of a complex information processing disorder. Journal of the International Neuropsychological Society: JINS,3(4), 303–316.
50. Opris, I., & Casanova, M. F. (2014). Prefrontal cortical minicolumn: From executive control to disrupted cognitive processing. Brain: A Journal Of Neurology,137(Pt 7), 1863–1875. doi:10.1093/brain/awt359.
51. Rommelse, N. N. J., Geurts, H. M., Franke, B., Buitelaar, J. K., & Hartman, C. A. (2011). A review on cognitive and brain endophenotypes that may be common in autism spectrum disorder and attention-deficit/hyperactivity disorder and facilitate the search for pleiotropic genes. Neuroscience and Biobehavioral Reviews,35(6), 1363–1396. doi:10.1016/j.neubiorev.2011.02.015.
52. Schacter, D. L., Norman, K. A., & Koutstaal, W. (1998). The cognitive neuroscience of constructive memory. Annual Review of Psychology,49(1), 289–318. doi:10.1146/annurev.psych.49.1.289.
53. Schuh, J. M., & Eigsti, I.-M. (2012). Working memory, language skills, and autism symptomatology. Behavioral Sciences,2(4), 207–218. doi:10.3390/bs2040207. (Basel, Switzerland).
54. Sgadò, P., Genovesi, S., Kalinovsky, A., Zunino, G., Macchi, F., Allegra, M., & Bozzi, Y. (2013). Loss of GABAergic neurons in the hippocampus and cerebral cortex of Engrailed-2 null mutant mice: Implications for autism spectrum disorders. Experimental Neurology,247, 496–505. doi:10.1016/j.expneurol.2013.01.021.
55. Shelton, D. J., & Kirwan, C. B. (2013). A possible negative influence of depression on the ability to overcome memory interference. Behavioural Brain Research,256, 20–26. doi:10.1016/j.bbr.2013.08.016.
56. Solomon, M., Yoon, J. H., Ragland, J. D., Niendam, T. A., Lesh, T. A., Fairbrother, W., & Carter, C. S. (2014). The development of the neural substrates of cognitive control in adolescents with autism spectrum disorders. Biological Psychiatry,76(5), 412–421. doi:10.1016/j.biopsych.2013.08.036.
57. Spielberger, C. D., Gorsuch, R. L., Lushene, R. E., Vagg, P. R., & Jacobs, G. A. (1983). Manual for the state-trait anxiety inventory. Consulting Psychologists Press. Retrieved from http://ubir.buffalo.edu/xmlui/handle/10477/2895.
58. Stephenson, D. T., O’Neill, S. M., Narayan, S., Tiwari, A., Arnold, E., Samaroo, H. D., & Morton, D. (2011). Histopathologic characterization of the BTBR mouse model of autistic-like behavior reveals selective changes in neurodevelopmental proteins and adult hippocampal neurogenesis. Molecular Autism,2(1), 7. doi:10.1186/2040-2392-2-7.
59. Stigler, K. A., McDonald, B. C., Anand, A., Saykin, A. J., & McDougle, C. J. (2011). Structural and functional magnetic resonance imaging of autism spectrum disorders. Brain Research,1380, 146–161. doi:10.1016/j.brainres.2010.11.076.
60. Tukey, J. W. (1977). Exploratory data analysis. Reading: Addison-Wesley.
61. Webb, S. (2008). Impairments in social memory in autism? Evidence from behavior and neuroimaging. In J. Boucher & D. Bowler (Eds.), Memory in autism: Theories and evidence (pp. 188–209). Cambridge: Cambridge University Press.
62. Wegiel, J., Kuchna, I., Nowicki, K., Imaki, H., Wegiel, J., Marchi, E., & Wisniewski, T. (2010). The neuropathology of autism: Defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathologica,119(6), 755–770. doi:10.1007/s00401-010-0655-4.
63. White, S. W., Mazefsky, C. A., Dichter, G. S., Chiu, P. H., Richey, J. A., & Ollendick, T. H. (2014). Social-cognitive, physiological, and neural mechanisms underlying emotion regulation impairments: Understanding anxiety in autism spectrum disorder. International Journal of Developmental Neuroscience: The Official Journal of the International Society for Developmental Neuroscience,39, 22–36. doi:10.1016/j.ijdevneu.2014.05.012.
64. Wojcik, D. Z., Moulin, C. J. A., & Souchay, C. (2013). Metamemory in children with autism: Exploring “feeling-of-knowing” in episodic and semantic memory. Neuropsychology,27(1), 19–27. doi:10.1037/a0030526.
65. Yuen, E. Y., Wei, J., Liu, W., Zhong, P., Li, X., & Yan, Z. (2012). Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron,73(5), 962–977. doi:10.1016/j.neuron.2011.12.033.