Overactive Pattern Separation Memory Associated with Negative Emotionality in Adults Diagnosed with Autism Spectrum Disorder
- 545 Downloads
- 4 Citations
Abstract
Bowler et al. (Journal of Autism and Developmental Disorders 44(9):2355–2362. doi:10.1007/s10803-014-2105-y, 2014) have suggested that a specific memory impairment in autism spectrum disorders (ASD) arises from hippocampal failure to consolidate multiple related pieces of information. Twenty-four adults diagnosed with ASD and matched healthy controls completed a pattern separation memory task that is known to critically depend on hippocampal involvement. They additionally completed questionnaires regarding anxiety, depression, and behavioral motivation. Specific deficits in pattern separation were significantly correlated with negative emotionality; the best predictor of memory deficit was from a measure of achievement motivation that has also been associated with hyperactivity and impulsivity. In the context of impaired emotion regulation in ASD, there is a need for integrated cognitive, affective, and neural systems approaches to build targeted interventions.
Keywords
Autism spectrum disorder Memory Pattern separation Hippocampus Emotion regulation AnxietyNotes
Acknowledgments
We thank the participants for their willingness to participate in this research. We would like to thank Suzanne Grimshaw, Suzette Bartlett, and Doug Gale from Scenic View Academy for their assistance in recruiting participants; and Chris Doxey for assistance in how to run the task. This research was supported by Brigham Young University Mentoring funds including an ORCA Grant to C.N. and a MEG grant to C.B.K. and M.S.
Author Contributions
MS and CBK conceived of the study and participated in its design. CAN, MM, DNT, and KGS coordinated the study and performed the measurement. MS and KGS performed the statistical analyses and drafted the manuscript. All authors read and approved the final manuscript.
References
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- Beck, A. T., Steer, R. A., & Brown, G. K. (1996). Manual for the Beck Depression Inventory-II. San Antonio, TX: Psychological Corporation.Google Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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).CrossRefPubMedGoogle Scholar
- Boucher, J., Mayes, A., & Bigham, S. (2012). Memory in autistic spectrum disorder. Psychological Bulletin, 138(3), 458–496. doi: 10.1037/a0026869.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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).CrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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).CrossRefPubMedGoogle Scholar
- 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.Google Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.PubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- Leary, M. R. (1983). A brief version of the Fear of Negative Evaluation Scale. Personality and Social Psychology Bulletin, 9, 371–376.CrossRefGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- McDonald, J. H. (2014). Handbook of biological statistics (3rd ed.). Baltimore, MD: Sparky House Publishing.Google Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.PubMedGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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).PubMedCentralCrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- Tukey, J. W. (1977). Exploratory data analysis. Reading: Addison-Wesley.Google Scholar
- 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.CrossRefGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar
- 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.CrossRefGoogle Scholar
- 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.CrossRefPubMedGoogle Scholar
- 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.PubMedCentralCrossRefPubMedGoogle Scholar