Abstract
This study examines declarative memory retrieval in ASD depending on the availability and access to stored conceptual knowledge. Fifteen autistic participants and a matched control group of 18 typically-developed (TD) volunteers completed a Remember-Know paradigm manipulated by encoding-type (categorical, perceptual) and item-typicality (high-typical, low-typical). The autistic group showed worse and slower recognition and less recollection but equivalent familiarity-based memories compared to TDs. Notably, low-typical items did not improve their memories as they did for TDs, likely due to difficulties in matching low-fit information to the stored schema. Results suggest that memory decline in ASD may derive from the episodic system and its dynamics with the semantic system. These findings may inform interventional strategies for enhancing learning abilities in ASD.
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Notes
Typicality refers to a semantic organization process reflecting how good an item is in representing its category. Typical items share the prototypical features of their categories (e.g., an apple in the Fruit category); atypical items present less fit with their categorical prototype (e.g., a dolphin is atypical in Mammals) (see Medin et al., 2007; Murphy & Medin, 1985; Rosch, 1978).
The items were selected from normative studies of concepts and their related pictures conducted with Portuguese samples (Santi et al., 2015; Souza et al, 2021b). The typicality ratings were obtained for items (displayed in a picture) representing specific basic concepts (e.g., penguin as less typical and cardinal as typical) within a specific superordinate category (e.g., birds).
References
Alves, M., & Raposo, A. (2015). Is it a bird? Differential effects of concept typicality on semantic memory and episodic recollection. Revista Portuguesa de Psicologia, 44, 65–79. https://doi.org/10.1126/science.277.5324.376
American Psychiatric Association (1994). Diagnostic and statistical manual of mental health disorders (4th edn.). Author.
Barr, D. J., Levy, R., Scheepers, C., & Tily, H. J. (2013). Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of Memory and Language, 68(3), 255–278. https://doi.org/10.1016/j.jml.2012.11.001
Bennetto, L., Pennington, B. F., & Rogers, S. J. (1996). Intact and impaired memory functions in autism. Child Development, 67(4), 1816–1835.
Bonasia, K., Sekeres, M. J., Gilboa, A., Grady, C. L., Winocur, G., & Moscovitch, M. (2018). Prior knowledge modulates the neural substrates of encoding and retrieving naturalistic events at short and long delays. Neurobiology of Learning and Memory, 153, 26–39. https://doi.org/10.1016/j.nlm.2018.02.017
Boucher, J., & Bowler, D. (2008). Memory in autism: Theory and evidence. Cambridge University Press.
Boucher, J., Mayes, A., & Bigham, S. (2012). Memory in autistic spectrum disorder. Psychological Bulletin, 138, 458–496. https://doi.org/10.1037/a0026869
Bowler, D. M., Gardiner, J. M., & Grice, S. J. (2000). Episodic memory and remembering in adults with Asperger Syndrome. Journal of Autism and Developmental Disorders, 30, 295–304. https://doi.org/10.1023/A:1005575216176
Bowler, D., Gaigg, S., & Lind, S. (2011). Memory in autism: Binding, self, and brain. In: I. Roth & P. Rezaie (Eds.), Researching the autism spectrum: Contemporary perspectives (pp. 316–346P. Cambridge University Press. https://doi.org/10.1017/cbo9780511973918.013
Carmo, J. C., Duarte, E., Pinho, S., Filipe, C. N., & Marques, J. F. (2016). Preserved proactive interference in autism spectrum disorder. Journal of Autism and Developmental Disorders, 46, 53–63. https://doi.org/10.1007/s10803-015-2540-4
Carmo, J. C., Souza, C., Gonçalves, F., Pinho, S., Filipe, C. N., & Lachmann, T. (2017). Effects of categorical representation on visuospatial working memory in autism spectrum disorder. Journal of Clinical and Experimental Neuropsychology, 39, 131–141. https://doi.org/10.1080/13803395.2016.1207754
Cooper, R. A., & Simons, J. S. (2018). Exploring the neurocognitive basis of episodic recollection in autism. Psychonomic Bulletin & Review, 26, 163–181. https://doi.org/10.3758/s13423-018-1504-z
Carmo, J. C., Martins, F., Pinho, S., Barahona-Correa, B., Ventura, P., & Filipe, C. N. (2020). We see the orange not the lemon: Typicality effects in ultra-rapid categorization in adults with and without spectrum disorder. Journal of Neuropsychology, 14, 154–164. https://doi.org/10.1111/jnp.12176
de Mendonça, A., Cardoso, S., Maroco, J., Guerreiro, M., & Carmo, J. C. (2020). The update of semantic memories in amnestic mild cognitive impairment. Journal of Neuropsychology, 15, 27–40. https://doi.org/10.1111/jnp.12217
Dudai, Y., Karni, A., & Born, J. (2015). The consolidation and transformation of memory. Neuron, 88, 20–32. https://doi.org/10.1016/j.neuron.2015.09.004
Frazier, T. W., Georgiades, S., Bishop, S. L., & Hardan, A. Y. (2014). Behavioral and cognitive characteristics of females and males with autism in the Simons simplex collection. Journal of the American Academy of Child & Adolescent Psychiatry, 53(3), 329-340.e3. https://doi.org/10.1016/j.jaac.2013.12.004
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 (Hove, England), 22(6), 669–678. https://doi.org/10.1080/09658211.2013.811256
Gaigg, S. B., Bowler, D. M., Ecker, C., Calvo-Merino, B., & Murphy, D. G. (2015). Episodic recollection difficulties in ASD result from atypical relational encoding: Behavioral and neural evidence. Autism Research, 8, 317–327. https://doi.org/10.1002/aur.1448
Gardiner, J. M. (1988). Functional aspects of recollective experience. Memory & Cognition, 16, 309–313. https://doi.org/10.3758/bf03197041
Gardiner, J. M., Java, R. I. Forgetting in recognition memory with and without recollective experience. Memory & Cognition, 19, 617–623 (1991). https://doi.org/10.3758/BF03197157
Gardiner, J. M., Ramponi, C., & Richardson-Klavehn, A. (1998). Experiences of remembering, knowing, and guessing. Consciousness and Cognition, 7, 1–26. https://doi.org/10.1006/ccog.1997.0321
Gastgeb, H. Z., & Strauss, M. S. (2012). Categorization in ASD: The role of typicality and development. Perspectives on Language Learning and Education, 19, 66–74. https://doi.org/10.1044/lle19.2.66
Gastgeb, H. Z., Strauss, M. S., & Minshew, N. J. (2006). Do individuals with autism process categories differently? The effect of typicality and development. Child Development, 77, 1717–1729. https://doi.org/10.1111/j.1467-8624.2006.00969.x
Giarelli, E., Wiggins, L. D., Rice, C. E., Levy, S. E., Kirby, R. S., Pinto-Martin, J., & Mandell, D. (2010). Sex differences in the evaluation and diagnosis of autism spectrum disorders among children. Disability and Health Journal, 3(2), 107–116. https://doi.org/10.1016/j.dhjo.2009.07.001
Griffin, J. W., Bauer, R., & Gavett, B. E. (2021). The episodic memory profile in autism spectrum disorder: A Bayesian meta-analysis. Neuropsychology Review. https://doi.org/10.1007/s11065-021-09493-5
Harand, C., Bertran, F., La Joie, R., Landeau, B., Mézenge, F., Desgranges, B., et al. (2012). The hippocampus remains activated over the long term for the retrieval of truly episodic memories. PLoS ONE, 7, e43495. https://doi.org/10.1371/journal.pone.0043495
Horchak, O. V., & Garrido, M. V. (2020a). Dropping bowling balls on tomatoes: Representations of object state-changes during sentence processing. Journal of Experimental Psychology: Learning, Memory, and Cognition. https://doi.org/10.1037/xlm0000980
Horchak, O. V., & Garrido, M. V. (2020b). Explicit (not implicit) attitudes mediate the focus of attention during sentence processing. Frontiers in Psychology, 11, 1–15. https://doi.org/10.3389/fpsyg.2020.583814
Joseph, R., Steele, S., Meyer, E., & Tager-Flusberg, H. (2005). Self-ordered pointing in children with autism: Failure to use verbal mediation in the service of working memory? Neuropsychologia, 43, 1400–1411. https://doi.org/10.1016/j.neuropsychologia.2005.01.010
Justus, S. A., Powell, P. S., & Duarte, A. (2021). Intact context memory performance in adults with autism spectrum disorder. Scientific Reports, 11, 20482. https://doi.org/10.1038/s41598-021-99898-2
Mäntylä, T. (1997). Recollections of faces: Remembering differences and knowing similarities. Journal of Experimental Psychology: Learning, Memory, and Cognition, 23, 1203–1216. https://doi.org/10.1037/0278-7393.23.5.1203
Medin, D. L., Unsworth, S. J., & Hirschfeld, L. (2007). Culture, categorization and reasoning. In S. Kitayama & D. Cohen (Eds.), Handbook of cultural psychology (pp. 615–644). Guilford Press.
Meier, B., Rey-Mermet, A., Rothen, N., & Graf, P. (2013). Recognition memory across the lifespan: The impact of word frequency and study-test interval on estimates of familiarity and recollection. Frontiers in Psychology. https://doi.org/10.3389/fpsyg.2013.00787
Meyer, B. J., Gardiner, J. M. & Bowler, D. M. (2014). Directed forgetting in high-functioning adults with autism spectrum disorders. Journal of Autism and Developmental Disorders, 44, 2514–2524. https://doi.org/10.1007/s10803-014-2121-y
Molesworth, C. J., Bowler, D. M., & Hampton, J. A. (2005). The prototype effect in recognition memory: Intact in autism? Journal of Child Psychology and Psychiatry, 46, 661–672. https://doi.org/10.1111/j.1469-7610.2004.00383.x
Murphy, G. L., & Medin, D. L. (1985). The role of theories in conceptual coherence. Psychological Review, 92(3), 289–316. https://doi.org/10.1037/0033-295X.92.3.289
Myles, B. S., Barnhill, G. P., Hagiwara, T., Griswold, D. E., & Simpson, R. L. (2001). A Synthesis of studies on the intellectual, academic, social/emotional and sensory characteristics of children and youth with Asperger Syndrome. Education and Training in Mental Retardation and Developmental Disabilities, 36(3), 304–311.
Nadel, L. (2020). What Is a Memory That It Can Be Changed? Neuroscience of Enduring Change. https://doi.org/10.1093/oso/9780190881511.003.0002
Nadel, L., & Moscovitch, M. (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Current opinion in Neurobiology, 7(2), 217–227. https://doi.org/10.1016/s0959-4388(97)80010-4
Queiroz-Garcia, I., Espirito Santo, H., & Pires, C. (2021). Psychometric properties of the Raven’s Standard Progressive Matrices in a Portuguese sample. Revista Portuguesa De Investigação Comportamental e Social, 7(1), 84–101. https://doi.org/10.31211/rpics.2021.7.1.210
R Core Team (2019). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/
Rosch, E. H. (1978). Principles of categorization. In E. H. Rosch & B. B. Lloyd (Eds.), Cognition and categorization (pp. 27–48). Erlbaum.
Santi, A., Raposo, A., & Marques, J. F. (2015). Superordinate and domain category structure: Evidence from typicality ratings. Revista Portuguesa de Psicologia, 44, 81–108. https://doi.org/10.21631/rpp44_81
Sekeres, M. J., Winocur, G., Moscovitch, M., Anderson, J. A. E., Pishdadian, S., Wojtowicz, J. M., St-Laurent, M., McAndrews, M. P., & Grady, C. (2018). Changes in patterns of neural activity underlie a time-dependent transformation of memory in rats and humans. Hippocampus, 28, 745–764. https://doi.org/10.1002/hipo.23009
Souchay, C., Wojcik, D. Z., Williams, H. L., Crathern, S., & Clarke, P. (2013). Recollection in adolescents with autism spectrum disorder. Cortex, 49, 1598–1609. https://doi.org/10.1016/j.cortex.2012.07.011
Souza, C., Coco, M. I., Pinho, S., Filipe, C. N., & Carmo, J. C. (2016). Contextual effects on visual short-term memory in high-functioning autism spectrum disorders. Research in Autism Spectrum Disorders, 32, 64–69. https://doi.org/10.1016/j.rasd.2016.09.003
Souza, C., Garrido, M. V., & Carmo, J. C. (2020). A systematic review of normative studies using images of common objects. Frontiers in Psychology, 11, 1–23. https://doi.org/10.3389/fpsyg.2020.573314
Souza, C., Garrido, M. V., Horchak, O., & Carmo, J. C. (2021a). Conceptual knowledge modulates memory recognition of common items: The selective role of item-typicality. Memory & Cognition. https://doi.org/10.3758/s13421-021-01213-x
Souza, C., Garrido, M. V., Saraiva, M., & Carmo, J. C. (2021b). RealPic: Picture norms of real-world common items. Behavior Research Methods. https://doi.org/10.3758/s13428-020-01523-z
Toichi, M., & Kamio, Y. (2002). Long-term memory and levels-of-processing in autism. Neuropsychologia, 40, 964–969. https://doi.org/10.1016/S0028-3932(01)00163-4
Toichi, M., & Kamio, Y. (2003). Long-term memory in high-functioning Autism: Controversy on episodic memory in Autism reconsidered. Journal of Autism and Developmental Disorders, 33, 151–161. https://doi.org/10.1023/a:1022935325843
Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., et al. (2007). Schemas and memory consolidation. Science, 316, 76–82. https://doi.org/10.1126/science.1135935
Tulving, E. (1972). Episodic and semantic memory. In E. Tulving & W. Donaldson (Eds.), Organization of memory (pp. 381–403). Academic Press.
Tulving, E. (1985). How many memory systems are there? American Psychologist, 40, 385–398. https://doi.org/10.1037/0003-066x.40.4.385
Tulving, E. (2000). Memory: An overview. Encyclopedia of Psychology, 5, 161–162. https://doi.org/10.1037/10520-078
van Kesteren, M. T. R., Rijpkema, M., Ruiter, D. J., & Fernández, G. (2013). Consolidation differentially modulates schema effects on memory for items and associations. PLoS ONE,. https://doi.org/10.1371/journal.pone.0056155
van Kesteren, M. T. R., Rijpkema, M., Ruiter, D. J., Morris, R. G. M., & Fernández, G. (2014). Building on prior knowledge: Schema-dependent encoding processes relate to academic performance. Journal of Cognitive Neuroscience, 26, 2250–2261. https://doi.org/10.1162/jocn_a_00630
Winocur, G., & Moscovitch, M. (2011). Memory transformation and systems consolidation. Journal of the International Neuropsychological Society, 17, 766–780. https://doi.org/10.1017/s1355617711000683
Winocur, G., Moscovitch, M., & Bontempi, B. (2010). Memory formation and long-term retention in humans and animals: Convergence towards a transformation account of hippocampal–neocortical interactions. Neuropsychologia, 48, 2339–2356. https://doi.org/10.1016/j.neuropsychologia.2010.04.016
Yonelinas, A. P. (2002). Components of episodic memory: The contribution of recollection and familiarity. In: A. Baddeley, J. Aggleton, & M. Conway (Eds.), Episodic memory: New directions in research (pp. 31–52). Oxford University Press. https://doi.org/10.1093/acprof:oso/9780198508809.003.0003
Yonelinas, A. P., Aly, M., Wang, W.-C., & Koen, J. D. (2010). Recollection and familiarity: Examining controversial assumptions and new directions. Hippocampus, 20, 1178–1194. https://doi.org/10.1002/hipo.20864
Yonelinas, A. P., Ranganath, C., Ekstrom, A. D., & Wiltgen, B. J. (2019). A contextual binding theory of episodic memory: Systems consolidation reconsidered. Nature Reviews Neuroscience, 20, 364–375. https://doi.org/10.1038/s41583-019-0150-4
Zwaigenbaum, L., Bryson, S.E., Szatmari, P., Brian, J., Smith, I. M., Roberts, W., Vaillancourt, T., & Roncadin, C. (2012). Sex differences in children with autism spectrum disorder identified within a high-risk infant cohort. Journal of Autism and Developmental Disorders., 42, 2585–2596. https://doi.org/10.1007/s10803-012-1515-y
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The authors would like to thank all the feedback from colleagues and experts who helped improve this work, the cooperation of the institutions that mediated the access to the clinical sample, and the participants for their valuable contribution to the present research.
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This research was supported by the Fundação para a Ciência e Tecnologia, Portugal, with grants awarded to CS (PD/BD/128249/2016), OH (SFRH/BPD/115533/2016) and JCC (Norma Transitória DL57/2016/CP1439/CT02 and through the Research Center for Psychological Science of the Faculty of Psychology, University of Lisbon, UIDB/ UIDP 04527/2020). The funders had no role in study design, data collection, analysis, publication decision, or manuscript preparation.
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CS, MG, and JC, contributed equally to designing the study, the procedures, and drafting the manuscript. CS executed the data collection and respective preliminary data analysis. OH performed the mixed-effects regression analyses in R. MG, and JC supervised and coordinated the whole process of producing this work. JB-C was responsible for the recruitment of individuals with ASD and for confirming their clinical diagnosis. All authors revised the manuscript and provided theoretical comments based on their expertise.
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Souza, C., Garrido, M.V., Horchak, O.V. et al. The Distinctive Pattern of Declarative Memories in Autism Spectrum Disorder: Further Evidence of Episodic Memory Constraints. J Autism Dev Disord 53, 3012–3022 (2023). https://doi.org/10.1007/s10803-022-05579-y
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DOI: https://doi.org/10.1007/s10803-022-05579-y