Mechanisms underlying corruption of working memory in Parkinson's disease.

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    • Source:
      Publisher: Wiley-Blackwell Country of Publication: England NLM ID: 101468753 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1748-6653 (Electronic) Linking ISSN: 17486645 NLM ISO Abbreviation: J Neuropsychol Subsets: MEDLINE
    • Publication Information:
      Publication: 2011- : Chichester : Wiley-Blackwell
      Original Publication: Leicester : British Psychological Society, c2007-
    • Subject Terms:
    • Abstract:
      Working memory (WM) impairments are reported to occur in patients with Parkinson's disease (PD). However, the mechanisms are unclear. Here, we investigate several putative factors that might drive poor performance, by examining the precision of recall, the order in which items are recalled and whether memories are corrupted by random guessing (attentional lapses). We used two separate tasks that examined the quality of WM recall under different loads and retention periods, as well as a traditional digit span test. Firstly, on a simple measure of WM recall, where patients were asked to reproduce the orientation of a centrally presented arrow, overall recall was not significantly impaired. However, there was some evidence for increased guessing (attentional lapses). On a new analogue version of the Corsi-span task, where participants had to reproduce on a touchscreen the exact spatial pattern of presented stimuli in the order and locations in which they appeared, there was a reduction in the precision of spatial WM at higher loads. This deficit was due to misremembering item order. At the highest load, there was reduced recall precision, whereas increased guessing was only observed at intermediate set sizes. Finally, PD patients had impaired backward, but not forward, digit spans. Overall, these results reveal the task- and load-dependent nature of WM deficits in PD. On simple low-load tasks, attentional lapses predominate, whereas at higher loads, in the spatial domain, the corruption of mnemonic information-both order item and precision-emerge as the main driver of impairment.
      (© 2023 The Authors. Journal of Neuropsychology published by John Wiley & Sons Ltd on behalf of The British Psychological Society.)
    • References:
      Aarsland, D., Creese, B., Politis, M., Chaudhuri, K. R., Ffytche, D. H., Weintraub, D., & Ballard, C. (2017). Cognitive decline in Parkinson disease. Nature Reviews Neurology, 13(4), Art. 4. https://doi.org/10.1038/nrneurol.2017.27.
      Baddeley, A. (2012). Working memory: Theories, models, and controversies. Annual Review of Psychology, 63, 1-29.
      Baddeley, A., Bressi, S. S., Della Sala, S., Logie, R., & Spinnler, H. H. (1991). The decline of working memory in Alzheimer's disease: A longitudinal study. Brain, 114(6), 2521-2542. https://doi.org/10.1093/brain/114.6.2521.
      Bak, T. H., & Mioshi, E. (2007). A cognitive bedside assessment beyond the MMSE: The Addenbrooke's cognitive examination. Practical Neurology, 7(4), 245-249.
      Bays, P. M., Catalao, R. F. G., & Husain, M. (2009). The precision of visual working memory is set by allocation of a shared resource. Journal of Vision, 9(10), 7.1-7.11.
      Bek, J., Humphries, S., Poliakoff, E., & Brady, N. (2022). Mental rotation of hands and objects in ageing and Parkinson's disease: Differentiating motor imagery and visuospatial ability. Experimental Brain Research, 240(7), 1991-2004. https://doi.org/10.1007/s00221-022-06389-5.
      Blackburn, H. L., & Benton, A. L. (1957). Revised administration and scoring of the digit span test. Journal of Consulting Psychology, 21, 139-143. https://doi.org/10.1037/h0047235.
      Calabresi, P., Castrioto, A., Di Filippo, M., & Picconi, B. (2013). New experimental and clinical links between the hippocampus and the dopaminergic system in Parkinson's disease. The Lancet Neurology, 12(8), 811-821. https://doi.org/10.1016/S1474-4422(13)70118-2.
      Camicioli, R., Moore, M. M., Kinney, A., Corbridge, E., Glassberg, K., & Kaye, J. A. (2003). Parkinson's disease is associated with hippocampal atrophy. Movement Disorders, 18(7), 784-790. https://doi.org/10.1002/mds.10444.
      Christopher, G., & MacDonald, J. (2005). The impact of clinical depression on working memory. Cognitive Neuropsychiatry, 10(5), 379-399. https://doi.org/10.1080/13546800444000128.
      Cole, D. M., Oei, N. Y., Soeter, R. P., Both, S., van Gerven, J. M., Rombouts, S. A., & Beckmann, C. F. (2012). Dopamine-dependent architecture of cortico-subcortical network connectivity. Cerebral Cortex, 23(7), 1509-1516.
      Delaveau, P., Salgado-Pineda, P., Fossati, P., Witjas, T., Azulay, J.-P., & Blin, O. (2010). Dopaminergic modulation of the default mode network in Parkinson's disease. European Neuropsychopharmacology, 20(11), 784-792. https://doi.org/10.1016/j.euroneuro.2010.07.001.
      Ester, E. F., Vogel, E. K., & Awh, E. (2012). Discrete resource limits in attention and working memory. Cognitive Neuroscience of Attention, 2, 99-112.
      Fallon, S. J., Bor, D., Hampshire, A., Barker, R. A., & Owen, A. M. (2017). Spatial structure normalises working memory performance in Parkinson's disease. Cortex, 96, 73-82.
      Fallon, S. J., Gowell, M., Maio, M. R., & Husain, M. (2019). Dopamine affects short-term memory corruption over time in Parkinson's disease. NPJ Parkinson's Disease, 5(1), 1-7.
      Fallon, S. J., Mattiesing, R. M., Dolfen, N., Manohar, S., & Husain, M. (2018). Ignoring versus updating in working memory reveal differential roles of attention and feature binding. Cortex, 107, 50-63. https://doi.org/10.1016/j.cortex.2017.12.016.
      Fallon, S. J., Mattiesing, R. M., Muhammed, K., Manohar, S., & Husain, M. (2017). Fractionating the neurocognitive mechanisms underlying working memory: Independent effects of dopamine and Parkinson's disease. Cerebral Cortex, 27(12), 5727-5738.
      Fallon, S. J., Muhammed, K., Drew, D. S., Ang, Y.-S., Manohar, S. G., & Husain, M. (2019). Dopamine guides competition for cognitive control: Common effects of haloperidol on working memory and response conflict. Cortex, 113, 156-168. https://doi.org/10.1016/j.cortex.2018.11.031.
      Fallon, S. J., Smulders, K., Esselink, R. A., van de Warrenburg, B. P., Bloem, B. R., & Cools, R. (2015). Differential optimal dopamine levels for set-shifting and working memory in Parkinson's disease. Neuropsychologia, 77, 42-51.
      Fallon, S. J., Zokaei, N., Norbury, A., Manohar, S. G., & Husain, M. (2016). Dopamine alters the Fidelity of working memory representations according to attentional demands. Journal of Cognitive Neuroscience, 29, 728-738. https://doi.org/10.1162/jocn_a_01073.
      Fournet, N., Moreaud, O., Roulin, J. L., Naegele, B., & Pellat, J. (2000). Working memory functioning in medicated Parkinson's disease patients and the effect of withdrawal of dopaminergic medication. Neuropsychology, 14(2), 247-253.
      Gathercole, S. E., Brown, L., & Pickering, S. J. (2003). Working memory assessments at school entry as longitudinal predictors of National Curriculum attainment levels. Educational and Child Psychology, 20(3), 109-122.
      Grogan, J. P., Knight, L. E., Smith, L., Irigoras Izagirre, N., Howat, A., Knight, B. E., Bickerton, A., Isotalus, H. K., & Coulthard, E. J. (2018). Effects of Parkinson's disease and dopamine on digit span measures of working memory. Psychopharmacology, 235(12), 3443-3450. https://doi.org/10.1007/s00213-018-5058-6.
      Gruszka, A., Bor, D., Barker, R. R., Necka, E., & Owen, A. M. (2016). The role of executive processes in working memory deficits in Parkinson's disease. Polish Psychological Bulletin, 47(1), 123-130. https://doi.org/10.1515/ppb-2016-0013.
      Helmich, R. C., de Lange, F. P., Bloem, B. R., & Toni, I. (2007). Cerebral compensation during motor imagery in Parkinson's disease. Neuropsychologia, 45(10), 2201-2215. https://doi.org/10.1016/j.neuropsychologia.2007.02.024.
      Jensen, O., & Mazaheri, A. (2010). Shaping functional architecture by oscillatory alpha activity: Gating by inhibition. Frontiers in Human Neuroscience, 4, 186.
      Kehagia, A. A., Murray, G. K., & Robbins, T. W. (2010). Learning and cognitive flexibility: Frontostriatal function and monoaminergic modulation. Current Opinion in Neurobiology, 20(2), 199-204.
      Kemps, E., Szmalec, A., Vandierendonck, A., & Crevits, L. (2005). Visuo-spatial processing in Parkinson's disease: Evidence for diminished visuo-spatial sketch pad and central executive resources. Parkinsonism & Related Disorders, 11(3), 181-186.
      Kleiner, M., Brainard, D., Pelli, D., Ingling, A., Murray, R., & Broussard, C. (2007). What's new in psychtoolbox-3. Perception, 36(14), 1-16.
      Lawson, R. A., Williams-Gray, C. H., Camacho, M., Duncan, G. W., Khoo, T. K., Breen, D. P., Barker, R. A., Rochester, L., Burn, D. J., Yarnall, A. J., & ICICLE-PD study group. (2021). Which neuropsychological tests? Predicting cognitive decline and dementia in Parkinson's disease in the ICICLE-PD cohort. Journal of Parkinson's Disease, 11(3), 1297-1308. https://doi.org/10.3233/JPD-212581.
      Lewis, S. J., Dove, A., Robbins, T. W., Barker, R. A., & Owen, A. M. (2003). Cognitive impairments in early Parkinson's disease are accompanied by reductions in activity in frontostriatal neural circuitry. The Journal of Neuroscience, 23(15), 6351-6356.
      Lewis, S. J., Slabosz, A., Robbins, T. W., Barker, R. A., & Owen, A. M. (2005). Dopaminergic basis for deficits in working memory but not attentional set-shifting in Parkinson's disease. Neuropsychologia, 43(6), 823-832.
      Liang, Y., Pertzov, Y., Nicholas, J. M., Henley, S. M., Crutch, S., Woodward, F., Leung, K., Fox, N. C., & Husain, M. (2016). Visual short-term memory binding deficit in familial Alzheimer's disease. Cortex, 78, 150-164.
      Ma, W. J., Husain, M., & Bays, P. M. (2014). Changing concepts of working memory. Nature Neuroscience, 17(3), 347-356.
      Masse, N. Y., Yang, G. R., Song, H. F., Wang, X. J., & Freedman, D. J. (2019). Circuit mechanisms for the maintenance and manipulation of information in working memory. Nature Neuroscience, 22(7), 1159-1167.
      Milner, B. (1971). Interhemispheric differences in the localization of psychological processes in man. British Medical Bulletin, 27, 272-277.
      Morris, R. G., Downes, J. J., Sahakian, B. J., Evenden, J. L., Heald, A., & Robbins, T. W. (1988). Planning and spatial working memory in Parkinson's disease. Journal of Neurology, Neurosurgery & Psychiatry, 51(6), 757-766.
      Myers, N. E., Stokes, M. G., Walther, L., & Nobre, A. C. (2014). Oscillatory brain state predicts variability in working memory. The Journal of Neuroscience, 34(23), 7735-7743.
      Oberauer, K., & Hein, L. (2012). Attention to information in working memory. Current Directions in Psychological Science, 21(3), 164-169.
      Owen, A. M., Beksinska, M., James, M., Leigh, P. N., Summers, B. A., Marsden, C. D., Quinn, N. P., Sahakian, B. J., & Robbins, T. W. (1993). Visuospatial memory deficits at different stages of Parkinson's disease. Neuropsychologia, 31(7), 627-644. https://doi.org/10.1016/0028-3932(93)90135-M.
      Owen, A. M., Iddon, J. L., Hodges, J. R., Summers, B. A., & Robbins, T. W. (1997). Spatial and non-spatial working memory at different stages of Parkinson's disease. Neuropsychologia, 35(4), 519-532.
      Owen, A. M., James, M., Leigh, P. N., Summers, B. A., Marsden, C. D., Quinn, N. P., Lange, K. W., & Robbins, T. W. (1992). Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain, 115(6), 1727-1751. https://doi.org/10.1093/brain/115.6.1727.
      Pertzov, Y., Dong, M. Y., Peich, M.-C., & Husain, M. (2012). Forgetting what was where: The fragility of object-location binding. PLoS One, 7(10), e48214.
      Pertzov, Y., Miller, T. D., Gorgoraptis, N., Caine, D., Schott, J. M., Butler, C., & Husain, M. (2013). Binding deficits in memory following medial temporal lobe damage in patients with voltage-gated potassium channel complex antibody-associated limbic encephalitis. Brain, 136, 2474-2485.
      Postle, B. R., Jonides, J., Smith, E. E., Corkin, S., & Growdon, J. H. (1997). Spatial, but not object, delayed response is impaired in early Parkinson's disease. Neuropsychology, 11(2), 171-179.
      Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., & Shulman, G. L. (2001). A default mode of brain function. Proceedings of the National Academy of Sciences, 98(2), 676-682.
      Ramos, A. A., & Machado, L. (2021). A comprehensive meta-analysis on short-term and working memory dysfunction in Parkinson's disease. Neuropsychology Review, 31, 288-311. https://doi.org/10.1007/s11065-021-09480-w.
      Sawamoto, N., Piccini, P., Hotton, G., Pavese, N., Thielemans, K., & Brooks, D. J. (2008). Cognitive deficits and striato-frontal dopamine release in Parkinson's disease. Brain, 131(5), 1294-1302.
      Siegert, R. J., Weatherall, M., Taylor, K. D., & Abernethy, D. A. (2008). A meta-analysis of performance on simple span and more complex working memory tasks in Parkinson's disease. Neuropsychology, 22(4), 450-461. https://doi.org/10.1037/0894-4105.22.4.450.
      Stoffers, D., Berendse, H. W., Deijen, J. B., & Wolters, E. C. (2003). Deficits on Corsi's block-tapping task in early stage Parkinson's disease. Parkinsonism & Related Disorders, 10(2), 107-111.
      Suchow, J. W., Brady, T. F., Fougnie, D., & Alvarez, G. A. (2013). Modeling visual working memory with the MemToolbox. Journal of Vision, 13(10), 9. https://doi.org/10.1167/13.10.9.
      Tabi, Y. A., Maio, M. R., Fallon, S. J., Udale, R., Dickson, S., Idris, M. I., Nobis, L., Manohar, S. G., & Husain, M. (2021). Impact of processing demands at encoding, maintenance and retrieval in visual working memory. Cognition, 214, 104758. https://doi.org/10.1016/j.cognition.2021.104758.
      Wesnes, K. A., McKeith, I., Edgar, C., Emre, M., & Lane, R. (2005). Benefits of rivastigmine on attention in dementia associated with Parkinson disease. Neurology, 65(10), 1654-1656. https://doi.org/10.1212/01.wnl.0000184517.69816.e9.
      Wheeler, B., & Torchiano, M. (2016). lmPerm: Permutation tests for linear models (2.1.0) [computer software]. https://CRAN.R-project.org/package=lmPerm.
      Wiecki, T. V., & Frank, M. J. (2010). Neurocomputational models of motor and cognitive deficits in Parkinson's disease. Progress in Brain Research, 183, 275-297.
      Wobbrock, J. O., Findlater, L., Gergle, D., & Higgins, J. J. (2011). The aligned rank transform for nonparametric factorial analyses using only Anova procedures. In Proceedings of the SIGCHI Conference on Human Factors in Computing Systems, 143-146. CHI. https://doi.org/10.1145/1978942.1978963.
      Ye, Z., Zhang, G., Zhang, Y., Li, S., Liu, N., Zhou, X., Xiao, W., & Münte, T. F. (2021). The role of the subthalamic nucleus in sequential working memory in De novo Parkinson's disease. Movement Disorders, 36(1), 87-95. https://doi.org/10.1002/mds.28344.
      Zhang, W., & Luck, S. J. (2008). Discrete fixed-resolution representations in visual working memory. Nature, 453(7192), 233-235.
      Zokaei, N., Burnett Heyes, S., Gorgoraptis, N., Budhdeo, S., & Husain, M. (2014). Working memory recall precision is a more sensitive index than span. Journal of Neuropsychology, 9, 319-329. https://doi.org/10.1111/jnp.12052.
      Zokaei, N., McNeill, A., Proukakis, C., Beavan, M., Jarman, P., Korlipara, P., Hughes, D., Mehta, A., Hu, M. T., Schapira, A. H., & Husain, M. (2014). Visual short-term memory deficits associated with GBA mutation and Parkinson's disease. Brain, 137(8), 2303-2311.
      Zokaei, N., Nour, M. M., Sillence, A., Drew, D., Adcock, J., Stacey, R., Voets, N., Sen, A., & Husain, M. (2019). Binding deficits in visual short-term memory in patients with temporal lobe lobectomy. Hippocampus, 29(2), 63-67. https://doi.org/10.1002/hipo.22998.
      Zokaei, N., Sillence, A., Kienast, A., Drew, D., Plant, O., Slavkova, E., Manohar, S. G., & Husain, M. (2020). Different patterns of short-term memory deficit in Alzheimer's disease, Parkinson's disease and subjective cognitive impairment. Cortex, 132, 41-50. https://doi.org/10.1016/j.cortex.2020.06.016.
    • Grant Information:
      United Kingdom WT_ Wellcome Trust; United Kingdom DH_ Department of Health
    • Contributed Indexing:
      Keywords: Parkinson's disease; attention; misbinding; spatial span; working memory
    • Publication Date:
      Date Created: 20230116 Date Completed: 20230609 Latest Revision: 20230614
    • Publication Date:
      20231215
    • Accession Number:
      10.1111/jnp.12306
    • Accession Number:
      36642965