The role of executive processes in working memory deficits in Parkinson’s Disease

• Authors: Aleksandra Gruszka , Daniel Bor , Roger R. Barker , Edward Necka , Adrian M. Owen
• Languages of publication: EN

Abstracts

EN

Idiopathic Parkinson’s disease (PD) impairs working memory, but the exact nature of this deficit in terms of the underlying cognitive mechanisms is not well understood. In this study patients with mild clinical symptoms of PD were compared with matched healthy control subjects on a computerized battery of tests designed to assess spatial working memory and verbal working memory. In the spatial working memory task, subjects were required to recall a sequence of four locations. The verbal working memory task was methodologically identical except for the modality of the stimuli used, requiring subjects to orally recall a sequence of six digits. In either case, half of the sequences were structured in a way that allowed ‘chunking’, while others were unstructured. This manipulation was designed to dissociate the strategic component of task performance from the memory-load component. Mild medicated patients with PD were impaired only on the structured versions of the verbal working memory tasks. The analogous deficit in the spatial working memory was less pronounced. These findings are in agreement with the hypothesis that working memory deficits in PD reflect mainly the executive component of the tasks and that the deficits may be at least partly modality-independent.

Keywords

EN

Parkinson’s disease; spatial working memory; verbal working memory; frontal lobe; executive function

• Publisher: Committee for Psychological Sciences, Polish Academy of Sciences
• Journal: Polish Psychological Bulletin
• Year: 2016
• Volume: 47
• Issue: 1
• Pages: 123-130

Dates

published

2016-04-01

online

2016-05-14

Contributors

author

Aleksandra Gruszka

• Institute of Psychology, Jagiellonian University, Krakow, Poland

author

Daniel Bor

• Sackler Centre for Consciousness Science, University of Sussex, UK
• Department of Informatics, University of Sussex, UK

author

Roger R. Barker

• Department of Neurology, Addenbrooke’s Hospital, Cambridge, UK

author

Edward Necka

• Institute of Psychology, Jagiellonian University, Krakow, Poland

author

Adrian M. Owen

• The Brain and Mind Institute, Western University, Natural Science Centre, London, Ontario, Canada

References

• Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annual Review of Neuroscience, 9, 357-381. 10.1146/annurev. ne.09.030186.002041[Crossref]
• Beato, R., Levy, R., Pillon, B., Vidal, C., du Montcel, S. T., Deweer, B., … Cardoso, F. (2008). Working memory in Parkinson’s disease patients: clinical features and response to levodopa. Arquivos de Neuro-Psiquiatria, 66(2a), 147-151. 10.1590/S0004-282X200 8000200001
• Bor, D., Cumming, N., Scott, C. E. L., & Owen, A. M. (2004). Prefrontal cortical involvement in verbal encoding strategies: Modality independent PFC involvement in strategies. European Journal of Neuroscience, 19(12), 3365-3370. 10.1111/j.1460-9568.2004.03438.x
• Bor, D., Duncan, J., Lee, A. C. H., Parr, A., & Owen, A. M. (2006). Frontal lobe involvement in spatial span: Converging studies of normal and impaired function. Neuropsychologia, 44(2), 229-237. 10.1016/j. neuropsychologia.2005.05.010[Crossref]
• Bor, D., Duncan, J., Wiseman, R. J., & Owen, A. M. (2003). Encoding Strategies Dissociate Prefrontal Activity from Working Memory Demand. Neuron, 37(2), 361-367. 10.1016/S0896-6273(02)01171-6[Crossref]
• Bor, D., & Owen, A. M. (2006). A Common Prefrontal-Parietal Network for Mnemonic and Mathematical Recoding Strategies within Working Memory. Cerebral Cortex, 17(4), 778-786. doi.org/10.1093/cercor/bhk035[Crossref]
• Bradley, V. A., Welch, J. L., & Dick, D. J. (1989). Visuospatial working memory in Parkinson’s disease. Journal of Neurology, Neurosurgery & Psychiatry, 52(11), 1228-1235. 10.1136/jnnp.52.11.1228[Crossref]
• Brown, R. G., & Marsden, C. D. (1984). How Common is Dementia in Paskinson’s Disease? The Lancet, 324(8414), 1262-1265. http://doi.org/10.1016/S0140-6736(84)92807-1[Crossref]
• Cabeza, R., & Nyberg, L. (2000). Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies. Journal of Cognitive Neuroscience, 12(1), 1-47. 10.1162/08989290051137585[Crossref]
• Caminiti, S. P., Siri, C., Guidi, L., Antonini, A., & Perani, D. (2015). The Neural Correlates of Spatial and Object Working Memory in Elderly and Parkinson’s Disease Subjects. Behavioural Neurology, 2015, 1-10. 10.1155/2015/123636
• Cools, R. (2006). Dopaminergic modulation of cognitive function-implications for l-DOPA treatment in Parkinson’s disease. Neuroscience & Biobehavioral Reviews, 30(1), 1-23. 10.1016/j.neubiorev. 2005.03.024[Crossref]
• Costa, A., Peppe, A., Dell’Agnello, G., Carlesimo, G. A., Murri, L., Bonuccelli, U., Caltagirone, C. (2003). Dopaminergic Modulation of Visual- Spatial Working Memory in Parkinson’s Disease. Dementia and Geriatric Cognitive Disorders, 15(2), 55-66. 10.1159/000067968
• Downes, J. J., Roberts, A. C., Sahakian, B. J., Evenden, J. L., Morris, R. G., & Robbins, T. W. (1989). Impaired extra-dimensional shift performance in medicated and unmedicated Parkinson’s disease: Evidence for a specific attentional dysfunction. Neuropsychologia, 27(11-12), 1329-1343. 10.1016/0028-3932(89)90128-0
• 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. 10.1016/j.neuropsychologia.2015.07.031
• Fletcher, P. C., & Henson, R. N. A. (2001). Frontal lobes and human memory: Insights from functional neuroimaging. Brain, 124(5), 849-881. 10.1093/brain/124.5.849
• Foster, P. S., Yung, R. C., Drago, V., Crucian, G. P., & Heilman, K. M. (2013). Working memory in Parkinson’s disease: The effects of depression and side of onset of motor symptoms. Neuropsychology, 27(3), 303-313. 10.1037/a0032265[Crossref]
• 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. 10.1037/0894-4105.14.2.247[Crossref]
• Gabrieli, J. D. E., Singh, J., Stebbins, G. T., & Goetz, C. G. (1996). Reduced working memory span in Parkinson’s disease: Evidence for the role of frontostriatal system in working and strategic memory. Neuropsychology, 10(3), 322-332. 10.1037/0894-4105.10.3.321[Crossref]
• Gibb, W. R. G., & Lees, A. J. (1988). A comparison of clinical and pathological features of young- and old-onset Parkinson’s disease. Neurology, 38(9), 1402-1402. 10.1212/WNL.38.9.1402[Crossref]
• Goldman-Rakic, P. S. (2011). Circuitry of Primate Prefrontal Cortex and Regulation of Behavior by Representational Memory. In R. Terjung (Ed.), Comprehensive Physiology. Hoboken, NJ, USA: John Wiley & Sons, Inc. Retrieved from 10.1002/cphy.cp010509
• Kraft, E., Binder, E., Lulé, D., Storch, A., & Gruber, O. (2012). Dopaminergic modulation of neural correlates of working memory in Parkinson’s Disease. Basal Ganglia, 2(1), 33-39. 10.1016/j. baga.2012.01.003[Crossref]
• Lange, K. W., Robbins, T. W., Marsden, C. D., James, M., Owen, A. M., & Paul, G. M. (1992). L-dopa withdrawal in Parkinson’s disease selectively impairs cognitive performance in tests sensitive to frontal lobe dysfunction. Psychopharmacology, 107(2-3), 394-404.[Crossref]
• Le Bras, C. L., Pillon, B., Damier, P., & Dubois, B. (1998). At which steps of spatial working memory processing do striatofrontal circuits intervene in humans? Neuropsychologia, 37(1), 83-90. 10.1016/ S0028-3932(98)00041-4[Crossref]
• Lewis, S. J. G., Cools, R., Robbins, T. W., Dove, A., Barker, R. A., & Owen, A. M. (2003). Using executive heterogeneity to explore the nature of working memory deficits in Parkinson’s disease. Neuropsychologia, 41(6), 645-654.[Crossref]
• Lewis, S. J. G., 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. G., 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. 10.1016/j.neuropsychologia.2004.10.001[Crossref]
• Miah, I. P., Olde Dubbelink, K. T., Stoffers, D., Deijen, J. B., & Berendse, H. W. (2012). Early-stage cognitive impairment in Parkinson’s disease and the influence of dopamine replacement therapy. European Journal of Neurology, 19(3), 510-516. 10.1111/j.1468-1331.2011.03578.x
• Miller, G. A. (1956). The magical number seven, plus or minus two: some limits on our capacity for processing information. Psychological Review, 63(2), 81-97. 10.1037/h0043158
• 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, and Psychiatry, 51(6), 757-766.[Crossref]
• Mortimer, J. A., Pirozzolo, F. J., Hansch, E. C., & Webster, D. D. (1982). Relationship of motor symptoms to intellectual deficits in Parkinson disease. Neurology, 32(2), 133-137.[Crossref]
• Nelson, H. E. (1982). National adult reading test (NART): for the assessment of premorbid intelligence in patients with dementia ; test manual. Windsor: NFER-Nelson.
• Owen, A. M. (2004). Cognitive Dysfunction in Parkinson’s Disease: The Role of Frontostriatal Circuitry. The Neuroscientist, 10(6), 525-537. 10.1177/1073858404266776[Crossref]
• Owen, A. M., Beksinska, M., James, M., Leigh, P. N., Summers, B. A., Marsden, C. D., … Robbins, T. W. (1993). Visuospatial memory deficits at different stages of Parkinson’s disease. Neuropsychologia, 31(7), 627-644.[Crossref]
• Owen, A. M., Evans, A. C., & Petrides, M. (1996). Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. Cerebral Cortex (New York, N.Y.: 1991), 6(1), 31-38.[Crossref]
• Owen, A. M., Herrod, N. J., Menon, D. K., Clark, J. C., Downey, S. P. M. J., Carpenter, T. A., … Pickard, J. D. (1999). Redefining the functional organization of working memory processes within human lateral prefrontal cortex. European Journal of Neuroscience, 11(2), 567-574.10.1046/j.1460-9568.1999.00449.x [Crossref]
• 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. 10.1016/S0028-3932(96)00101-7[Crossref]
• Owen, A. M., James, M., Leigh, P. N., Summers, B. A., Marsden, C. D., Quinn, N. P., … Robbins, T. W. (1992). Fronto-striatal cognitive deficits at different stages of Parkinson’s diesease. Brain, 115(6), 1727-1751. 10.1093/brain/115.6.1727
• Owen, A. M., Morris, R. G., Sahakian, B. J., Polkey, C. E., & Robbins, T. W. (1996). Double dissociations of memory and executive functions in working memory tasks following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Brain: A Journal of Neurology, 119 (Pt 5), 1597-1615.
• Owen, A. M., Sahakian, B. J., Hodges, J. R., Summers, B. A., & et al. (1995). Dopamine-dependent frontostriatal planning deficits in early Parkinson’s disease. Neuropsychology, 9(1), 126-140.10.1037/0894-4105.9.1.126[Crossref]
• Owen, A. M., Stern, C. E., Look, R. B., Tracey, I., Rosen, B. R., & Petrides, M. (1998). Functional organization of spatial and nonspatial working memory processing within the human lateral frontal cortex. Proceedings of the National Academy of Sciences, 95(13), 7721-7726.
• Palazzini, E., Soliveri, P., Filippini, G., Fetoni, V., Zappacosta, B., Scigliano, G., … Girotti, F. (1995). Progression of motor and cognitive impairment in Parkinson’s disease. Journal of Neurology, 242(8), 535-540. 10.1007/BF00867426
• Pillon, B., Deweer, B., Vidailhet, M., Bonnet, A.-M., Hahn-Barma, V., & Dubois, B. (1998). Is impaired memory for spatial location in Parkinson’s disease domain specific or dependent on ‘strategic’ processes? Neuropsychologia, 36(1), 1-9. http://doi.org/10.1016/S0028-3932(97)00102-4[Crossref]
• Pochon, J.-B. (2001). The Role of Dorsolateral Prefrontal Cortex in the Preparation of Forthcoming Actions: an fMRI Study. Cerebral Cortex, 11(3), 260-266. 10.1093/cercor/11.3.260[Crossref]
• Possin, K. L., Filoteo, J. V., Song, D. D., & Salmon, D. P. (2008). Spatial and object working memory deficits in Parkinson’s disease are due to impairment in different underlying processes. Neuropsychology, 22(5), 585-595. 10.1037/a0012613[Crossref]
• 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.[Crossref]
• Prabhakaran, V., Narayanan, K., Zhao, Z., & Gabrieli, J. D. (2000). Integration of diverse information in working memory within the frontal lobe. Nature Neuroscience, 3(1), doi.org/10.1038/71156 [Crossref]
• Robbins, T. W., Weinberger, D., Taylor, J. G., & Morris, R. G. (1996). Dissociating Executive Functions of the Prefrontal Cortex [and Discussion]. Philosophical Transactions of the Royal Society B: Biological Sciences, 351(1346), 1463-1471. 10.1098/rstb.1996.0131
• 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. 10.1037/0894-4105.22.4.450[Crossref]
• Slabosz, A., Lewis, S. J. G., Smigasiewicz, K., Szymura, B., Barker, R. A., & Owen, A. M. (2006). The role of learned irrelevance in attentional set-shifting impairments in Parkinson’s disease. Neuropsychology, 20(5), 578-588. 10.1037/0894-4105.20.5.578[Crossref]
• Taylor, A. E., Saint-Cyr, J. A., & Lang, A. E. (1986). Frontal lobe dysfunction in Parkinson’s disease. The cortical focus of neostriatal outflow. Brain: A Journal of Neurology, 109 (Pt 5), 845-883.
• Trujillo, J. P., Gerrits, N. J. H. M., Veltman, D. J., Berendse, H. W., van der Werf, Y. D., & van den Heuvel, O. A. (2015). Reduced neural connectivity but increased task-related activity during working memory in de novo Parkinson patients: Working Memory in Parkinson’s Disease. Human Brain Mapping, 36(4), 1554-1566. 10.1002/ hbm.22723[Crossref]
• Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory: Cognitive, Affective, & Behavioral Neuroscience, 3(4), 255-274. 10.3758/CABN.3.4.255

Identifiers

DOI

10.1515/ppb-2016-0013