Two semantic priming tasks, designed to isolate automatic and controlled semantic activation, were utilized to investigate the impact of dopamine depletion on semantic processing in Parkinson's disease (PD). Seven people with PD (tested whilst on and off levodopa medication) and seven healthy adults participated in the study. The healthy adult participants demonstrated intact automatic and controlled semantic activation. Aberrant controlled semantic activation was observed in the PD group on levodopa; however, automatic semantic activation was still evident. In contrast, automatic semantic activation was not evident in the PD group off levodopa. These results further clarify the impact of PD on semantic processing, demonstrating that dopamine depletion can cause disturbances in both automatic and controlled semantic activation. 1. Introduction Studies of language processing in Parkinson’s disease (PD) have provided clear evidence that even in the absence of overt dementia, semantic processing impairments may be evident in some people with the disease. In addition to widely reported impairments to verbal fluency in PD [1], impairments have been observed on tasks involving action naming [2], the judgment of semantic attributes and hierarchies [3], semantic word search [4], and semantic priming [5–8]. Despite these findings, the impact of PD on automatic versus controlled mechanisms of semantic processing is still unclear. The present study sought to utilize measures of automatic and controlled semantic priming to further elucidate the impact of dopamine depletion on these mechanisms of semantic processing in PD. Semantic priming refers to the faster recognition of target words that are preceded by a related prime word (e.g., apple fruit) compared to an unrelated prime word (e.g., paper fruit). Importantly, these semantic priming effects can be attributed to either automatic or controlled mechanisms. Automatic semantic priming is fast acting and refers to the automatic spreading of activation from prime to target that occurs within semantic networks [9]. Controlled priming, on the other hand, is slower acting and is typically attributed to either prelexical expectancy generation or postlexical semantic checking strategies [9]. During prelexical expectancy generation, participants use the prime word to generate an expectancy set of possible target words that are related to the prime word. Lexical decisions are subsequently faster to related target words that were included within the expectancy set. In contrast, postlexical semantic matching involves
References
[1]
J. D. Henry and J. R. Crawford, “Verbal fluency deficits in Parkinson's disease: a meta-analysis,” Journal of the International Neuropsychological Society, vol. 10, no. 4, pp. 608–622, 2004.
[2]
J. Rodríguez-Ferreiro, F. Cuetos, E. Herrera, M. Menéndez, and R. Ribacoba, “Cognitive impairment in Parkinson's disease without dementia,” Movement Disorders, vol. 25, no. 13, pp. 2136–2141, 2010.
[3]
R. Portin, S. Laatu, A. Revonsuo, and U. K. Rinne, “Impairment of semantic knowledge in parkinson disease,” Archives of Neurology, vol. 57, no. 9, pp. 1338–1343, 2000.
[4]
W. L. Arnott, H. J. Chenery, A. J. Angwin, B. E. Murdoch, P. A. Silburn, and D. A. Copland, “Decreased semantic competitive inhibition in Parkinson's disease: evidence from an investigation of word search performance,” International Journal of Speech-Language Pathology, vol. 12, no. 5, pp. 437–445, 2010.
[5]
A. J. Angwin, H. J. Chenery, D. A. Copland, B. E. Murdoch, and P. A. Silburn, “Summation of semantic priming and complex sentence comprehension in Parkinson's disease,” Cognitive Brain Research, vol. 25, no. 1, pp. 78–89, 2005.
[6]
A. J. Angwin, H. J. Chenery, D. A. Copland, B. E. Murdoch, and P. A. Silburn, “The speed of lexical activation is altered in Parkinson's disease,” Journal of Clinical and Experimental Neuropsychology, vol. 29, no. 1, pp. 73–85, 2007.
[7]
D. Copland, “The basal ganglia and semantic engagement: potential insights from semantic priming in individuals with subcortical vascular lesions, Parkinson's disease, and cortical lesions,” Journal of the International Neuropsychological Society, vol. 9, no. 7, pp. 1041–1052, 2003.
[8]
M. Grossman, E. Zurif, C. Lee et al., “Information processing speed and sentence comprehension in Parkinson's disease,” Neuropsychology, vol. 16, no. 2, pp. 174–181, 2002.
[9]
J. H. Neely, “Semantic priming effects in visual word recognition: a selective review of current findings and theories,” in Basic Processes in Reading: Visual Word Recognition, D. Besner and G. W. Humphreys, Eds., pp. 264–336, Lawrence Erlbaum, Hillsdale, NJ, USA, 1991.
[10]
D. A. Copland, H. J. Chenery, B. E. Murdoch, W. L. Arnott, and P. A. Silburn, “Dopamine enhances semantic salience: semantic priming evidence from healthy individuals,” Brain and Language, vol. 87, pp. 103–104, 2003.
[11]
D. A. Copland, K. L. McMahon, P. A. Silburn, and G. I. De Zubicaray, “Dopaminergic neuromodulation of semantic processing: a 4-T fMRI study with levodopa,” Cerebral Cortex, vol. 19, no. 11, pp. 2651–2658, 2009.
[12]
U. Kischka, T. H. Kammer, S. Maier, M. Weisbrod, M. Thimm, and M. Spitzer, “Dopaminergic modulation of semantic network activation,” Neuropsychologia, vol. 34, no. 11, pp. 1107–1113, 1996.
[13]
D. Roesch-Ely, S. Weiland, H. Scheffel et al., “Dopaminergic modulation of semantic priming in healthy volunteers,” Biological Psychiatry, vol. 60, no. 6, pp. 604–611, 2006.
[14]
A. J. Angwin, H. J. Chenery, D. A. Copland, W. L. Arnott, B. E. Murdoch, and P. A. Silburn, “Dopamine and semantic activation: an investigation of masked direct and indirect priming,” Journal of the International Neuropsychological Society, vol. 10, no. 1, pp. 15–25, 2004.
[15]
G. G. Brown, S. J. Brown, G. Christenson et al., “Effects of task structure on category priming in patients with Parkinson's disease and in healthy individuals,” Journal of Clinical and Experimental Neuropsychology, vol. 24, no. 3, pp. 356–369, 2002.
[16]
P. M. Butler, P. McNamara, and R. Durso, “Deficits in the automatic activation of religious concepts in patients with Parkinsons disease,” Journal of the International Neuropsychological Society, vol. 16, no. 2, pp. 252–261, 2010.
[17]
J. V. Filoteo, F. J. Friedrich, L. M. Rilling, J. D. Davis, J. L. Stricker, and M. Prenovitz, “Semantic and cross-case identity priming in patients with Parkinson's disease,” Journal of Clinical and Experimental Neuropsychology, vol. 25, no. 4, pp. 441–456, 2003.
[18]
W. L. Arnott, H. J. Chenery, B. E. Murdoch, and P. A. Silburn, “Semantic priming in Parkinson's disease: evidence for delayed spreading activation,” Journal of Clinical and Experimental Neuropsychology, vol. 23, no. 4, pp. 502–519, 2001.
[19]
A. J. Angwin, D. A. Copland, H. J. Chenery, B. E. Murdoch, and P. A. Silburn, “The influence of dopamine on semantic activation in Parkinson's disease: evidence from a multipriming task,” Neuropsychology, vol. 20, no. 3, pp. 299–306, 2006.
[20]
M. M. Hoehn and M. D. Yahr, “Parkinsonism: onset, progression and mortality,” Neurology, vol. 17, no. 5, pp. 427–442, 1967.
[21]
S. Mattis, Dementia Rating Scale. Professional Manual, Psychological Assessment Resources, Inc., Odessa, Fla, USA, 1988.
[22]
C. W. Olanow, A. H. V. Schapira, and O. Rascol, “Continuous dopamine-receptor stimulation in early Parkinson's disease,” Trends in Neurosciences, vol. 23, no. 10, pp. S117–S126, 2000.
[23]
P. J. Casey and R. A. Heath, “Category norms for Australians,” Australian Journal of Psychology, vol. 40, pp. 323–339, 1988.
[24]
W. L. Arnott and H. J. Chenery, “Lexical decision in Parkinson's disease: a comment on Spicer, Brown, and Gorell (1994), and McDonald, Brown, and Gorell (1996),” Journal of Clinical and Experimental Neuropsychology, vol. 21, no. 3, pp. 289–300, 1999.
[25]
H. J. Chenery, J. C. L. Ingram, and B. E. Murdoch, “The effect of repeated prime-target presentation in manipulating attention-induced priming in persons with dementia of the Alzheimer′s type,” Brain and Cognition, vol. 25, no. 1, pp. 108–127, 1994.
D. A. Copland, G. Sefe, J. Ashley, C. Hudson, and H. J. Chenery, “Impaired semantic inhibition during lexical ambiguity repetition in Parkinson's disease,” Cortex, vol. 45, no. 8, pp. 943–949, 2009.
[28]
C. Cepeda and M. S. Levine, “Dopamine and N-methyl-D-aspartate receptor interactions in the Neostriatum,” Developmental Neuroscience, vol. 20, no. 1, pp. 1–18, 1998.
[29]
R. G. Brown and C. D. Marsden, “Internal versus external cues and the control of attention in Parkinson's disease,” Brain, vol. 111, no. 2, pp. 323–345, 1988.
[30]
A. L. Price, “Contextual cues remediate problem solving: deficits in Parkinsons disease,” Journal of the International Neuropsychological Society, vol. 16, no. 1, pp. 70–76, 2010.
[31]
M. Gold, S. E. Nadeau, D. H. Jacobs, J. C. Adair, L. J. Gonzalez Rothi, and K. M. Heilman, “Adynamic aphasia: a transcortical motor aphasia with defective semantic strategy formation,” Brain and Language, vol. 57, no. 3, pp. 374–393, 1997.
[32]
A. Price, J. V. Filoteo, and W. T. Maddox, “Rule-based category learning in patients with Parkinson's disease,” Neuropsychologia, vol. 47, no. 5, pp. 1213–1226, 2009.
[33]
S. Goebel, H. M. Mehdorn, and B. Leplow, “Strategy instruction in Parkinson's disease: influence on cognitive performance,” Neuropsychologia, vol. 48, no. 2, pp. 574–580, 2010.
[34]
S. C. Grant and G. D. Logan, “The loss of repetition priming and automaticity over time as a function of degree of initial learning,” Memory & Cognition, vol. 21, no. 5, pp. 611–618, 1993.
[35]
K. A. Hutchison, D. A. Balota, M. J. Cortese, and J. M. Watson, “Predicting semantic priming at the item level,” The Quarterly Journal of Experimental Psychology, vol. 61, no. 7, pp. 1036–1066, 2008.
[36]
A. Antal, S. Kéri, Z. T. Kincses et al., “Dopaminergic contributions to the visual categorization of natural scenes: evidence from Parkinson's disease,” Journal of Neural Transmission, vol. 110, no. 7, pp. 757–770, 2003.
[37]
S. Righi, M. P. Viggiano, M. Paganini, S. Ramat, and P. Marini, “Recognition of category-related visual stimuli in Parkinson's disease: before and after pharmacological treatment,” Neuropsychologia, vol. 45, no. 13, pp. 2931–2941, 2007.
[38]
A. S. Pederzolli, M. E. Tivarus, P. Agrawal, S. K. Kostyk, K. M. Thomas, and D. Q. Beversdorf, “Dopaminergic modulation of semantic priming in Parkinson disease,” Cognitive and Behavioral Neurology, vol. 21, no. 3, pp. 134–137, 2008.
[39]
C. H. Williams-Gray, T. Foltynie, C. E. G. Brayne, T. W. Robbins, and R. A. Barker, “Evolution of cognitive dysfunction in an incident Parkinson's disease cohort,” Brain, vol. 130, no. 7, pp. 1787–1798, 2007.
[40]
H. L. Katzen, B. E. Levin, and W. Weiner, “Side and type of motor symptom influence cognition in Parkinson's disease,” Movement Disorders, vol. 21, no. 11, pp. 1947–1953, 2006.