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Abnormalities of habituation and task switching in patients with Parkinson's disease: an ERP study with frequent nontarget stimuli
International Congress Series 1278 (2005) 325 – 328
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Abnormalities of habituation and task switching in patients with Parkinson’s disease: an ERP study with frequent nontarget stimuli Junko Ito* Central Clinical Laboratory, Division of Neurophysiology, Kyoto University Hospital, 54 Shogoin Kawaracho, Sakyo-ku, Kyoto 606-8507, Japan
Abstract. To evaluate the effects of preceding stimuli, event-related potentials (ERPs) elicited by frequent nontarget stimuli (FNT) were studied in nondemented patients with Parkinson’s disease (PD) and healthy control subjects (Controls). Each stimulus, composed of two Japanese phonetic characters, was presented. Identical dhirakanaT characters (9%) were designated as target stimuli (Targets). FNT (73%) were composed of different dhirakanaT characters, and remaining stimuli were category-deviant nontarget stimuli (CDNT) composed of different dkatakanaT as well as phonetically task-relevant but category-deviant nontarget stimuli (RCDNT) composed of identical dkatakana.T Trials elicited by FNT were divided based on the preceding four stimulus types and averaged, respectively. ERPs elicited by FNT among the preceding four stimulus conditions were compared. Controls showed significant differences in N2 amplitudes, depending upon the preceding four stimulus conditions, whereas the PD patients did not show such differences. Regardless of the preceding stimulus conditions, the P3 components showed frontal maximal distribution, with larger P3 amplitudes for the PD patients than Controls. These findings suggest abnormalities of habituation and task-switching deficits resulting from depletion of attentional resources in PD patients. D 2004 Elsevier B.V. All rights reserved. Keywords: Parkinson’s disease; Frequent stimuli; Attention; Habituation
1. Introduction In a simple oddball paradigm, rare target stimuli elicit robust P3 components, but these components usually diminish in response to frequent nontarget stimuli (FNT) or standard * Tel.: +81 75 751 3658; fax: +81 75 752 3732. E-mail address: [email protected]. 0531-5131/ D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.ics.2004.11.105
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J. Ito / International Congress Series 1278 (2005) 325–328
stimuli. During a go–no/go task in a category-deviant dual paradigm, P3 components in response to FNT were comparatively less attenuated in patients with Parkinson’s disease (PD) [1]. To evaluate the effects of preceding stimulus types and changes in information processing strategies, event-related potentials (ERPs) elicited by FNT were evaluated in nondemented PD patients. 2. Patients and methods Sixteen nondemented idiopathic PD patients (seven males and nine females; mean age, 63.1 years) and 15 age-matched healthy control subjects (Controls; six males and nine females; mean age, 63.9 years) participated in this study. All subjects were native speakers of Japanese. Informed consent was obtained from both patients and Controls. X-ray CT and/or magnetic resonance imaging showed no ischemic lesions in the PD patients. None of the PD patients showed evidence of a secondary cause of PD or any extraparkinsonian neurological impairment. Motor symptoms in PD patients ranged from Stage I to Stage III [I (2), II (8) and III (6)] on the Hoehn and Yahr scale. Two patients had motor symptoms localized on the right side, while the remaining patients had motor symptoms on both sides. At the time of testing, they were treated with levodopa/dopadecarboxylase inhibitors and dopamine agonist. None of the control subjects or PD patients had taken any other drugs that might have affected the ERP components. Scores on the Mini-Mental State examination showed no significant differences between the two subject groups (Controls 29.1F0.6; PD patients 28.6F0.8). There were no significant differences in depression scores between the two subject groups. Each stimulus, composed of two Japanese phonetic characters, was displayed in the center of a computer monitor. Identical dhirakanaT characters, comprising 9% of all stimuli, were designated as target stimuli (Targets). FNT (73%) were composed of different dhirakanaT characters, and remaining stimuli were category-deviant nontarget stimuli (CDNT; 9%) composed of different dkatakanaT characters, as well as phonetically taskrelevant but category-deviant nontarget stimuli (RCDNT; 9%) composed of identical dkatakanaT characters. Each stimulus, which varied from trial-to-trial, was presented for 400 ms, and interstimulus intervals were 1800F100 ms. Each run was composed of 140 stimuli, and five runs were presented to individual subjects. The subjects were instructed to press a button with their preferred hand in response to Targets (go) and disregard other stimuli (no-go). Speed and accuracy were equally emphasized. The recording arrangement consisted of G1 affixed to the Fz, Cz, Pz and Oz of the International 10-20 System and G2 affixed to linked earlobes. The electroencephalogram (EEG) was amplified with a band-pass filter of 0.05 to 60 Hz. The electrooculogram (EOG) was recorded from the left outer canthus and the right supraorbital region. Trials elicited by FNT in each run were averaged, and N2 and P3 components of ERPs were compared across runs. Trials elicited by FNT obtained from five runs were divided into four conditions, depending whether the preceding stimulus was Target, CDNT, RCDNT or FNT. N2 and P3 components obtained from averages for the preceding four stimulus conditions were compared. The N2 and P3 components were subjected to an analysis of variance
J. Ito / International Congress Series 1278 (2005) 325–328
327
Fig. 1. Comparison of grand averaged waveforms for Controls and the PD patients obtained from the first (thick lines) and fifth (thin lines) run.
(ANOVA) with the subject group (Controls, PD), preceding stimulus condition (Targets, FNT, CDNT and RCDNT) and electrode (Fz, Cz, Pz and Oz). The criterion for significance was less than 0.05. 3. Results P3 amplitudes obtained from the fifth run was significantly reduced compared with that obtained from the first run in Controls [ F(1,28)=28.72, p=0.00001] and in the PD patients [ F(1,30)=8.54, p=0.007], and the amplitude reduction was smaller for the PD patients[ F(1,29)=16.13, p=0.0004] (Fig. 1). Controls showed significant differences in N2 amplitudes among the four stimulus conditions [ F(3,60)=5.57, p=0.002], whereas the PD patients did not show such differences (Fig. 2). Regardless of the preceding stimulus, the P3 components showed frontal maximal distribution in both subject groups [ F(3,60)=7.13, p=0.0003], with the PD patients showing larger P3 amplitudes than Controls [ F(1,29)=5.85, p=0.022] (Fig. 2).
Fig. 2. Grand averaged waveforms elicited by FNT among the preceding four stimulus types that were recorded from Controls and the PD patients. Thick lines indicate ERP waveforms elicited by FNT following Targets, thin lines those following RCDNT, thinner lines those following FNT and thinnest lines those following CDNT.
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J. Ito / International Congress Series 1278 (2005) 325–328
4. Discussion In the present paradigm, the subjects might have adopted a strategy involving simultaneous cognitive tasks, wherein the two characters were classified as dhirakanaT or category-deviant dkatakana,T and classified as different or identical and then decided whether to press the button or not. Moreover, each stimulus varied from trial to trial, so that subjects had to pay attention to each stimulus and change strategy from trial to trial. Deviance and discriminability of the preceding stimuli from FNT may have resulted in differences in the N2 amplitudes elicited by FNT among the four stimulus conditions in Controls. The lack of differences in the N2 amplitudes among the four stimulus conditions in the PD patients may have resulted from difficulty in changing strategy for information processing with each stimulus since PD patients have shown task-switching deficits resulting from depletion of attentional resources [2]. Rare dnovelT stimuli elicit a frontal maximal novelty P3 component [3]. Although stimulus probability was high, each FNT that varied from trial to trial was a dnovelT stimulus for the subjects. Thus, the P3 components in response to FNT were not so attenuated in the paradigm used for this study and showed frontal maximal distribution. The smaller P3 amplitude reduction from the first to the fifth run seen in the PD patients resulted from impairment of habituation. These findings are comparable with previous findings for PD patients that showed a lack of P3a habituation [4] and less habituation of novelty P3 component over the frontal scalp sites [3]. Thus, the larger P3 amplitude elicited by FNT in PD patients may be attributable to abnormalities of habituations resulting from the frontal lobe and basal ganglia dysfunction. References [1] J. Ito, Event-related potentials in Parkinson’s disease using category deviant and inhibition paradigm, Clinical Encephalography 43 (4) (2001) 243 – 248 (in Japanese). [2] T.S. Woodward, D.N. Bud, M.A. Hunter, Task switching deficits associated with Parkinson’s disease reflect depleted attentional resources, Neuropsychologia 40 (12) (2002) 1948 – 1955. [3] H. Tsuchiya, S. Yamaguchi, S. Kobayashi, Impaired novelty detection and frontal lobe dysfunction in Parkinson’s disease, Neuropsychologia 388 (5) (2000) 645 – 654. [4] A. Hozumi, et al., Perseveration for novel stimuli in Parkinson’s disease: a evaluation based on event-related potentials topography, Mov. Disord. 15 (5) (2000) 835 – 842.
www.ics-elsevier.com
Abnormalities of habituation and task switching in patients with Parkinson’s disease: an ERP study with frequent nontarget stimuli Junko Ito* Central Clinical Laboratory, Division of Neurophysiology, Kyoto University Hospital, 54 Shogoin Kawaracho, Sakyo-ku, Kyoto 606-8507, Japan
Abstract. To evaluate the effects of preceding stimuli, event-related potentials (ERPs) elicited by frequent nontarget stimuli (FNT) were studied in nondemented patients with Parkinson’s disease (PD) and healthy control subjects (Controls). Each stimulus, composed of two Japanese phonetic characters, was presented. Identical dhirakanaT characters (9%) were designated as target stimuli (Targets). FNT (73%) were composed of different dhirakanaT characters, and remaining stimuli were category-deviant nontarget stimuli (CDNT) composed of different dkatakanaT as well as phonetically task-relevant but category-deviant nontarget stimuli (RCDNT) composed of identical dkatakana.T Trials elicited by FNT were divided based on the preceding four stimulus types and averaged, respectively. ERPs elicited by FNT among the preceding four stimulus conditions were compared. Controls showed significant differences in N2 amplitudes, depending upon the preceding four stimulus conditions, whereas the PD patients did not show such differences. Regardless of the preceding stimulus conditions, the P3 components showed frontal maximal distribution, with larger P3 amplitudes for the PD patients than Controls. These findings suggest abnormalities of habituation and task-switching deficits resulting from depletion of attentional resources in PD patients. D 2004 Elsevier B.V. All rights reserved. Keywords: Parkinson’s disease; Frequent stimuli; Attention; Habituation
1. Introduction In a simple oddball paradigm, rare target stimuli elicit robust P3 components, but these components usually diminish in response to frequent nontarget stimuli (FNT) or standard * Tel.: +81 75 751 3658; fax: +81 75 752 3732. E-mail address: [email protected]. 0531-5131/ D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.ics.2004.11.105
326
J. Ito / International Congress Series 1278 (2005) 325–328
stimuli. During a go–no/go task in a category-deviant dual paradigm, P3 components in response to FNT were comparatively less attenuated in patients with Parkinson’s disease (PD) [1]. To evaluate the effects of preceding stimulus types and changes in information processing strategies, event-related potentials (ERPs) elicited by FNT were evaluated in nondemented PD patients. 2. Patients and methods Sixteen nondemented idiopathic PD patients (seven males and nine females; mean age, 63.1 years) and 15 age-matched healthy control subjects (Controls; six males and nine females; mean age, 63.9 years) participated in this study. All subjects were native speakers of Japanese. Informed consent was obtained from both patients and Controls. X-ray CT and/or magnetic resonance imaging showed no ischemic lesions in the PD patients. None of the PD patients showed evidence of a secondary cause of PD or any extraparkinsonian neurological impairment. Motor symptoms in PD patients ranged from Stage I to Stage III [I (2), II (8) and III (6)] on the Hoehn and Yahr scale. Two patients had motor symptoms localized on the right side, while the remaining patients had motor symptoms on both sides. At the time of testing, they were treated with levodopa/dopadecarboxylase inhibitors and dopamine agonist. None of the control subjects or PD patients had taken any other drugs that might have affected the ERP components. Scores on the Mini-Mental State examination showed no significant differences between the two subject groups (Controls 29.1F0.6; PD patients 28.6F0.8). There were no significant differences in depression scores between the two subject groups. Each stimulus, composed of two Japanese phonetic characters, was displayed in the center of a computer monitor. Identical dhirakanaT characters, comprising 9% of all stimuli, were designated as target stimuli (Targets). FNT (73%) were composed of different dhirakanaT characters, and remaining stimuli were category-deviant nontarget stimuli (CDNT; 9%) composed of different dkatakanaT characters, as well as phonetically taskrelevant but category-deviant nontarget stimuli (RCDNT; 9%) composed of identical dkatakanaT characters. Each stimulus, which varied from trial-to-trial, was presented for 400 ms, and interstimulus intervals were 1800F100 ms. Each run was composed of 140 stimuli, and five runs were presented to individual subjects. The subjects were instructed to press a button with their preferred hand in response to Targets (go) and disregard other stimuli (no-go). Speed and accuracy were equally emphasized. The recording arrangement consisted of G1 affixed to the Fz, Cz, Pz and Oz of the International 10-20 System and G2 affixed to linked earlobes. The electroencephalogram (EEG) was amplified with a band-pass filter of 0.05 to 60 Hz. The electrooculogram (EOG) was recorded from the left outer canthus and the right supraorbital region. Trials elicited by FNT in each run were averaged, and N2 and P3 components of ERPs were compared across runs. Trials elicited by FNT obtained from five runs were divided into four conditions, depending whether the preceding stimulus was Target, CDNT, RCDNT or FNT. N2 and P3 components obtained from averages for the preceding four stimulus conditions were compared. The N2 and P3 components were subjected to an analysis of variance
J. Ito / International Congress Series 1278 (2005) 325–328
327
Fig. 1. Comparison of grand averaged waveforms for Controls and the PD patients obtained from the first (thick lines) and fifth (thin lines) run.
(ANOVA) with the subject group (Controls, PD), preceding stimulus condition (Targets, FNT, CDNT and RCDNT) and electrode (Fz, Cz, Pz and Oz). The criterion for significance was less than 0.05. 3. Results P3 amplitudes obtained from the fifth run was significantly reduced compared with that obtained from the first run in Controls [ F(1,28)=28.72, p=0.00001] and in the PD patients [ F(1,30)=8.54, p=0.007], and the amplitude reduction was smaller for the PD patients[ F(1,29)=16.13, p=0.0004] (Fig. 1). Controls showed significant differences in N2 amplitudes among the four stimulus conditions [ F(3,60)=5.57, p=0.002], whereas the PD patients did not show such differences (Fig. 2). Regardless of the preceding stimulus, the P3 components showed frontal maximal distribution in both subject groups [ F(3,60)=7.13, p=0.0003], with the PD patients showing larger P3 amplitudes than Controls [ F(1,29)=5.85, p=0.022] (Fig. 2).
Fig. 2. Grand averaged waveforms elicited by FNT among the preceding four stimulus types that were recorded from Controls and the PD patients. Thick lines indicate ERP waveforms elicited by FNT following Targets, thin lines those following RCDNT, thinner lines those following FNT and thinnest lines those following CDNT.
328
J. Ito / International Congress Series 1278 (2005) 325–328
4. Discussion In the present paradigm, the subjects might have adopted a strategy involving simultaneous cognitive tasks, wherein the two characters were classified as dhirakanaT or category-deviant dkatakana,T and classified as different or identical and then decided whether to press the button or not. Moreover, each stimulus varied from trial to trial, so that subjects had to pay attention to each stimulus and change strategy from trial to trial. Deviance and discriminability of the preceding stimuli from FNT may have resulted in differences in the N2 amplitudes elicited by FNT among the four stimulus conditions in Controls. The lack of differences in the N2 amplitudes among the four stimulus conditions in the PD patients may have resulted from difficulty in changing strategy for information processing with each stimulus since PD patients have shown task-switching deficits resulting from depletion of attentional resources [2]. Rare dnovelT stimuli elicit a frontal maximal novelty P3 component [3]. Although stimulus probability was high, each FNT that varied from trial to trial was a dnovelT stimulus for the subjects. Thus, the P3 components in response to FNT were not so attenuated in the paradigm used for this study and showed frontal maximal distribution. The smaller P3 amplitude reduction from the first to the fifth run seen in the PD patients resulted from impairment of habituation. These findings are comparable with previous findings for PD patients that showed a lack of P3a habituation [4] and less habituation of novelty P3 component over the frontal scalp sites [3]. Thus, the larger P3 amplitude elicited by FNT in PD patients may be attributable to abnormalities of habituations resulting from the frontal lobe and basal ganglia dysfunction. References [1] J. Ito, Event-related potentials in Parkinson’s disease using category deviant and inhibition paradigm, Clinical Encephalography 43 (4) (2001) 243 – 248 (in Japanese). [2] T.S. Woodward, D.N. Bud, M.A. Hunter, Task switching deficits associated with Parkinson’s disease reflect depleted attentional resources, Neuropsychologia 40 (12) (2002) 1948 – 1955. [3] H. Tsuchiya, S. Yamaguchi, S. Kobayashi, Impaired novelty detection and frontal lobe dysfunction in Parkinson’s disease, Neuropsychologia 388 (5) (2000) 645 – 654. [4] A. Hozumi, et al., Perseveration for novel stimuli in Parkinson’s disease: a evaluation based on event-related potentials topography, Mov. Disord. 15 (5) (2000) 835 – 842.