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RESPONSE SLOWING OF PARKINSONIAN PATIENTS UNDER AUDITORY DISCRIMINATION TASKS


D. Philipova*, S. Georgiev*, I. Milanov**, D. Bogdanova**, W. Wolf*** Institute of Physiology, Bulgarian Academy of Science, Sofia 1113, Bulgaria* University Neurological Hospital, Movement disorders department, Sofia1113, Bulgaria** University AF Munich, Department of Informations techniques and Electrical Engineering*** Response slowing of parkinsonian patients under auditory discrimination tasks D. Philipova, S. Georgiev, I. Milanov, D. Bogdanova, W. Wolf Homeostasis 44, 3, 2006 Impairment of movement execution in Parkinsons disease patients (PPs) could be due to disorders of cognitive and /or motor information processing. One appropriate noninvasive method for assessing cognitive information processing at central brain level is the investigation of event related potentials (ERPs), especially the late cognitive P3 component (Sutton 1965). A choice reaction task involves the evaluation of a stimulus, the selection of an appropriate response and then programming and executing of the movement. The aim of our work was to investigate the role of central (sensorimotor and cognitive) information processing disturbances in the organization of voluntary movement performance in Parkinsonian patients in the early stages of the disease. Method: The acoustic event related potentials (ERPs) reflecting the central processes (recorded from Fz, Cz, Pz, C3 and C4), the force profile as the peripheral (effector) signals and the electromyographic activity pattern of the first dorsal interosseus muscles were recorded simultaneously in reaction time (RT) experiments. A response locked lateralized readiness potential (LRP) indicating the differential activation processes of the contralateral motor cortex was defined as the difference C3 C4 for right hand responses and C4 C3 for left hand responses. PPs and control subjects (CS) operating a force key with the index finger of each hand were asked to make rapid and accurate choice responses with the left or right hand to a high frequency (1000 Hz) or low frequency (800Hz) tone respectively. Results and conclusion: The behavioural responses (RT) of PPs were slower than those of healthy adults of similar age; significant force peak latency differences and response force duration differences were found between the two groups. PPs also displayed a delayed onset of response-locked LRP and exhibited lower P2 and P3 amplitudes at the Fz position. The results here confirm the presence of qualitative differences between PP and CS in the processing of stimulus information when performing sensomotor tasks which suggest that both cognitive and motor information processing are relevant to the impairment of movement execution in Parkinsons disease. Keywords: Parkinsons disease, Event-related potentials (ERPs), Lateralized readiness potentials (LRP), reaction time, cognitive processing INTRODUCTION Investigation of event related potentials (ERPs) has been widely used as an appropriate noninvasive method in scientific study for researching sensory and cognitive information processing at a central brain level in both healthy persons and in neurological patients (Vieregge et al. 1994, Philipova et al. 1998, Robertson, 1999, Montirosso 2002, Philipova et al. 2004 etc.). Of the various ERP waveforms, the P1, N1 and P2 compoHomeostasis, 44, 2006, No 3 109

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nents are considered to be indices of the early processing stages (automatic or obligatory) after stimulus delivery, while N2 and P3 reflect the later cognitive processes. The main cognitive P3 component (Sutton et al. 1965) requires an intact temporo-parietal junction and is thought to be linked with processes such as attention, learning, memory and decision-making capacity (Donchin and Coles, 1988, Ullsperger and Grune 1995, Verleger 1988, Hruby, Marsalek 2003). P3 latency is considered to be a measure of stimulus classification speed and increases with a decrease of cognitive capability. P3 amplitude is considered to reflect brain activity that is required in the maintenance of working memory and in the updating of a mental model of the stimulus environment. The lateralized readiness potential (LRP), a slow negativity that emerges up to one second before voluntary movement onset and rises over central scalp sites, reflects the increasing of the contralateral EEG activity and it is regarded as a hand specific response preparation. The LRP is defined as the average brain activation difference, contralateral minus ipsilateral, relative to the responding hand. Brain disorders that affect these processes can influence ERP component parameters by changing their amplitude or latency. One integrative behavioural indicator including sensory and cognitive central neurosystem processing as well as the organization of motor action and the effectiveness of performance is the reaction time (RT). In recent years, there has been a growing interest in the role of the basal ganglia (BG) as the integrating centre for sensory and cognitive processing of information and the relationship between this processing and movement. Parkinsons disease causes neurodegeneration of dopaminergic neurons within substantia nigra, pars compacta. Current knowledge of the functional role of BG in humans is based mainly on investigations of Parkinsonian patients (PPs) as a natural model of BG disturbances (Franz, 2002). There is no clear link between the observed symptoms, which include difficulty in movement initiation and execution, changes in reaction time in sensorimotor tasks and cognitive information processing in PPs. PPs very often exhibit a significant delay in RT compared with healthy persons (Evarts et al. 1981, Bloxham et al. 1984, Sheridan et al. 1987, Cooper et al. 1994, Low et al. 2002 etc.). Impairment of movement execution in Parkinsons disease patients could be due to disorders of either cognitive and/or motor information processing. The aim of our present study was to investigate the role of central (sensorimotor and cognitive) information processing disturbances in the organization of voluntary movement performance in Parkinsonian patients in early stages of the disease. Our hypothesis is that destructive processes of basal ganglia lead to disturbances in cognitive and sensorimotor information processing. METHOD Twelve idiopathic non-demented PPs (10 female, 2 male, mean age= 64 years, range 3478 years, exhibiting tremor-rigid forms in the early stages of disease for an average duration 2.8 years) and thirteen healthy volunteers matched for age, sex and education participated in the study. Excluding factors were the presence of arthereosclerosis, dementia, hearing impairment, attendant neurological complications or pronounced tremor. Informed consent was obtained after an explanation of the nature and procedures of the experiments was given. Each subject was comfortably seated in an ergonomically designed chair within a sound-proof, electrically screened chamber which could be monitored by a Canon Video System. The hand and forearm were positioned along the armrests. The index finger was immobilized within a rigid rail attached to a pull-push force transducer such that the output signal was proportional to the isometric force produced. Verbal contact was supported via an intercom system. 110 Homeostasis, 44, 2006, No 3

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An electroencephalogram (EEG) was recorded from Fz, Cz, Pz, C3 and C4 using Ag/AgCl Nihon-Kohden electrodes with reference to both processi mastoidei according to the system 1020. An electrode placed on the forehead served as ground. An oculogram (EOG) was recorded from m. orbicularis oculi dex. Electromyogram (EMG) was recorded from m. inrerosseus dorsalis I dex. and sin. using surface electrodes. EEG (bandpass filtered between 0.370 Hz), EOG and EMG (bandpass filtered between 0.03500 Hz) data were recorded using a Nihon-Kohden polyphysiograph. All signals were stored on computer disc for later off-line analysis. Computer programmes were used to determine and calculate the peak latency and amplitudes of the N1, P2, N2 and P3 components. ERP latencies were measured in ms from the stimulus onset to the wave peak and the amplitude values were determined base to peak. The processing period was 1024 ms including a prestimulus interval of 200 ms, and a resolution of 4 ms. The averaged brain potentials for the tone stimuli were processed selectively from the series from the Fz, Cz, Pz, C3 and C4 records and with regard to tone frequency. A response locked lateralized readiness potential (LRP) indicating the differential activation processes of the contralateral motor cortex was defined with respect to 500 ms before and 500 ms after EMG onset as the C3 C4 difference for right hand responses and the C4 C3 difference for left hand responses. Onset of the LRP was determined in MATLAB on the basis of individual averages by fitting two lines by using a least squares method (see. Mordkoff & Gianaros, 2000). In this report we present only the comparison between CS and PPs of response locked LRP onset. (The LRP data will be object of another report). 100 computer generated acoustic stimuli 1000 Hz (high frequency) and 800 Hz (low frequency) tones with an acoustic intensity of 60 dB, duration of 50 ms and an interstimulus interval of 2.5 3.5 s were presented to the subjects in a randomized order. After a short practice period, the subject participated in a section of 100 trials each a passive series (passive listening without any task) and a sensomotor task series. The subjects were asked to respond as quickly as possible by depressing the relevant key with their index finger (with the left hand in response to a high frequency tone and with the right hand in response to a low frequency tone). No explicit instructions were given to the participants regarding response force. The following parameters of movement execution were defined: 1. Motor reaction time from stimulus presentation to the onset of voluntary force production. 2. Force peak latency from stimulus presentation to the force peak. 3. Response force duration from the force onset to the force end. 4. Execution time from stimulus onset to the movement end. 5. Force peak amplitude. A computer program was used to perform Mann-Whitney U-test statistical processing. RESULTS The evoked potentials recorded1 in the patient group could be classified into normal potentials and into potentials with diminished components. No latency differences for N1, P2, N2 or P3 were found in either the passive or task series between the CS and PPs in response to the low or the high tone.

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In both passive and task series, we found a lower mean group value for some of the ERP components in PPs. (Tabl. 1, Fig. 1. Fig. 2) We found lower P2 amplitude in PPs in passive series and task series. In passive series, the difference for the low tone for P2, Cz, was significant p<0.006, U=21; P2, C3 p<0.03, U=16; P2, C4 p<0.008, U=23, P2; Pz low tone p<0.014, U=26.

Fig. 1. Grand average ERP waveforms for Fz, Cz, Pz, C3, C4 in passive series in healthy persons (thin lines) and Parkinsonian patients (thick lines).

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For the high tone, the difference for P2, Fz was significant p<0.04, U= 29; P2, Cz p<0.007, U=22; P2, C3 p<0.02, U=14; P2, C4 p<0.007, U=22; P2, Pz p<0.014, U=26. In the task series we found lower P2 component in PPs in response to the low and high tones. The P2 difference was prominent in answer to the high tone for C3 p<0.02, U= 17; C4 p<0.03, U=38. For P2, Fz 0.05<p<0.1, U=38. For the low tone, P2 difference did not reach statistical significance.

Fig. 2. Grand average ERP waveforms for Fz, Cz, Pz, C3, C4 in sensomotor task series in healthy persons (thin lines) and Parkinsonian patients (thick lines).

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Table 1. Mean amplitude parameters of ERP components in V

PASSIVE SERIES
[V] Fz HIGH TONE [V] Fz HIGH TONE [V] Fz LOW TONE [V] Fz LOW TONE N1 P2 -12.01 1.03 3.24 1.25 N1 P2 -13.19 1.01 5.51 0.95 N1 P2 -11.27 0.9 * 2.43 1.31 N1 P2 -11.71 1.076 0.85 HEALTHY PERSONS Cz -13.52 1.17 ** 9.70 0.95 Cz -10.56 1.24 ** 5.60 0.82 HEALTHY PERSONS Cz -14.14 1.06 **10.47 1.10 Cz -10.85 1.55 ** 6.72 1.10 Pz -9.25 0.97 ** 8.77 1.04 Pz -6.88 1.14 ** 5.13 1.12 C3 -12.79 1.29 * 8.33 0.58 C3 -11.08 1.62 * 4.66 1.29 C4 -12.73 1.01 ** 7.30 0.91 C4 -11.33 1.45 ** 5.08 1.18 Pz -8.68 1.19 ** 7.74 0.83 Pz -6.40 0.91 ** 4.26 0.68 C3 -12.52 1.48 ** 7.94 0.61 C3 -11.19 1.10 ** 3.46 1.09 C4 -11.61 1.04 ** 7.18 0.80 C4 -10.50 1.67 ** 4.35 1.06

PARKINSONIAN PATIENTS

PARKINSONIAN PATIENTS

SENSOMOTOR TASK SERIES


[V] Fz LOW TONE N1 P2 N2 P3 [V] Fz N1 LOW TONE [V] Fz HIGH TONE N1 P2 N2 P3 [V] Fz HIGH TONE N1 P2 N2 P3 -12.95 0.97 0.80 1.03 -3.34 0.99 ** 1.82 0.53 -13.12 1.57 4.00 0.96 0.52 1.06 ** 5.27 1.15 P2 N2 P3 -12.12 0.92 2.09 1.17 -2.61 1.20 2.85 0.73 -13.34 1.30 3.36 0.66 -1.07 0.95 4.41 1.24 HEALTHY PERSONS Cz -15.38 1.48 5.53 1.06 -1.43 1.40 4.15 1.41 PARKINSONIAN PATIENTS Cz -11.62 1.21 3.54 1.77 -2.46 1.61 2.22 1.54 HEALTHY PERSONS Cz -14.81 1.70 5.87 1.16 0.44 1.24 5.11 1.19 Cz -11.32 1.32 2.62 1.69 -2.39 2.00 0.95 1.67 PARKINSONIAN PATIENTS Pz -6.66 0.99 3.22 0.82 -1.58 1.07 4.37 1.26 C3 -12.37 1.26 ** 0.86 1.35 -3.44 1.17 1.02 0.69 C4 -11.96 1.56 * 1.47 1.39 -4.15 1.06 * 0.63 0.97 Pz -9.86 1.42 5.14 1.37 0.43 1.10 6.29 1.29 C3 -13.00 1.38 ** 4.98 1.11 -0.13 0.91 3.86 0.85 C4 -12.37 1.64 * 5.06 1.37 0.64 1.07 * 3.83 1.40 Pz -7.34 0.85 4.84 0.90 -1.13 1.17 4.88 1.14 C3 -12.09 1.35 3.45 1.25 -3.76 1.18 1.02 1.19 C4 -11.84 1.24 3.48 1.37 -2.74 1.21 2.62 1.34 Pz -10.58 1.32 6.20 1.15 -0.01 1.27 4.54 1.15 C3 -13.31 1.17 4.92 1.16 -1.20 1.44 3.40 0.93 C4 -12.48 1.35 3.64 0.88 -0.53 1.12 3.68 1.32

0.1>p>0.05 * p<0.05 ** p<0.02 *** p<0.005

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The ERP investigation data showed the fronto-central P3 amplitude diminishing in PP, particularly in the Fz record. Significant P3 differences between CS and PPs were found to be P3, Fz, high tone, p<0.003, U=21; P3, C4 high tone, p<0.03, U=37. For the low frequency tone, P3 amplitude was lower in PPs but the difference did not reach significance. P3 amplitude at the Pz position appeared to be unaffected by the disease. We found that the onset of LRP negativity occurred later in PPs in comparison with healthy persons 153 22 ms in CS and 75 45 ms for PPs (right hand LRP, p<0.02, U=20) and 114 41 ms for CS and 33 29 for PPs (left hand LRP, p<0.04, U=14.5)

Fig. 3. Grand average LRP waveforms in healthy persons (thin lines) and Parkinsonian patients (thick lines).

Response parameters: Subjects with Parkinsons disease had slower reactions compared with healthy subjects. The time between stimulus and force onset (motor reaction time) was delayed in PPs with significant differences between the two groups for the right hand (p<0.044, U=41). The difference for the force peak latency was significant between the two groups for both the right hand and the left hand (p<0.01, U=28 and p<0.002, U=22 respectively). The response force duration was significantly delayed in patients for the left hand (p<0.022, U=36) but for the right hand the difference did not reach statistical significance.. Execution time (the time from stimulus onset to the end of movement) was significantly longer in patients for both the left hand (p<0.002, U=22) and the right hand (p<0.01, U=29). The rate of force exertion varied and we did not find any significant difference between the two groups. Also the error differences were not significant between groups. (Tabl. 2, Fig. 4).

Fig. 4. EMG and response parameters: a) healthy person b) Parkinsonian patients.

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DISCUSSION The present study was carried out to evaluate motor and cognitive processing in Parkinsons disease patients. Our investigation revealed reduced amplitudes for P2 and P3 components in patients, delayed onset of response locked LRPs and global differences between healthy persons and PPs for most response parameters. Investigation of ERP components allows analysis of different aspects of information processing functions. The evaluation of the time of sensory analysis processes by N1 and P2 latency and the time of classification and discrimination of the stimuli by N2 and P3 latency did not show any significant differences between the two groups. This data is in accordance with the data of Prasher and Findlay,1991, Vieregge et al. 1994 and suggests that the prolongation of response parameters in patients under our experimental conditions is not associated with any prolongation of central sensory analysis and discrimination processing time. We found that cognitive speed concerning stimulus classification and discrimination is not affected in PPs. The lower P2 amplitude in patients in comparison with healthy persons can probably be attributed to a more expressed orienting reaction in healthy volunteers. It is known that the P3 component has a multigeneratory origin including temporoparietal junctions and the hippocampus. Hippocampal atrophy has been demonstrated in PPs. The ERP investigation data showing fronto-central P3 amplitude diminution in PPs, particularly in the Fz record, are in line with our previous investigations, Philipova et al. 1997, Philipova et al. 2005 and with some of the data in the literature which indicates arousal differences between the two groups and an impaired activation, predominantly of the frontal lobe, in patients (Stam et al.1993, Botzel et al. 1995). The qualitative differences in the stimulus information processing and frontal lobe dysfunction are in accordance with reported neurophysiological (Piccirili et al. 1989, Taylor et al. 1990) and cerebral blood flow studies (Bes et al. 1983) in Parkinsonian patients.
Table 2. Response time parameters in ms
HEALTHY PERSONS Means [ms] Low Tone High Tone Means [ms] Low Tone High Tone MRT 419 25 * 410 23 MRT 509 37* 494 41 FPL 680 31** 677 33*** FPL 934 72 ** 898 63*** RFD 559 50 542 36* RFD 713 68 747 80* ET 958 51** 952 46*** ET 1223 68** 1206 60***

PARKINSONIAN PATIENTS

0.1>p>0.05 * p<0.05 ** p<0.01 *** p<0.005

The behavioural responses (RT) of PPs were slower than those of healthy adults. Staude et al. 1995 showed the prominent tremor to be a factor in the prolonged RT of PPs. Our patients had mild to moderate Parkinsons disease and most of them demonstrated a slight tremor during responding. Some authors interpreted a prolonged RT as deficits in utilizing advanced information during movement selection and initiation (Evarts et al. 1981, Bloxham et al. 1984, Sheridan et al. 1987 etc.). A choice reaction time task includes identification and evaluation of a stimulus, selection of the appropriate response and programming and executing the movement. For better evaluation of the processes responsible for the slowing of performing the response, we used an investigation of response locked LRPs in view of the fact that the onset of LRPs marks the 116 Homeostasis, 44, 2006, No 3

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beginning of hand specific central motor activation. The received data showing the delay of the onset of response locked LRP reveal that the longer RT in PPs is associated with central motor slowing. We did not find a lower level of force output in patients; unlike the data of Wascher et al. 1997 and Franz, Miller 2002. The different results appear to be dependent on disease form, the lack of explicit instruction to the participants regarding response force, the task and experimental conditions. Taken as a whole, the data obtained confirms the presence of qualitative differences between healthy persons and PPs in early stages of the disease in the processing of stimulus information during the performance of sensorimotor tasks. The results confirm the role of the basal ganglia as an integrating centre for sensory and cognitive information processing and the fact of a relationship between this processing and impairment of movement in PPs. ACKNOWLEDGEMENT The research was supported by National Science Fund grant L 1413, 20042007 REFERENCES
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Presented at CIANS Conference, Milan, Italy, June 1718, 2006

Address for correspondence: Assoc. Prof. Philipova, D., MD, PhD Institute of Physiology, Bulgarian Academy of Science, Acad. Bonchev str., bl.23, Sofia 1113, Bulgaria* E-mail: dolja@iph.bio.bas.bg

EARLY INTERVENTION IN PSYCHOSIS: PREVENTION OPPORTUNITIES de Girolamo G.: The first-ever hospital admission: the need of early interventions Lasalvia A., Ruggeri M., Bertani M., Bonetto C., Bissoli S., Marrella G., Cristofalo D., Tansella M.: The Psychosis Incident Cohort Outcome Study (PICOS). A survey on new cases of psychoses in the Community Mental Health Services of the Veneto Region, Italy. Hrrmann F., Maurer K., Hfner H. ERIraos: An instrument for the identification of at risk mental states. Presentation of the instrument and first results Meneghelli A., Caprin C., Cocchi A.: Assessing initial phases of psychosis: the PROGRAMMA 2000 strategy Galvan F., Pisano A., Cocchi A.: Preventing social deterioration in the first phases of psychosis. The SIS (Social Integration Support) project. Ponteri M., Meneghelli A., Cocchi A.: Subjective Quality of Life for Subjects at Risk and First Episode Psychosis: One Year Follow-Up in an Early Intervention Individualized Program

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