This article was downloaded by:[Lachmann, Thomas]On: 28 February 2008Access Details: [subscription number 791040317]Publisher: Psychology PressInforma Ltd Registered in England and Wales Registered Number: 1072954Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Journal of Clinical and ExperimentalNeuropsychology Publication details, including instructions for authors and subscription information:Procedural learning eliminates specific slowing down ofresponse selection in patients with idiopathic ParkinsonsyndromeThomas Lachmann ab; Bettina Schumacher ac; Michael Joebges c; HorstHummelsheim c; Cees van Leeuwen b a University of Kaiserslautern, Kaiserslautern, Germany b Laboratory for Perceptual Dynamics, Brain Science Institute, RIKEN, Wako-shi,Japan c University of Leipzig, Leipzig, Germany To cite this Article: Lachmann, Thomas, Schumacher, Bettina, Joebges, Michael, Hummelsheim, Horst and vanLeeuwen, Cees (2007) 'Procedural learning eliminates specific slowing down of response selection in patients withidiopathic Parkinson syndrome', Journal of Clinical and Experimental Neuropsychology, 30:3, 319 - 326To link to this article: DOI: 10.1080/13803390701399278URL: This article maybe used for research, teaching and private study purposes. Any substantial or systematic reproduction,re-distribution, re-selling, loan or sub-licensing, systematic supply or distribution in any form to anyone is expresslyforbidden.
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JOURNAL OF CLINICAL AND EXPERIMENTAL NEUROPSYCHOLOGY2008, 30 (3), 319–326 Procedural learning eliminates specific slowing down
of response selection in patients with idiopathic
Parkinson syndrome
Thomas Lachmann,1,2 Bettina Schumacher,1,3 Michael Joebges,3
Horst Hummelsheim,3 and Cees van Leeuwen2

1University of Kaiserslautern, Kaiserslautern, Germany2Laboratory for Perceptual Dynamics, Brain Science Institute, RIKEN, Wako-shi, Japan3University of Leipzig, Leipzig, Germany Patients with idiopathic Parkinson syndrome and normally aged controls participated in a psychological refrac-tory period experiment. Two tasks were presented on each trial: auditory discrimination of high versus low tones,followed by visual classification of letters versus their mirror images. Speeded responses to both tasks wererequired. Stimulus onset asynchrony between the tasks was varied (short vs. long). Both groups showed equalresponse times overall, but patients were slower on the second task in the short stimulus onset asynchrony condi-tion. This effect was eliminated with practice. The results were interpreted in terms of reduced capacity for cogni-tive processes involving decision making as a secondary symptom of the Parkinson syndrome.
Downloaded By: [Lachmann, Thomas] At: 21:04 28 February 2008 The idiopathic Parkinson syndrome (IPS) has an ever, a number of studies have suggested consider- incidence rate of 1% of all over-65-year-olds in typ- ing cognitive deficits as well (see Brown & Marsden, ical western countries. Proteinaceous inclusion 1987, for an overview). General cognitive slowing bodies accumulate within neurons, leading to cell down (bradyphrenia) has been proposed (Naville, death in specific vulnerable areas. The process 1922; Smith et al., 1998) but such symptoms could advances in a predictable sequence to other areas.
also be attributed to normal aging (Phillips et al., During early stages, synuclein accumulations can 1999), dementia, or late-life depression (Butters be detected as precursors of the inclusion bodies in et al., 2004). Others have argued for more specific the medulla oblongata and olfactory bulb and later deficits (Sullivan & Sagar, 1989; Brown & in the substantia nigra. In addition, other nuclear Marsden, 1987), involving mainly two specific func- substances of the midbrain and basal forebrain are tions: visuo-spatial processing (Amick, Cronin- the focus of initially subtle and subsequently more Golomb, & Gilmore, 2003; Lee, Harris, & Calvert, severe changes. At this point the disease reaches its 1998; Natsopoulos, Bostantzopoulou, Katsarou, & symptomatic phase. Patients show rigor, hypo- Grouios, 1993; Pirozzolo, Hansch, Mortimer, kinesia, or tremor. During the end-stages, the Webster, & Kuskowsky, 1982; Proctor, Riklan, pathological progression encroaches upon the tel- Cooper, & Teuber, 1964; Taylor, Saint-Cyr, & Lang, encephalic cortex, and additional symptoms like 1986) and memory search (Ivory, Knight, Longmore, postural instability occur (Braak et al., 2002).
& Caradoc-Davies, 1999; Pirozzolo et al., 1982).
Parkinson (1817) originally considered IPS as an Regarding visuo-spatial processing: McDowell exclusively motor system disease. Since then, how- and Harris (1997), using questionnaires, found that Thanks are due to Max David from the Parkinson self-help group in Leipzig, to Steffen Huebner (Leipzig) and Andreas Widmann (Leipzig) for technical support, and to Daniel Tranel and anonymous reviewers for their helpful remarks on an earlier draft of thispaper.
Address correspondence to Thomas Lachmann, University of Kaiserslautern, Pfaffenbergstr. 103, 67663 Kaiserslautern, Germany 2007 Psychology Press, an imprint of the Taylor & Francis Group, an Informa business patients reported problems with depth and motion cessing task and study the effect of practice. To this perception but not with color, brightness, and aim we use the psychological refractory period shape perception. Lee et al. (1998) showed that IPS (PRP) paradigm (Szameitat, Lepsien, von Cramon, patients have impairments in mental rotation Sterr, & Schubert, 2006; Szameitat, Schubert, tasks, in which visuo-spatial representations have to be manipulated internally. Other experimental The PRP paradigm belongs to the family of studies, however, failed to find visuo-spatial orien- dual-task paradigms. Cognitive processing capa- tation problems in IPS patients (Hsieh, Hwang, city is limited, so when two tasks that require cent- ral processes are performed simultaneously, Regarding memory search, Appollonio et al.
performance is usually worse than when these (1994) and Breen (1993) found free-recall impair- tasks are performed independently (Telford, 1931; ment in IPS, whereas recognition memory was nor- Welford, 1952). When they are performed in rapid mal. Brown and Marsden (1987) and Flowers, succession, performance is degraded most when Pearce, and Pearce (1984) similarly found specific the difference between the onset of the first and deficits in memory retrieval. It was concluded that second task (stimulus onset asynchrony, SOA) is although patients were able to adopt adequate pro- minimal. These results are an effect of the central cessing strategies, they were less efficient in using information-processing bottleneck (Pashler, 1984; these (Breen, 1993). Press, Mechanic, Tarsy, and Pashler & Johnston, 1998; Welford, 1952), which Manoach (2002) investigated memory search in may be identified with the frontal system. Szameitat IPS patients using a classical Sternberg task et al. (2002) located PRP-related activity in (Sternberg, 1966). Multiple items are kept in mem- various frontal areas (inferior frontal sulcus, mid- ory, and participants must search for a given item dle frontal gyrus) and the intraparietal sulcus.
within this memory set. Linear increase in memory These brain areas were activated in a dual-task search time as a function of the number of items in situation but not when the tasks were performed Downloaded By: [Lachmann, Thomas] At: 21:04 28 February 2008 memory set is understood as memory search rate.
Press et al. (2002) found a slower memory search In the PRP bottleneck paradigm (Pashler, 1984, rate in IPS patients than in normal controls.
1994), the SOA is systematically varied with differ- Wilson, Kasniak, Klawans, and Garron (1980) had ent levels of a task complexity variable (e.g., previously found reduced retrieval rates in IPS Lachmann & van Leeuwen, 2007; Schwarz & patients. Posner, Walker, Friedrich, and Rafel Ischebeck, 2001). Priority is given to the first task.
(1984) failed to find such a difference, but reported To involve the central bottleneck, this task must a general increase in reaction time (RT).
require a decision (as in a choice response task), Visuo-spatial perception and memory retrieval but should otherwise be kept simple. Binary classi- studies both involve manipulating information fication of tones is typically used (Pashler, 1994).
internally in the service of guiding behavior. Such Central processing of the second task will have to central processes are typically a function of the wait until the bottleneck is cleared from the first frontal network (Taylor et al., 1986), which is lim- task. As a result RT increases with decreasing ited in its processing capacity. To alleviate its work- SOA. The waiting time for clearance, however, will load, proceduralization (Anderson, 1982) results in be equal for all these processes, independently of the formation of automatized behavioral routines their level of complexity. In a factorial design, this for efficient task execution. Deficits in procedurali- means that effects of SOA and central processing complexity will have additive effects.
for capacity limitations in IPS patients (Haaland, In contrast, processes prior to the central bottle- Harrington, O’Brien, & Hermanowicz, 1997; neck stage of the second task may overlap with the Pascual-Leone et al., 1993; Sommer, Grafman, bottleneck stage of the first task, without diminish- Clark, & Hallett, 1999). Press et al. (2002) found ing the rate of processing for either task. With that the reduction in memory search rate in IPS decreasing SOA, an increasing proportion of pre- patients disappeared after the first experimental bottleneck second-task processes will overlap. Thus, session. The authors suggested that there was a the complexity of these processes will increasingly delay in proceduralization of memory search.
be buried in the overlap if the SOA is diminished.
Our aim is to establish whether there is a delay in As a result, we would observe a subadditive inter- proceduralization in IPS patients in visuospatial action of second task complexity with decreasing processing. We investigate to what extent the involvement of the frontal system disappears with Thus, using the PRP paradigm allows us to dis- practice. To do so we need to show the involve- tinguish between perceptive, central-cognitive and ment of the frontal system in our visuo-spatial pro- motor processes for a given task. If there are RT differences between IPS patients and controls, the lack a task complexity variable, with which SOA PRP effects tell us why, where, and how. By look- could interact, as in the PRP bottleneck paradigm.
ing at practice effects, we may observe effects of In addition, they fail to provide us with data on Previous dual-task studies with IPS patients have yielded mixed results. Malapani, Pillon, EXPERIMENT
Dubois, and Agid (1994) found that IPS patientsperformed equal to controls on visual and auditory go/no-go tasks, but when the two tasks were pre-sented simultaneously the speed of performance in Participants
the former showed a greater drop than that in thelatter. This indicates that IPS patients find com- We recruited a total of 28 participants through plex decision making particularly hard. Other advertisement in the monthly magazine of a local studies supported this hypothesis (Brown & Parkinson self-help group. A total of 16 of them Marsden, 1991; Dalrymple-Alford, Kalders, Jones, were in the patients group (experimental group), 10 & Watson, 1994; Fournet et al., 1996; Horstink, of whom were females. Average age in this group Berger, van Spaendonck, van den Bercken, & was 66 years, ranging from 52–75. Patients’ IPS Cools, 1990; Robertson, Hazlewood, & Rawson, diagnosis was validated by experienced neurolo- gists specialized on the area of IPS, according to In contrast, Hein, Schubert, and von Cramon brain bank criteria. The Hoehn and Yahr state of (2005) found no greater drop in performance in all patients was diagnosed as between 2.0 and 2.5.
IPS patients than in normal controls when two Duration of illness, medication, and laterality of tasks were presented close in time. Similarly, the patients are reported in Table 1. According to Hsieh (2000) presented two tasks with an SOA of Press et al. (2002), medication, and its correspond- Downloaded By: [Lachmann, Thomas] At: 21:04 28 February 2008 50, 150, or 650 ms. The first task was a tone dis- ing dopaminargic state, has no influence on the crimination task, the second a digit identification performance in a typical RT task, such as memory task (replication of Pashler, 1989). She found increased RT and error rates for the first task. For Participants of the control group were 12 family the second task she found increased RT for IPS, members of the patients, 8 of whom were females.
but no interaction with SOA. Hsieh concluded Average age was 67 years, ranging from 52–81.
that extra motor execution time might have pro- Participants in the control group were selected for duced the group main effect. The main problem reporting no history of neurological disorders and with all these experiments, however, is that they not receiving any psychopharmacological drugs.
Description of the patients with IPS participating in the experiment Note. IPS = idiopathic Parkinson syndrome. F = female, M = male.
aIn years. bIn mg.
Patients and controls received 10 euros for their respond to the tone first and that, although both participation. All participants had normal or cor- tasks were important, they should focus on rected-to-normal seeing and hearing abilities. An responding to the tones. At the beginning of a trial, interview was held prior to the experiment with a fixation cross was shown for 300 ms in the center all participants to assure normal intelligence and of the screen, followed by a tone. High or low to exclude ailments such as acute untreated tones were used with equal frequency in the experi- depression or other psychiatric or psychological ment. The visual stimulus was presented with illnesses that might influence the level of cognitive either a short (50-ms) or long (400-ms) SOA. Vis- ual stimuli were shown until the response occurred.
All stimuli occurred with equal frequency within Stimuli
the experiment. Whenever participants failed torespond to the tone within 1,600 ms, the text: Tones were presented for 33 ms at either 900 “Please respond faster to the tone!” appeared on (high) or 300 Hz (low) using standard sound card the screen in addition to the feedback. If the and speakers. The letters F, R, g, and their mirror response time in the first 16 trials was above 1,600 images were presented visually. Letters were com- ms on average, the program was interrupted posed of straight-line segments drawn on a 5-cm briefly, and a full-screen text appeared: “Please try (horizontal) by 7-cm (vertical) grid and were dis- to be a bit faster! Average response time to the played on a 14-inch standard PC monitor. The vis- tone: [e.g., 1,892] ms.” When a response to a tone ual angel was about 5° horizontally and about 6.5° was given faster than 200 ms, the sentence: “Please vertically. There was no fixation of the partici- do not guess the tone!” appeared. No feedback was given for correct responses. The next trial started2 s later.
A total of six blocks of 24 trials was presented, in Downloaded By: [Lachmann, Thomas] At: 21:04 28 February 2008 Participants were seated at 60-cm distance from which equal numbers of long and short SOA trials the monitor in a sound-attenuated and darkened were randomly intermixed. Halfway through and room. They were instructed to rest their hands on a at the end of each block participants were offered wooden panel, 50 cm long, which contained four an optional short break. After each block they response keys, two on the left-hand side and two received feedback on their within-block average on the right-hand side, one next to each other. As response times and percentages correct on both keys, 7.5 × 7.5-cm standard light push-buttons were used. The keys on the left side contained thelabels “high” and “low.” The keys on the right side contained the labels “normal” and “mirrored.” Participants started with a 25-trials training ses- Individual mean response times and error rates sion of the auditory discrimination task, for which were positively correlated in the first task (R = they were instructed to respond as fast and accu- .586, p < .01); in the second task no correlation was rately as possible depending on whether the tone presented was “high” or “low,” using the responsekeys on the left-hand side. Subsequently they were Task 1: Auditory classification
trained for 30 trials on the letter discriminationtask. There, in each trial a fixation cross appeared The overall mean RT was 946 ms (SD = 504), for 300 ms prior to the presentation of a letter in and the mean error rate was 8.6%. Analysis of var- the center of the screen. Participants were iance (ANOVA) on RT, with factors group (IPS instructed to respond as fast as possible whether vs. control) as between-subjects factor and SOA the letter presented was “normal” or “mirrored” (long vs. short) and reflection (normal vs. mirrored by using the response keys on their right-hand side.
items in the second task) as within-subjects factors, Speed and accuracy feedback were given during resulted in a main effect of SOA, F(1, 26) = 51.88, the training sessions. Following a correct trial, the p < .001. Performance was weaker with short response time in ms was briefly presented in green; (1,018 ms, SD = 550) than with long SOA (877 ms, following an incorrect response, the time was given SD = 444), and for reflection, F(1, 26) = 8.725, p < in red. Feedback on the auditory task was given in .01, faster for normal (925 ms, SD = 483) than for the lower left corner of the screen, on the visual mirrored letters (967 ms, SD = 523). The interac- task in the lower right corner of the screen.
tion of SOA and reflection reached significance, After training participants were instructed to F(1, 26) = 5.10, p < .05; for short SOA, normal let- perform both tasks together. They were told to ters yielded 977 ms (SD = 507), mirrored 1,060 ms (SD = 588), and for long SOA, normal letters independent process. The other interaction is that yielded 874 ms (SD = 453) and mirrored 879 ms of Reflection × SOA, F(1, 26) = 9.29, p < .001. Fig- (SD = 436). Thus, the interaction is based on the ure 2 shows that for short SOA, normal letters are restriction of the effect of reflection to short SOA.
faster (1,719 ms, SD = 722) than mirrored (1,885 For group, (F = 0) no other effect approached sig- ms, SD = 889) but not for long SOA. The direction nificance. The same analysis on error rates yielded of this interaction, too, is opposite to what would have been expected from an automatic, bottleneck-independent process.
The same analysis on error rates resulted in a Task 2: Visual classification
main effect of group, F(1, 26) = 5.268, p < .05— The mean RT for the second task was 1,564 ms more errors were made in the patients group (SD = 770 ms), and the mean error rate was 7.6%.
(9.9%) than in the control group (4.5%)—and of ANOVA on RT, with factors group (patients vs.
SOA, F(1, 26) = 7.808, p < .05—more errors were controls) as between-subjects factor and SOA and made for short (8.8%) than for long SOA (6.4%).
reflection as within-subjects factors, resulted in No interactions reached significance.
main effects for SOA, F(1, 26) = 268.37, p < .001, The present study involves many trial repeti- with faster responses for long (1,336 ms, SD = 649) tions. It is therefore possible to investigate the than for short SOA (1,801 ms, SD = 813), and for question of whether practice can remedy the spe- reflection, F(1, 26) = 11.10, p < .005, with faster cific deficit in IPS patients. To study this question, responses for normal (1,522 ms, SD = 718) than the complete session was divided into four practice for mirrored letters (1,607 ms, SD = 817). No main stages (I–IV). An ANOVA with factors group, effect of group was obtained (F < 1; controls = 1,527 SOA, and practice resulted in main effects of SOA, ms, SD = 685; patients = 1,595 ms, SD = 833).
F(1, 26) = 296.3, p < .001, and practice, F(3, 78) = Two interactions reached significance. Figure 1 53.30, p < .001. The first result duplicates that of Downloaded By: [Lachmann, Thomas] At: 21:04 28 February 2008 shows the interaction Group × SOA, F(1, 26) = the first analysis; the second shows that practice 5.36, p < .05. Patients (1,861 ms, SD = 905) were leads to improvement in both groups. As before, slower than controls (1,727 ms, SD = 677) for there was no group main effect. Significant interac- short SOA but not for long SOA. The direction of tions were obtained of Group × SOA, F(1, 26) = the interaction is opposite to what would have 4.69, p < .001, of SOA × Practice, F(3, 78) = 5.00, resulted if the difference between the two groups p < .005, and a triple interaction of Group × SOA had been based on an automatic, bottleneck- × Practice, F(3, 78) = 2.99, p < .05.
Figure 1. Interaction of group and stimulus onset asynchrony
Figure 2. Interaction of reflection and stimulus onset asyn-
(SOA); reaction times (RTs) and 95% confidence interval of chrony (SOA); reaction times (RTs) and 95% confidence inter- IPS patients versus controls on the secondary mirror image task val for normal versus mirrored letters on the secondary task for short (50-ms) and long (400-ms) SOA between the first and for short (50-ms) and long (400-ms) SOA between the first and Post hoc analyses showed that the effect of SOA times with mirrored than with normal letters), a remained in all practice stages separately, F(1, 26) = complexity variation of the second task, on the 68–226, p < .001. An interaction of Group × SOA, response times of the first task when SOA between however, was found in Practice Stage I, F(1, 26) = the two tasks is short. With long SOA between 5.76, p < .05, but not in any of the subsequent these tasks, such cross-talk does not occur.
stages (see Table 2 for detailed data information).
In the second task, IPS patients made more The same ANOVA was run on error rates.
errors than did controls, but showed no differences Main effects were found for SOA, F(1, 26) = overall in response times. For RT an interaction 8.95, p < .01, and group, F(1, 26) = 5.47, p < .05, between SOA and reflection was obtained; higher duplicating former results, and for practice, F(1, RT for mirrored letters than for normal letters was 26) = 4.07, p < .05, with decreasing error rates only found in the short SOA condition, whereas with practice in both groups (see Table 2 for there were no effects in the long SOA condition.
detailed data information). No interactions were Had this pattern of interaction been opposite (big- ger effect for long SOA), this would mean evidencefor automatic processing of reversed letters. The Discussion
present result, however, suggests that letterreversal involves the central bottleneck, equally in Patients with IPS and age-matched controls per- both groups of participants. This result indicates formed a dual-task experiment using a PRP para- that, in accordance with Ruthruff, Miller, and Lachmann (1995), the central bottleneck is classification, the second task visual classification involved in visuo-spatial manipulations (such as of normal versus mirrored letters. For the first task, no group differences were obtained. Equally IPS patients and normal controls showed no dif- in the two groups, both the first and second task ference in overall performance on the second task, Downloaded By: [Lachmann, Thomas] At: 21:04 28 February 2008 showed main effects of SOA. This means that a contrary to the notion of general cognitive slowing bottleneck has occurred in this experiment. At present, the debate is still on about whether limited The IPS patients, however, were showing spe- capacity resources of the bottleneck are allocated cific cognitive slowing down when the SOA in an all-or-none fashion (Pashler, 1984, 1989; between the first and second task was short. If this Welford, 1952), or whether capacity sharing were caused by primary motor symptoms of the between tasks is allowed (Navon & Miller, 2002; disease, this would have occurred in both SOA Tombu & Jolicoeur, 2002). When there are effects conditions. IPS patients, therefore, may find it par- of SOA on both tasks this implies, according to the ticularly difficult to combine overlapping decision logic of the PRP paradigm, that resource sharing has taken place between the first and second task.
With practice, the effect of SOA was reduced in In other words, the limited capacity has not been both groups. Proceduralization means that both devoted exclusively to the two tasks in sequence, tasks can be executed more efficiently together. In but has been divided over the tasks, resulting in a accordance with Press et al. (2002), we may ascribe slowing of both. In accordance with this explana- the initially weaker performance in IPS patients to tion, there is an effect of reversal (longer response lack of proceduralization. Performance of IPS Reaction times and error rates for different SOA levels in controls and Parkinson patients for different levels of practice Note. IPS = idiopathic Parkinson syndrome. SOA = stimulus onset asynchrony. Reaction times in ms. Error rates in percentages.
patients approached that of the controls already in medicated Parkinson’s disease patients: The cent- after about the first 25% of the trials within a sin- ral executive seems to work. Journal of Neurology, Neurosurgery and Psychiatry, 60, 313–317.
Haaland, K. Y., Harrington, D. L., O’Brien, S., & Not only is it difficult to assess cognitive deficits Hermanowicz, N. (1997). Cognitive motor learn- in Parkinson patients, it is also possible that they ing in Parkinson’s disease. Neuropsychology, 11, reflect secondary symptoms, resulting from a vicious circle of lack of practice, lack of confid- Hein, G., Schubert, T., & von Cramon, D. Y. (2005).
ence, and avoidance behavior in performing cer- Closed head injury and perceptual processing in dual-task situations. Experimental Brain Research, 160, tain tasks, and depression. The currently observed deficit may be in fact such a secondary symptom.
Horstink, M. W., Berger, H. J., van Spaendonck, K. P., Let this be so; the value of the present study is that van den Bercken, J. H., & Cools, A. R. (1990).
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