Speed of Elementary Visual Recognition Operations in

* The present research was conducted with the support from Estonian Science Foundation Grant No. 885.Address correspondence to Talis Bachmann who is now at the Department of Psychology, University ofPortsmouth, King Henry Building, Portsmouth PO1 2DY, Hampshire, UK. E-mail: [email protected] for publication: November 29, 1997.

Journal of Clinical and Experimental Neuropsychology 1380-3395/98/2001-118$12.001998, Vol. 20, No. 1, pp. 118-134 © Swets & Zeitlinger

Speed of Elementary Visual Recognition Operations inParkinson’s Disease as Measured by the Mutual Masking

Method*

Talis Bachmann1, Toomas Asser2, Mari Sarv1, Pille Taba2, Ene Lausvee1, Endel Põder1, NeemeKahusk1, and Tarmo Reitsnik2

1 Laboratory of Cognitive Neuroscience, Tallinn University of Social and Educational Sciences, Tallinn,Estonia and2 Department of Neurology & Neurosurgery, University of Tartu, Tartu, Estonia

ABSTRACT

Pairs of mutually different, spatially overlapping letters were exposed for recognition to groups of patientswith Parkinson’s disease (PD) and the age-matched control group. Stimulus onset asynchrony (SOA),medical treatment status (de novo vs. treated), and predominant symptoms (tremor vs. hypokinetic rigidity)were an other main variables. The highly significant main effects of SOA and health status demonstratedslowing of elementary visual recognition operations in Parkinson’s disease; the results are based on theexperimental method that requires neither fast manual responses nor tracking of the display events bysaccadic eye movements. Significant interaction between the temporal order of stimulus exposure andhealth status showed that impairment due to PD was more pronounced for the first stimulus, including thede novo group. Qualitatively similar recognition functions in the binocular and dichoptic conditionsshowed that the typical pattern of results – prevalence of S2 over S1 at intermediate SOAs – cannot beattributed to retinal processes and should be originating from central processes. An earlier finding (Bach-mann, 1994) that PD patients whose nonspecific thalamic nuclei were stimulated intracranially producedqualitatively unusual recognition functions that should have been the result of stimulation, rather than PDas such.

The list of the effects of Parkinson’s disease(PD) on behavioural/psychological functions isboth long and controversial. There is no doubtthat executive functions and motor processessuffer in PD as a direct and/or indirect result ofimpairment in the dopaminergic system. How-ever, the picture is less clear for relatively morepure cognitive and perceptual functions due totheir being cofounded with measured motor andeffector components in most experiments.Whereas a number of studies suggest that PDcauses at least some impairment of purely cogni-tive functions, including perceptual processingat various levels, other studies either fail to findevidence of cognitive/perceptual impairment or

report ambiguous findings, often qualifyingmeasured cognitive impairments as conditionalon the more concrete values of other variables.Let us list some examples from three groups ofstudies, beginning with more elementary levelsof function.

1. Elementary sensory processes of temporalresolution. According to Artieda, Pastor, La-cruz, and Obeso (1992), two-pulse temporal dis-crimination thresholds may be elevated in Par-kinsonian subjects with temporary improvementbeing effected by levodopa treatment. A relatedfinding was reported earlier by Bodis-Wollner etal. (1987) who showed that sensitivity to flickermay be diminished in PD.

TIME COURSE OF RECOGNITION IN PARKINSON’S DISEASE 119

2. Elementary processes of preconscious sen-sory detection.Not only conscious processesand explicitly reportable and intentionally exe-cuted responses may be impaired in PD. For ex-ample, automatic detection of stimulus changeas revealed by mismatch negativity componentof auditory ERPs may be impaired as well(Pekkonen, Jousmäki, Reinikainen, & Partanen,1995).

3. Speeded responses to sensory-perceptualstimuli. Jordan, Sagar, and Cooper (1992) havefound that cognitive components in reaction time(RT) may be slowed in PD, but are not sensitiveto dopamine treatment. On the other hand, in-crease in average RT in PD may be caused notby steady slowing of perceptual operations, butby the increase in the number of occasional long-latency trials as a result of oscillation of atten-tive state – the main distribution of RTs in PDhaving been found to coincide with that of a nor-mal group, except for asymmetrical edge at thelong-latency range (Brown et al., 1993). Therelatively more response-stage contribution tothe effects of RT slowing can also be inferredfrom the fact that latencies of sensory ERP com-ponents have been found to be unimpaired eventhough overt response latencies were slowed inPD (Karayanidis, Andrews, Ward, & Michie,1995). The benefit from pre-cueing in simple RTand choice RT tasks can be equal for PD andcontrol groups, given a smaller number of alter-natives with lower demands on higher cognitivelevels of processing (Willingham, Korozhets,Treadwell, & Bennett, 1995).

In some studies prolongation of simple RT inPD has also been documented in conditionswhere stimuli and responses are predictable,with this impairment being susceptible to dopa-mine treatment (Henderson & Goodrich, 1993);these authors found that treatment was less de-monstrable with simple RT than with choice RT.Deficits in performing concurrent choice reac-tion time tasks have been found to be dependenton the state of PD patients, which was inter-preted as referring to the necessity of adequatedopaminergic transmission in concurrent pro-cessing of cognitive information (Malapani,Pillon, Dubois, & Agid, 1994).

4. Visuospatial information processing.Spe-cific deficits such as impairment of facial recog-nition or visuoconstruction (Levin et al., 1991)or impairment of 3-D stereovision, figure-ground discrimination, and pattern perception(Flowers & Robertson, 1995) have been re-ported in PD. Similar cognitive impairments, forexample, impairments in visual discriminationamong 15 superimposed objects, and cognitiveslowing that were found among a PD group havebeen found to be not treatable by levodopa (Pil-lon et al., 1989).

5. Divided attention.Accuracy of performinga dichotic attention test has been found unim-paired in PD regardless of overt response slow-ing (Karayanidis et al., 1995) and regardless ofthe findings by other researchers concerningimpairments in set-shifting abilities (cf. below).

6. Top-down controlled attentional and/orproductive cognitive processes and capacities.Attentional focusing (Bradshaw et al., 1993),word fluency (Flowers, Robertson, & Sheridan,1995) and cognitive set-shifting ability (Raskin,Borod, & Tweedy, 1992; Van Spaendonck, Ber-ger, Horstink, Borm, & Cools, 1995) have alsobeen found to be impaired in PD.

Mixed findings have also been reported. Forexample, in experiments where PD subjects per-formed parallel and conjunction search tasks, nochanges in the latency of the ERP componentP300 were found, although the diminished ERPamplitude together with the finding of the spe-cific site of the strongest effect was interpretedas indicative of parietal identification systeminvolvement in PD dysfunctions (Weinstein,Troscianco, & Calvert, 1995). In attentional andmovement programming tasks, strategic leveloperations have been reported to be impaired inPD (Jones et al., 1994). At the same time, in astudy by Taylor, Saint-Cyr, and Lang (1987),cognitive processes at various stages were foundnot to be affected in PD if standard test methodswere used.

7. Short-term memory scanning.Russ andSeger (1995) found that the slope of the memoryscanning RT functions for words or pictures wasunaffected in PD, showing the absence of slow-ing of elementary cognitive operations (lack of

120 TALIS BACHMANN ET AL.

bradyphrenia), although the intercept of thefunctions was increased, which is indicative ofresponse system impairment. If motor compo-nents of the RT are disentangled from cognitivecomponents of memory scanning, attentionalorienting, or movement preparation, then RTs ofa PD population were not different from those ofa control group in the study by Rafal, Posner,Walker, and Friedrich (1984). Nevertheless, thedecrease of memory scanning speed in PD canbe found in other conditions. For example, whenWilson, Kaszniak, Klawans, and Garron ( 1980)used digits as stimuli and compared two agegroups of PD subjects, then slowing of the scan-ning speed in comparison with the age-matchednormal controls was found in the older group,but not in younger subjects.

8. Learning and working memory operations.Various findings can be listed here: impairmentof procedural learning in PD (Jackson, Jackson,Harrison, Henderson, & Kennard, 1995); im-pairment of the speed of discrimination learningin PD, but without the concomitant deficit in theshift of the decision rule (Joosten, Coenders, &Eling, 1995); impairment of spatial workingmemory and cognitive planning whereby dopa-mine treatment restored the accuracy, but not thelatency of performance (Owen et al., 1995).

In their recent meta-analytic review of thestudies of the components of visual cognition inPD, Waterfall and Crowe (1995) point out that anumber of methodological and theoretical faultscharacterize the respective research literature.Generalizing from 70 studies, they concludedthat PD subjects tend to demonstrate deficits inhigher-order attention and problem-solvingtasks, but that evidence in favor of deficits inmore basic visuoperceptual functions remainsfar from conclusive. Therefore, many observeddeficits may be either a consequence of hiddenlower level visual-cognitive deficits, a compro-mise in executive functioning, or both. Studiesby Flowers and Robertson (e.g., 1995) add tothis equivocity by showing that a mixture of bot-tom-up and top-down processes determine per-ceptual abnormalities in PD, depending on otherfactors such as severity of the stage of disease.

In analysing the body of research literatureabout the effects of PD on visual cognitive func-

tions, we noticed that although there are severalstrongly established traditions of study, someobvious and theoretically important experimen-tal approaches have not received sufficient at-tention. Whereas our main theoretical interestconcerns the problem of possible impairments ofthe speed of elementary perceptual recognitionoperations in PD (especially without the need toinvolve manual reaction times as dependentmeasures) and, therefore, also relates to theproblem of the hypothetical Parkinsonian brady-phrenia, we decided to concentrate our attentionon finding out if there are any more or less defi-nite data and conclusions with regard to thisproblem. If we regard the studies listed in items1, 3, 6, and 7 above as closest to those capableof disclosing some basic information processingcomponents and prerequisites of Parkinsonianbradyphrenia, it is not difficult to notice that it ispremature to speak about definitive conclusions.Temporally distributed processes, processeswith strong strategic and decision-making com-ponents, processes that are measured with man-ual reaction-time methods, and processes thattake part within short-term memory or heavilyrely upon complex memory processes are widelystudied, whereas simple, predominantly bottom-up directed, single-act processes of visual recog-nition without the need to invoke fast manualresponses are relatively neglected.

The studies that have been directed towardselementary processes of temporal resolutionsuch as two-pulse integration or flicker fusionalso lack the component of pattern or form rec-ognition. In other words, the speed of the obvi-ous, elementary perceptual recognition opera-tions that could be an important aspect in thedevelopment of bradyphrenia in PD and thatshould be measured without heavy participationof higher-level cognitive processes have re-mained relatively unnoticed by researchers.

Those studies that have been directed towardsthe solution of the problem of bradyphrenia are(1) quite controversial, (2) deal mostly with thecognitive processes of top-down heritage and/orshort-term memory, and (3) are based onmethods that require manual responding by thesubjects. In light of these specifications, the fun-damental question remains as to whether one


can document impairment in bottom-up di-rected, perceptual-cognitive processes (includ-ing slowing of the elementary mental opera-tions) in addition to motor- and planning-systemimpairments. Because a general behavioral out-come – say, slowing of perceptual recognition ordiscrimination performance – can be both theresult of impairment in afferent and in efferentstages of information processing, then it wouldbe useful to find experimental paradigms thatare capable of disentangling these stages.

The basic strategy in studying the temporalaspect of information processing (includingspeed of processing) is based on the well-devel-oped standard RT methods for studying thespeed and temporal dynamics of perceptual pro-cessing in normal populations. However, thisstrategy seems to be inadequate for a Parkinso-nian population due to the obvious basic centralmotor system impairment both at the executiveand coordinating levels. Thus, methods capableof measuring the speed and time-course of per-ceptual-cognitive processing without the need toinvoke fast manual or oculomotor responses andreaction time measurement are necessary.

Other desirable characteristics of such amethod are (1) low demand on memory capacity(no more than two to three response alternativesof a highly overlearned nature per trial); (2) ab-sence of image scanning by saccadic eye move-ments (see White et al., 1988, for hypometricsaccades with diminished compensatory move-ments in PD); (3) the possibility to control theimpact of possible retinal dopamine deficiency(see Flowers, Robertson, & Sheridan, 1987, onrespective deficiency in PD); (4) good temporalresolution of the method and possibility to varytemporal variables parametrically. The methodof mutual masking (Bachmann & Allik, 1976;Michaels & Turvey, 1979) satisfies these criteriawell. Pairs of mutually different, but spatiallyoverlapping visual stimuli are exposed succes-sively, for a very short duration (e.g., 10 ms).Subjects are asked to recognize both stimuli ateach trial. With gradually varying stimulus onsetasynchrony (SOA) between the values of, say, 0ms and 300 ms, recognition efficiency for thefirst stimuli in the pairs (S1) and for the secondstimuli in the pairs (S2) can be plotted as a func-

tion of SOA. The values of SOA where the func-tion of recognition of S1 approaches upper as-ymptote can be regarded as the indice of thespeed of processing (the time value of the pro-cessing episode by which S1 can be successfullyrecognized without interference from the fol-lowing S2).

The relative efficiencies of S1 and S2 at vari-ous SOA values are indicative of the perceptualsystem tendency to switch or not to switch pro-cessing operations from the previous input sig-nals to the succeeding ones and/or of the ten-dency to process signals in parallel. Exposure oftwo small, spatially overlapping stimuli at thecenter of the visual field and within the brieftime window helps to obviate the need to invokepurposeful eye movements.

Because both binocular (both stimuli exposedto both retinas) and dichoptic (S1 to one eye, S2to the other eye) exposure regimes can be used,then retinal effects can be controlled. Only tworequired identity responses at each trial put nohigh demand on memory. Fast manual responsesare eliminated from this procedure as well.Overlearned and relatively simple stimuli, suchas letters, are common means to satisfy usefulexperimental requirements and to adapt automa-tized (computerized) experimental techniquesthat can be easily standardized between labora-tories.

In Figure 1, typical results of mutual maskingare seen in the conditions where the intensity ofS1 exceeds that of S2 (function A: solid linewith discs) or where respective intensities aremore or less equal (function B: dashed line withtriangles) (Bachmann, 1994). IntermediateSOAs are characterized by the dominance of S2over Sl for perceptual processing regardless ofthe condition of their relative brightness. Thevalues of SOA around 150 ms that are indicativeof equalization of the values of S1 and S2 recog-nition functions close to upper asymptotic levelcan be regarded as an operational measure of thetypical duration of the elementary visual recog-nition cycle.

If PD patients lag behind the normal controlgroup in terms of the isoeffectiveness values ofSOA, this outcome, if statistically significant,can be regarded as support for the regularity by


Fig. 1. Typical mutual masking functions (percent correct recognition as dependent on SOA) for the pairs ofsuccessively exposed, spatially overlapping visual stimuli, S1 and S2. A: the intensity of Sl exceeds thatof S2 (solid line, discs). B: the intensities of S1 and S2 are compatible (dashed line, triangles).

which perceptual recognition functions in PDare slowed. This constitutes our first and mainhypothesis in this study. The second, additionalhypothesis concerns the possibility to discrimi-nate between the de novo PD group and a PDgroup that has had treatment. The third hypothe-sis is related to the tentative possibility to dis-criminate between two groups of PD patientsdifferentiated according to their predominantsymptoms – a tremor group and a hypokineticrigidity group.

In an earlier study (Bachmann, 1994) wefound mutual masking functions with hospital-ized PD patients who were undergoing stereo-tactic treatment in the Department of Neurologyand Neurosurgery of the Institute of Experimen-tal Medicine of the Russian Academy of Medi-cal Sciences (St. Petersburg). The patients par-ticipated in the tachistoscopic experiments im-mediately following the sessions of activatingstimulation of the nonspecific thalamic nuclei

via the implanted electrodes (Smirnov &Reznikova, 1985). Qualitatively unusual func-tions were found (Figure 2): PD patients tendedto perceive Sl with unusual efficiency and PDpatients did not produce typical predominanceof S2 over S1 at intermediate SOA values incontrast with the normal control group and withthe typical functions of other studies where thesame experimental variables were used. ‘‘Stick-ing to first stimulus’’ could be the proper nameof the effect.

Unfortunately, it cannot be said at present ifthis effect was a result of PD or a result of acti-vating thalamic stimulation. If it was a result ofPD, one could think along the lines of develop-ing an early diagnostic test for the proneness todevelop PD symptoms – unusual mutual mask-ing functions could indicate the presence of po-tential risk factor(s). If it is a result of activatingtreatment via nonspecific thalamic nuclei, itgives additional converging evidence for the


Fig. 2. Unusual mutual masking functions obtained with PD patients whose nonspecific thalamic nuclei werestimulated by chronically implanted microelectrodes for treatment purposes: S1 is strongly dominatingover S2 and intermediate SOAs do not lead to S2 prevalence. (Adapted from Bachmann, 1994.)

perceptual retouch theory of visual masking (fordetails see Bachmann, 1984,1988,1994).

One of the objectives of the present study wasto test these alternative predictions. Hence, ourfourth specific hypothesis inquires if the PDgroup could display qualitatively different mu-tual masking functions as compared to the con-trol group. This should reveal itself in statisti-cally significant interaction between the factorsof health status and SOA and/or first or secondstimulus (Sl vs. S2).

EXPERIMENT 1

METHOD

Thirty-seven PD patients and 19 age-matched nor-mal controls were employed as subjects in thisstudy. The patients were recruited from among

those who were subject to PD treatment in the De-partment of Neurology and Neurosurgery at theUniversity of Tartu or the Neurology Departmentat the Mustamäe Hospital of Tallinn. Informedconsent was obtained. Participants were assignedto experimental groups according to their treat-ment history ((1) de novo without dopaminergicmedication – 21 subjects, 11 males and 10 femalesaged between 38 and 81 years; (2) medicated – 16subjects, 8 males and 8 females aged between 51and 82 years) and according to predominant symp-toms ((1) hypokinetic rigidity – 15 subjects, 8males and 7 females aged between 43 and 75years; (2) tremor – 16 subjects, 8 males and 8 fe-males aged between 44 and 82 years). Two PDsubjects belonged to stage 3.0; 5 to 2.5; 11 to 2.0;7 to 1.5; and 12 to stage 1.0 according to theHoehn and Yahr scale. The Wilcoxon-Mann-Whit-ney U-test showed that the distribution of de novoand treated patients between different Hoehn andYahr PD stages was statistically unbiased (sum ofinversions was equal to 163,p > 0.05; scale aver-ages were: 1.61 for de novo patients, and 1.81 for


treated patients). All subjects had normal or cor-rected to normal vision. All subjects participated inthe mutual masking experiment. In addition PDpatients completed the standard memory test fromthe Luria test battery in order to control the possi-ble memory deficits. The subjects in the presentstudy had unimpaired memory capacity in terms ofreproducing the first two remembered stimuli fromthe list. This was necessary in order to ascertain ifthe subjects would be capable of performing thetwo-letter recognition without limitations from theimmediate memory-related aspect of processing.

In the mutual masking experiment the standardIBM PC was used for stimulus exposure. Pairs ofmutually different letters from the English alpha-bet were chosen at random for each exposure trial.Letters were exposed for 25 ms each. They ap-peared successively at the same, overlapping cen-tral area immediately above the fixation point. Thefollowing values of stimulus onset asynchronies(SOAs) were used, each value for an equal numberof times: 25 ms, 40 ms, 55 ms, 95 ms, 165 ms, or285 ms. Letters were light on dark background.The luminance of the background equalled 5.16cd/m2, the point luminance of the first letter (S1)equalled 64.2 cd/m2 and that of the second letter(S2) 35.5 cd/m2. The size of the letter was equal to0.6 degrees of the visual angle along the verticaldimension. Each subject was given 40 exposuresof the letter pairs for each of the SOA values, thus240 exposures in toto. The task of the subjects con-sisted in recognition of both letters in a pair ac-cording to the forced response requirement. (sub-jects had to guess if unsure.)

ProcedureThe subject was seated in front of the computerdisplay and the task was explained to him/her. Itwas emphasized that responses are required forboth of the letters in each pair and if unsure, thebest guess(es) should be made. Each trial beganwith an oral warning, then a small lighted fixationdot appeared for 1000 ms at the center of the dis-play, followed by the exposure of the stimuli im-mediately above the fixation point. Responseswere recorded by the experimenter’s assistant viathe computer keys. Order of SOAs was random-ized by the computer. Subjects were allowed peri-ods of rest if necessary. Conditions of light adap-tion were not changed.

RESULTS AND DISCUSSION

As one can observe from Figure 3 both the con-trol group (Figure 3 A) and the PD group (Fig-ure 3 B) produced typical recognition functionsfor S1 vis-à-vis S2 – the clear advantage of S2recognition at intermediate SOAs is evident. Theinteraction between SOA and temporal order ofthe stimuli (S1 vs. S2) was highly significant [F(5,443) = 10.270;p < .001]. Two types of gen-eral highly significant main effects were re-vealed by ANOVA. First, the effect of healthstatus shows that the control group performedsignificantly better than did the PD groups [F(2,335) = 20.397;p < .001 for Sl recognition andF (2,335) = 11.033;p < .001 for S2 recognition].Comparing Figure 3A and Figure 3B, it takesabout 50 ms increase of SOA for the PD patientsto reach the level of Sl recognition that is equalto that of the normal control group. If with SOA= 165 ms in the normal control group the effi-ciency of S1 recognition already exceeds that ofS2 (76 and 74 %, respectively) then in PDgroups S1 recognition level has not reached thatof S2 (62 and 67 %, respectively). Second, theeffect of the SOA shows that recognition effi-ciency increases with SOA both for Sl [F(5,335) = 45.828;p < .001] and for S2 [F(5,335) = 24.112;p < .001].

There was no significant interaction betweenhealth status and SOA neither for S 1 recogni-tion [F (10,335) = 0.546;p = 0.85], nor for S2recognition (F (10,335) = 0.162;p = .99), how-ever. As one can see on Figure 4 (A,B), the ef-fect of health status is additive across SOA val-ues. This finding, together with the clear pre-dominance of S2 recognition over S1 recogni-tion at intermediate SOAs that is even strongerin the PD groups than in the control group (cf.Figure 3) invalidates our hypothesis about possi-ble qualitative differences in mutual maskingfunctions of PD patients (both treated and denovo) as compared to normal control. PD pa-tients did not display abnormally high relativelevels of S1 recognition in comparison with S2recognition as was found by Bachmann (1994).At intermediate SOAs respective Sl and S2 rec-ognition levels in the PD group in the presentstudy were 35% versus 52% for SOA = 40 ms,


A.

B.

Fig. 3. Efficiency of recognition of first and second letters (solid line for S1 and dashed line for S2,rerspectively) in successively exposed pairs as a function of SOA for the control group (A) and for theParkinson’s disease group (B); Experiment 1.


A.

B.

Fig. 4. A: Efficiency of recognition of S1 as a function of SOA and treatment status (de novo, treated, andnormal control). B: Efficiency of recognition of S2 as a function of SOA and treatment status. Data fromExperiment 1.


31% versus 62% for SOA = 55 ms, and 47%versus 69% for SOA = 95 ms. Thus that earliereffect should most probably have been the resultof direct thalamic activation through implantedelectrodes.

A significant interaction between the tempo-ral position of a stimulus letter in a pair (S1 vs.S2) and health status was found between thecontrol group and de novo group [F (l,479) =5.136;p < .02]: the effect of PD was clearcutprimarily in impairment of S1 recognition, butnot in S2 recognition (compare respective func-tions on Figures 4A and B).

This again substantiates the thesis that whatmatters first of all is speed of recognition opera-tions that can be executed on perceptual evi-dence of S1 before the succeeding, interferingletter (S2) arrives. We sought for the analoguousANOVA interaction between the control groupand the treated PD group but did not find a sig-nificant effect [F (1,419) = 0.448;p = .50], al-though the main effect – impairment of recogni-tion in the treated PD group – was significantacross all SOAs both for S1 recognition [F(1,209) = 36.430;p < .001] and for S2 recogni-tion [F (1,209) = 18.175;p < .001]. If our PDgroup with treatment were equal to our de novoPD group in terms of average rating according tothe Hoehn and Yahr scale (see the Method sec-tion), then we speculate that the baseline Hoehnand Yahr scale rating in the treated PD groupmay be actually higher, but is partly alleviatedby treatment.

To test if this might be the reason why thetreated group performed worse than the de novogroup (especially in comparison with controlgroup if S2 was to be recognized) should be apossible task in future studies where the experi-mental design with before-after medicationscheme within the treated group should be used.At present we cannot assign this effect exclu-sively either to medication or to baseline stageof PD, however. What we can say is that PD hasa detrimental effect on fast recognition regard-less of medication status (cf impairment of S1processing).

The switching to S2 processing is not im-paired in our group of patients with relativelymild, nontreated PD (cf. equal level of S2 recog-

nition functions in nontreated and controlgroups).

We found also a significant main effect of theHoehn and Yahr ratings both for S1 recognitionand S2 recognition [F (1,221) = 30.485;p <.001, andF (1,221) = 41.250;p < .001, respec-tively]. There were significant negative correla-tions between Hoehn and Yahr ratings and rec-ognition efficiency: the stronger the PD symp-toms, the more impaired the recognition level (r= – 0.237;p < .001 for Sl, andr = –0.307;p <.001 for S2). There were no significant interac-tions between the Hoehn and Yahr scale ratingsand any other factors, however. The PD effectsseen in these ratings were uniformly additiveacross SOA values and differently positionedstimuli. If one expects increased difficulties inshifting attention from S1 to S2 with the ad-vancement of PD, then interaction between scaleratings and the position of stimuli could befound. Because this effect was absent, we con-clude that either the stages of PD of our patientswere not sufficiently high or this experimentalparadigm is not a proper means to test the shiftof attention that is related to variable mental setto simple characteristics of stimulation like tem-poral position of stimulus order. (It may also bethat set-shifting effects in PD in principle can befound only with more complex or more abstractinter-categorical or with incompatible inter re-sponse-category experimental designs.)

We did not find significant differences be-tween the performance of two different groupsof predominant symptoms – tremor versus hypo-kinetic rigidity – in recognizing S2 [F (1,185) =0.336;p = .56], but there was a significant maineffect of symptom category if Sl had to be rec-ognized: the hypokinetic rigidity group per-formed at a higher level than did the tremorgroup uniformly at all SOAs [F (1,185) = 4.221;p < .04]. Future studies should look for the pos-sible causes and underlying mechanisms of thiseffect. There were no significant interactionsbetween predominant symptoms and SOA nei-ther with S1 recognition, nor with S2 recogni-tion [F (5,185) = .042;p < 0.99, andF (5,185) =0.009;p = 1.0, respectively].

There were no significant effects of medica-tion type. ANOVA that contrasted Madopar and


Nakom treatment revealedF (1,191) = 2.321;p= 0.13. The Luria memory test results showedno significant main effects or interactions withother factors. The average memory test indexwas equal to 0.765.

In the present experiment both successivestimuli were exposed to the same retinas of thesubjects, thus making it possible that interac-tions between competing processing operationscan begin already at the peripheral sensory level.In the study by Bachmann (1994), a similar bin-ocular exposure regimen was used, yet unusualfunctions without S2 prevalence were found.

It would be useful to see, whether we couldobtain that type of unusual mutual maskingfunction if we exclude retinal interactions be-tween the stimuli. Another difference betweenour Experiment 1 and that of Bachmann (1994)was the number of stimulus alternatives.Bachmann (1994) used only five different geo-metric forms but the whole alphabet was em-ployed in Experiment 1. Thus in addition todichoptic regime we may want to decrease thenumber of stimulus alternatives as well. It isalso known (e.g., Flowers, 1987), that in PDsubjects retinal dopamine deficiency is a com-mon finding.

Therefore it is not possible to ascribe the ob-tained recognition functions unambiguously toeither peripheral or central levels of processing.Dichoptic tachistoscopic exposures would benecessary for this reason as well in order to seeif the same qualitative picture would appear inthe results if the interaction between the stimulitakes place only beginning with cortical levelsof processing. By decreasing the number of re-sponse alternatives we also diminish the possi-ble effects of capacity limitations for memorysearch. To test the possible impact of these fac-tors and to seek other conditions for obtainingthe potentially important, qualitatively unusualfunctions with S1 prevalence (possibility to de-velop diagnostic methods!) another experimentwas completed.

EXPERIMENT 2

METHOD

12 PD patients (8 de novo, 4 treated) aged between42 and 82 years were used as subjects. The basicrationale of the experiment was similar to that ofExperiment 1, except the following differences. Inthis experiment stimuli were exposed by the meansof five-channel tachistoscope (manufactured byTSU Experimental Construction Shop) dichopti-cally (one stimulus in a pair to one eye, the otherstimulus of the same pair to the other eye). Sl wasexposed for 30 ms with background intensity equalto about 3 cd/m2, S2 was exposed for 15 ms. Stim-uli consisted of dark capital letters – H, M, R, W,K, or B – onlight ackground and were presented atthe center of the visual field. The center was desig-nated by the small fixation dot. The size of thestimulus letters was equal to 0.72 degrees of thevisual angle along the vertical dimension. After theready-signal in each trial fixation was exposed for1000 ms, followed by the two successive, spatiallyoverlapping stimuli. The SOA values used were 0ms, 20 ms, 50 ms, 90 ms, 140 ms, or 260 ms.

ProcedureEach subject received 30 successively paired Sland S2 exposures at each SOA value. SOA valueswere counterbalanced within and between subjects.Brief periods of rest were allowed when necessary,however without change in light adaptation. Aftereach exposure subjects responded with reportingthe identities of both letters they saw, guessing ifunsure. Their responses were recorded with the aidof the computer by the experimenter’s assistant.

RESULTS

As it can be seen from Figure 5, both groups ofsubjects – treated PD, de novo PD – have pro-duced in dichoptic conditions mutual mask-ing/recognition functions that are qualitativelytypical to this type of interaction: prevalence ofS2 at intermediate SOAs, and general increaseof efficiency with increase in SOA. The differ-ent dynamics of Sl and S2 recognition is sub-stantiated by the significant ANOVA interactionbetween SOA and ordinal position of a stimulus:F (5, 1074) = 15.97; p < 0.0001 for de novo PDpatients;F (5,1074 ) = 12.57;p < 0.0001 fortreated PD patients. (Due to the small number of


Fig. 5. Efficiency of recognition of S1 (solid line) and S2 (dashed line) as a function of SOA for de novo pa-tients (A) and treated patients (B) in dichoptic exposure regime; Experiment 2.

A.

B.

subjects in this experiment we included all responses of respective subjects’ groups to theANOVA in contrast to Experiment l, where av-erages of different subjects were forming the

entrance table for ANOVA.) Thus we can con-clude that this qualitative picture is most proba-bly of the central processing level origin andthat unusual mutual masking functions with Sl


facilitation relative to S2 found in Bachmann(1994) were not the result of PD (either pharma-cologically treated or not), but the result of in-tracranial electrical thalamic stimulation thatimmediately preceded the tachistoscopic experi-ment.

GENERAL DISCUSSION

The main feature of our present study consistedof the absence of the need to execute fast man-ual or ocular movements by the subjects in orderto measure the speed of elementary perceptual-cognitive processes. Yet the results of the Ex-periment 1, by the virtue of juxtaposing Sl andS2 processing (as collated via parametricallyvaried SOA values and thus indirectly measur-ing the time course of processing), provide sup-port for the hypothesis about slowing of elemen-tary visual recognition processes in PD. In thecontext of this result the findings of Artieda etal. (1992) and Bodis-Wollner (1987) who re-ported the impairment of simple temporal reso-lution in PD seem to be hinting at the possiblebasis of our obtained perceptual slowing. If ele-mentary processes of temporal integration in thePD subject’s visual system are slowed, then alsothe perceptual evidence for recognition opera-tions should be accumulating more slowly and itwould take longer SOAs to reach at some criti-cal levels of Sl recognition in comparison withnormal subjects.

It seems to us, however, that – given impair-ments in spatiotemporal integration – it is stilldifficult to interpret why S2 recognition alsotakes longer in treated PD subjects. If it weresimply for stronger forward masking as a resultof longer temporal integration of the luminousenergy from Sl that interferes with S2 process-ing, then we would obtain the interaction be-tween health status and the temporal position ofstimulus exactly in the opposite direction – rela-tively larger impairment of S2 recognition inPD. That was not the case (see the Results sec-tion of Experiment 1). These facts together withthe clearly observable switch from Sl processingto S2 processing (see Figure 3 about the preva-lence of S2 over S1 at intermediate SOAs in PD

group and notice that this prevalence is not lessexpressed than in normal control) suggest thatsimple impairment of the pre-recognition pro-cesses of fast temporal integration of luminousenergy need not be the only cause of the slow-ing. We may thus conclude that our results ofExperiment l lend support to the standpoint thatcentral, elementary perceptual-cognitive opera-tions are impaired in PD and that medicationmay partly restore the distribution of resourcesbetween Sl and S2 in relative terms, but not inabsolute terms. That these effects are not causedby general memory deficit can be derived fromthe fact that the results of Luria memory testwere quite good and that only two responses ofreporting highly overlearned stimuli were re-quired from the subjects at each trial.

Various examples of decreased visuospatialinformation processing in PD have been pre-sented (e.g., Pillon et al., 1989; Levin et al.,1991; Flowers and Robertson, 1995; see alsoWaterfall and Crowe, 1995). It would thus bepossible to hypothesise that the effect of PD onrecognition found in the present study couldconsiderably or partly stem from certain generalor specific spatial perceptual disabilities. If sim-ple, overlearned stimuli are presented in invari-ant spatial position then it is highly improbablethat spatial orientation deficiencies form the ba-sis of the obtained effects. The general ability toperceive forms and execute recognition opera-tions should not be impaired as well, because thefunctions at S2 recognition were not much dif-ferent in PD as compared with normal controls.

Cummings and Huber (1992) proposed todivide visuospatial functioning in the context ofParkinsonian research into six categories: (1)visual sensory functions, (2) visual perceptualskills, (3) visuomotor abilities, (4) visuospatialattention, (5) visuospatial cognition, and (6)body-spatial orientation. Again, relying on un-impaired efficiency of S2 recogni t ion,invariance of spatial position of the stimuli, andbottom-up nature of the processing task in ourexperiments none of the listed subcategoriescould be regarded as the site of the impairmentthat was found in this study. In the similar, butrelatively more thorough list of 12 categoriesthat was proposed by Waterfall and Crowe


(1995) the only item that is relevant in order toidentify the visual cognitive function that seemsto be impaired in our perceptual task is theiritem 5: perception and recognition of shapes(and faces). And even here we should introducea constraint by specifying the function as that offast or speeded shape recognition.

In a recent study, Russ and Seger (1995)found that in a memory-scanning experimentwith words and pictures as stimuli, reaction timeslopes (increments in RT per unit of increase inthe size of the memory set) of PD subjects andcontrols do not differ. The authors conclude thatalthough the speed of executive componentsmay be decreased in PD (the intercept of the RTfunction indicating the generally slower re-sponses in PD), the speed of cognitive opera-tions need not: switching between the succes-sively matched alternatives in memory-set pro-ceeds equally fast in PD and in control groups.This variety of the lack of bradyphrenia some-what contradicts our present results. We againdraw attention to one important difference be-tween their study and our study: while Russ andSeger used a task that had strong top-down com-ponent of processing and operations relevant totheir theoretical interest took part in short-termmemory, then in our task the principal process-ing route consisted in bottom-up direction. Thisfact, together with the observations byWeinstein, Troscianko, and Calvert (1995) whofound that in PD-subjects diminished ERP com-ponents tend to be especially localized in pari-etal sites, suggests that the locus of slowingand/or impairment could be assigned to identifi-cation and perceptual classification system.

On the other hand, Wilson et al. (1980) havefound that if PD subjects perform memory scan-ning with relatively more simple stimuli – digits– then in the older group of PD subjects the ef-fect of slowing obtains. It could be that indica-tions of bradyphrenia in relatively mild stages ofPD can be better disclosed in conditions whereextreme rapidity of processing is at hand eitherdue to simpler perceptual material (as in Wilsonet al., 1980) and/or due to experimental designthat enforces speeded processing (as in ourstudy, where arrival of S2 after Sl constrains the

time-window of recognition-processing and per-ceptual shape formation).

The effects of predominant symptoms (tremorvs hypokinetic rigidity) cannot be discussed in aclearcut fashion. The small effect with S1 recog-nition may include a cofound from the medica-tion status and/or Hoehn and Yahr scale evalua-tion. This should be a matter of respective fol-low-up studies. Lack of the effects of medica-tion status (Nakom vs Madopar treatment) indi-rectly refers to cognitive sites of the obtainedperceptual slowing. It should also be clear thatstandard levodopa medication that is targeted atalleviating dopaminergic deficiencies, althoughthrough somewhat different drugs, need nothave significantly different effects on recogni-tion processes unless we specifically control thetemporal dynamics of the drug effects and espe-cially test the effects of these respective time-patterns on recognition performance. (Anotherdimension of potential interest that was left outof the present study was the potential impact ofthe on-off dynamics of the parkinsonian states.)

In the present experiments mostly the PDsubjects who belonged to the stages from the 1stto 2nd of PD (Hoehn and Yahr scale) were em-ployed. Thus, if combined with the absence ofsubstantial complications in the planning or ex-ecutive components in the present experimentaltask, the potential effects of pharmacologicaltreatment and predominant symptoms need notmanifest themselves very strongly. On the otherhand, several authors (e.g., Pillon et al., 1989)have shown that cognitive impairment in PDpatients is not correlated with symptoms that aretreated by levodopa. (Also, for example, carefulinspection of the study by Daniels, Harding, &Anderson, 1994, reveals that reduced amplitudeof the N2-P2 component of the ERP in responseto luminous flash in PD subjects can be obtainedwith dopaminergic and/or anticholinergic treat-ment.) Accordingly we may hypothesise thatsome indirectly affected systems out of the basalganglia might be involved.

Indirect support to this view comes fromBachmann (1994) where mutual masking func-tions change substantially if thalamic nonspe-cific nuclei of the patients are stimulated. The


phenomenon of ‘‘sticking to the first stimulus’’found in that study may mean at least one of thetwo different scenarios, or both: (1) unusuallyfast and ‘‘contrasted’’ perceiving of Sl and re-spectively larger spending of the share of lim-ited capacy attentional resources for the fast pro-cessing of S1; (2) inhibition of the attentionalswitching and/or novel stimulus detecting mech-anisms or perturbations in the mental shift of setthat usually would push the system from S1 toS2. The latter possibility is supported by thefinding of Pekkonen et al. (1995) who showedthat in PD the mismatch negativity – the earlyautomatic, negative deflection of ERP in re-sponse to novel or changed stimulus, cf.Näätänen (1992) – is diminished in PD patients.

In our results this idea is supported by the factthat nontreated patients, whose baseline PDstage is most probably lower than in treated PD(whose average Hoehn and Yahr rating was nowequal to that of the nontreated group) performedvery well on S2 recognition (which is possible ifefficient switch from Sl was made), but not sowell on Sl. Larger values of negative correlationcoefficients between recognition efficiency andthe value of Hoehn and Yahr ratings were foundfor S1 recognition than for S2, which supportsour statement. Whether our results are related toautomatic or focal-attentional components ofperceptual-cognitive processing would requiresome special studies, however.

Although slowing in elementary visual recog-nition operations in PD was found in Experi-ment 1, the effects are by no means very dra-matic. The general pattern of results demon-strates that patients are quite good at performingthe task of recognition of two consecutive, verybrief visual stimuli that alternate within veryshort temporal window. The same regularitywhereby the perceptual system tends to favor thefollowing one from the two rapidly alternatinginputs characterizes both the normal controlgroup and the PD patients regardless of thetreatment history and predominant symptoms ofthe latter group. The results of Experiment 2show that this regularity is based on central pro-cesses and not on any masking artefacts of theretinal origin. With dichoptic exposures the fac-tor of eye dominance would require much larger

number of subjects in order to avoid the possibleeye dominance artefact if we would like to re-peat Experiment 1 in dichoptic conditions. As amatter of fact, since the factorial combination of(1) inputs to the right and left eye, and (2) tem-poral order of exposure was balanced in Experi-ment 2, then subjects with strong eye dominanceshould have suffered more from the dichopticregimen than subjects with weak dominance fac-tor. This question needs to be analysed in somespecial future research.

The not so dramatic, however highly signifi-cant from the statistical point of view, effect ofperceptual slowing/impairment in PD togetherwith the absence of any striking qualitative dif-ferences in the mutual masking functions of S1vis-à-vis S2 of PD patients as compared to nor-mal controls (although the results of Bachmann,1994, hinted towards this possibility) leaves uswith the conclusion that it would be prematureand unjustified at present to expect the develop-ment of a diagnostic or classificatory method ofPD based on the mutual masking paradigm orany other similar visual processing paradigms.On the other hand, given that patients who canbe rated as having more advanced stages of PDwill be studied and/or given the possibilities ofmore purposeful and systematic psychopharma-cological intervention be involved, it seems jus-tified to continue some basic science studies thatare based on the time-course paradigms thatabandon necessity to use manual reactions onthe one hand and too simple temporal resolutionmethods on the other.

REFERENCES

Artieda, J., Pastor, M.A., Lacruz, F., & Obeso, J.A.(1992). Temporal discrimination is abnormal inParkinson’s disease.Brain, 115,199-210.

Bachmann, T. (1984). The process of perceptual re-touch: Nonspecific afferent activation dynamics inexplaining visual masking.Perception and Psycho-physics, 35,69-84.

Bachmann, T. (1988). Time course of the subjectivecontrast enhancement for a second stimulus in suc-cessively paired above-threshold transient forms:Perceptual retouch instead of forward masking.Vision Research, 28,1255-1261.


Bachmann, T. (1994).Psychophysiology of visualmasking: The fine structure of conscious experi-ence.Commack, NY: Nova Science.

Bachmann, T., & Allik, J. (1976). Integration and in-terruption in the masking of form by form.Percep-tion, 5,79-97.

Bodis-Wollner, I., Marx, M.S., Mitra, S., Bobak, P.,Mylin, L., & Yahr, M. (1987). Visual dysfunctionin Parkinson’s disease: Loss in spatiotemporal con-trast sensitivity.Brain, 110,1675-1698.

Bradshaw, J.L., Waterfall, M.L., Phillips, J.G.,Iansek, R., Mattingley, J.B., & Bradshaw, J.A.(1993). Re-orientation of attention in Parkinson’sdisease: An extension to the vibrotactile modality.Neuropsychologia, 31,51-66.

Brown, V.J., Schwarz, U., Bowman, E.M., Fuhr, P.,Robinson, D.L., & Hallett, M. (1993). Dopaminedependent reaction time deficits in patients withParkinson’s disease are task specific.Neuro-psychologia, 31,459-469.

Cummings, J.L., & Huber, S.J. (1992). Visuospatialabnormalities in Parkinson’s disease. In S.J.Huber& J.L.Cummings (Eds.),Parkinson’s disease:Neurobehavioural aspects(pp. 59-73). New York:Oxford University Press.

Daniels, R., Harding, G.F.A., & Anderson, S.J.(1994). Effect of dopamine and acetylcholine onthe visual evoked potential.International Journalof Psychophysiology, 16,251-261.

Flowers, K.A. (1987). Parkinsonism. In R.L. Gregory(Ed.),The Oxford companion to the mind(pp. 587-591). Oxford: Oxford University Press.

Flowers, K.A., & Robinson, C. (1995). Perceptualabnormalities in Parkinson’s disease: Top-down orbottom-up processes?Perception, 24,1201-1221.

Flowers, K.A., Robertson, C., & Sheridan, M.R.(1995). Some characteristics of word fluency inParkinson’s disease.Journal of Neurolinguistics, 9,33-46.

Henderson, L., & Goodrich, S.J. (1993). Simple reac-tion time and predictive tracking in Parkinson’sdisease: Do they converge on a single, fixed im-pairment of preparation?Journal of Motor Behav-ior, 25, 89-96.

Jackson, G.M., Jackson, S.R., Harrison, J., Hender-son, L., & Kennard, C. (1995). Serial reaction timelearning and Parkinson’s disease: Evidence for aprocedural learning deficit.Neuropsychologia, 33,577-593.

Jones, D.L., Bradshaw, J.L., Phillips, J.G., Iansek, R.,Mattingley, J.B., & Bradshaw, J.A. (1994). Alloca-tion of attention to programming of movement se-quences in Parkinson’s disease.Journal of Clinicaland Experimental Neuropsychology, 16,117-128.

Joosten, J.P.A., Coenders, C.J.H., & Eling, P.A.T.M.(1995). Shifting behavior: An analysis of responsepatterns of Parkinson patients in discriminationlearning.Brain and Cognition, 29,115-126.

Jordan, N., Sagar, H.J., & Cooper, J.A. (1992). Cogni-tive components of reaction time in Parkinson’sdisease.Journal of Neurology and Psychiatry, 55,658-664.

Karayanidis, F., Andrews, S., Ward, P.B., & Michie,P.T. (1995). ERP indices of auditory selective at-tention in aging and Parkinson’s disease.Psycho-physiology, 32,335-350.

Levin, B.E., Llabre, M.M., Reisman, S., Weiner,W.J., Sanches-Ramos, J., Singer, C., & Brown,M.C. (1991). Visuospatial impairment in Parkin-son’s disease.Neurology, 41,365-369.

Malapani, C., Pillon, B., Dubois, B., & Agid, Y.(1994). Impaired simultaneous cognitive task per-formance in Parkinson’s disease: A dopamine-re-lated dysfunction.Neurology, 44,319-326.

Michaels, C.F., & Turvey, M.T. (1979). Centralsources of visual masking: Indexing structures sup-porting seeing at a single, brief glance.Psychologi-cal Research, 41,1-61.

Näätänen, R. (1992).Attention and brain function.Hillsdale, NJ: Lawrence Erlbaum.

Owen, A.M., Sahakian, B.J., Hodges, J.R., Summers,B.A., Polkey, C.E., & Robbins, T.W. (1995). Do-pamine-dependent frontostriatal planning deficitsin early Parkinson’s disease.Neuropsychology, 9,126-140.

Pekkonen, E., Jousmäki, V., Reinikainen, K., &Partanen, J. (1995). Automatic auditory discrimi-nation is impaired in Parkinson’s disease. Papersubmitted toElectroencephalography and ClinicalNeurophysiology EEG Journal, 95, 47-52.

Pillon, B., Dubois, B., Cusimano, G., Bonnet, A.-M-,Lhermitte, F., & Agid, Y. (1989). Does cognitiveimpairment in Parkinson’s disease result from non-dopaminergic lesions?Journal of Neurology, Neu-rosurgery, and Psychiatry, 52,201-206.

Pillon, B., Dubois, B., Bonnet, A.-M., Esteguy, M.,Guimaraes, J., Vigouret, J.-M., Lhermitte, F., &Agid, Y. (1989). Cognitive slowing in Parkinson’sdisease fails to respond to levodopa treatment: The15-objects test.Neurology, 39,762-767.

Rafal, R.D., Posner, M.I., Walker, J.A., & Friedrich,F.J. (1984). Cognition and the basal ganglia: Sepa-rating mental and motor components of perfor-mance in Parkinson’s disease.Brain, 107,1083-1094.

Raskin, S.A., Borod, J.C., & Tweedy, J.R. (1992).Set-shifting and spatial orientation in patients withParkinson’s disease.Journal of Clinical and Ex-perimental Neuropsychology, 14,801-821.

Russ, M.O., & Seger, L. (1995). The effect of taskcomplexity on reaction times in memory scanningand visual discrimination in Parkinson’s disease.Neuropsychologia, 33,561-575.

Smirnov, V.M., & Reznikova, T.N. (1985). Artificialstable functional relations as a method of researchand treatment [in Russian].Vestnik AkademiiMeditsinskikh Nauk SSSR, 9,18-23.


Taylor, A.E., Saint-Cyr, J.A., & Lang, A.E. (1987).Parkinson’s disease: Cognitive changes in relationto treatment response.Brain, 110,35-51.

Van Spaendonck, K.P.M., Berger, H.J.C., Horstink,M.W.I.M., Borm, G.F., & Cools, A.R. (1995).Card sorting performance in Parkinson’s disease:A comparison between acquisition and shiftingperformance.Journal of Clinical and ExperimentalNeuropsychology, 17,918-925.

Waterfall, M.L., & Crowe, S.F. (1995). Meta-analyticcomparison of the components of visual cognitionin Parkinson’s disease.Journal of Clinical and Ex-perimental Neuropsychology, 17,759-772.

Weinstein, A.M., Troscianko, T., & Calvert, J. (1995).Impaired visual search mechanisms in Parkinson’sdisease: A psychophysical and event-related poten-

tials study.Paper presented at the 18th EuropeanConference on Visual Perception, Tübingen, Ger-many, 21-25, August 1995. [Abstract inPercep-tion, 24, Supplement,113.]

White, O.B., Saint-Cyr, J.A., Tomlinson, R.D., &Sharpe, J.A. (1988). Ocular motor deficits in Par-kinson’s disease. III. Coordination of eye and headmovements.Brain, 111,115-129.

Willingham, D.B., Korozhets, W.J., Treadwell, J.R.,& Bennett, J.P. (1995). Comparison of Hunting-ton’s and Parkinson’s disease patients’ use of ad-vance information.Neuropsychology, 9,39-46.

Wilson, R.S., Kaszniak, A.W., Klawans, H.L., &Garron, D.C. (1980). High speed memory scanningin Parkinsonism.Cortex, 16,67-72.

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