perseverations

15
953 Journal of Clinical and Experimental Neuropsychology, 27:953–966, 2005 Copyright © Taylor & Francis Ltd. ISSN: 1380-3395 DOI: 10.1080/13803390490919092 NCEN 1380-3395 Journal of Clinical and Experimental Neuropsychology, Vol. 27, No. 08, August 2005: pp. 1–24 Journal of Clinical and Experimental Neuropsychology Is a Perseveration a Perseveration? An Evaluation of Cognitive Error Types in Patients with Subcortical Pathology Perseverations and Intrusions K. L. Possin et al. KATHERINE L. POSSIN, 1 J. VINCENT FILOTEO, 2 SCOTT C. ROESCH, 3 VANESSA ZIZAK, 2 LAURIE M. RILLING, 4 AND JENNIFER D. DAVIS 5 1 SDSU/UCSD Joint Doctoral Program in Clinical Psychology, San Diego, CA, USA 2 University of California, San Diego and the VASDHS, San Diego, CA, USA 3 San Diego State University, San Diego, CA, USA 4 UT Southwestern Medical Center 5 Brown Medical School This study investigated several constructs of executive functioning in a group of 77 patients with subcortical pathology. Specifically, we examined the validity of catego- rizing perseverative errors as “recurrent,” “stuck-in-set,” or “continuous,” as pro- posed by Sandson and Albert (1984). A principal components analysis of 2 measures of recurrent perseveration, 2 measures of stuck-in-set perseveration, and 2 measures of intrusive errors yielded a 2 component solution with stuck-in-set perseverations and intrusive errors loading on Component 1, and recurrent perseverations loading on Component 2. Presence of a continuous perseveration on a graphomotor test was sig- nificantly associated with higher factor scores on Component 1, but not Component 2. The stuck-in-set perseveration and intrusion component was associated with the majority of the other neuropsychological tests administered, including tests of execu- tive function and memory. The recurrent perseveration component was not associated with the other measures of cognitive functioning. Presence of a continuous persevera- tion was associated with executive function but not memory measures. This study pro- vides evidence that recurrent perseverations are distinct from the other types of perseverative and intrusive errors, and that stuck-in-set and intrusive errors are good indicators of general cognitive functioning in patients with subcortical pathology. Historically, the development of neuropsychological tests has been based on the assump- tion that the level of absolute performance provides useful information about the cognitive domains assessed (Lezak, 1995; Reitan & Wolfson, 1993). It is well known, however, that careful observation of behavior during the process enroute to a solution is also likely to provide useful information (Kaplan, 1988; Luria, 1966). The observation and character- ization of error types is one way to monitor the process that patients use to perform vari- ous cognitive tasks, and the use of this type of information has lead to a better Received 3 October 2003; accepted 4 August 2004. This research was supported in part by National Institute of Neurological Disorders and Stroke Grant R01 41372 to J.V.F. Address correspondence to Dr. Katherine Possin, SDSU/UCSD Joint Doctoral Program in Clinical Psychology, 4030 Haines St., Unit E, San Diego, CA, 92109. E-mail: [email protected]

description

perseveraciones en lesiones subcorticales, 2005

Transcript of perseverations

Page 1: perseverations

953

Journal of Clinical and Experimental Neuropsychology, 27:953–966, 2005Copyright © Taylor & Francis Ltd.ISSN: 1380-3395DOI: 10.1080/13803390490919092

NCEN1380-3395Journal of Clinical and Experimental Neuropsychology, Vol. 27, No. 08, August 2005: pp. 1–24Journal of Clinical and Experimental NeuropsychologyIs a Perseveration a Perseveration? An Evaluation of Cognitive Error Types in Patients with

Subcortical Pathology

Perseverations and IntrusionsK. L. Possin et al. KATHERINE L. POSSIN, 1 J. VINCENT FILOTEO,2 SCOTT C. ROESCH,3 VANESSA ZIZAK,2 LAURIE M. RILLING,4 AND JENNIFER D. DAVIS5

1SDSU/UCSD Joint Doctoral Program in Clinical Psychology, San Diego, CA,USA

2University of California, San Diego and the VASDHS, San Diego, CA, USA3San Diego State University, San Diego, CA, USA4UT Southwestern Medical Center5Brown Medical School

This study investigated several constructs of executive functioning in a group of 77patients with subcortical pathology. Specifically, we examined the validity of catego-rizing perseverative errors as “recurrent,” “stuck-in-set,” or “continuous,” as pro-posed by Sandson and Albert (1984). A principal components analysis of 2 measures ofrecurrent perseveration, 2 measures of stuck-in-set perseveration, and 2 measures ofintrusive errors yielded a 2 component solution with stuck-in-set perseverations andintrusive errors loading on Component 1, and recurrent perseverations loading onComponent 2. Presence of a continuous perseveration on a graphomotor test was sig-nificantly associated with higher factor scores on Component 1, but not Component 2.The stuck-in-set perseveration and intrusion component was associated with themajority of the other neuropsychological tests administered, including tests of execu-tive function and memory. The recurrent perseveration component was not associatedwith the other measures of cognitive functioning. Presence of a continuous persevera-tion was associated with executive function but not memory measures. This study pro-vides evidence that recurrent perseverations are distinct from the other types ofperseverative and intrusive errors, and that stuck-in-set and intrusive errors are goodindicators of general cognitive functioning in patients with subcortical pathology.

Historically, the development of neuropsychological tests has been based on the assump-tion that the level of absolute performance provides useful information about the cognitivedomains assessed (Lezak, 1995; Reitan & Wolfson, 1993). It is well known, however, thatcareful observation of behavior during the process enroute to a solution is also likely toprovide useful information (Kaplan, 1988; Luria, 1966). The observation and character-ization of error types is one way to monitor the process that patients use to perform vari-ous cognitive tasks, and the use of this type of information has lead to a better

Received 3 October 2003; accepted 4 August 2004.This research was supported in part by National Institute of Neurological Disorders and Stroke

Grant R01 41372 to J.V.F.Address correspondence to Dr. Katherine Possin, SDSU/UCSD Joint Doctoral Program in

Clinical Psychology, 4030 Haines St., Unit E, San Diego, CA, 92109. E-mail: [email protected]

Page 2: perseverations

954 K. L. Possin et al.

understanding of the nature of the cognitive deficits in different neurological disorders(Walsh, 1987).

The measurement of error types is incorporated into some standardized neuropsycho-logical tests, such as the Wisconsin Card Sorting Test (WCST; Berg, 1948; Heaton,Chelune, Talley, Kay, & Curtiss, 1993). In addition to providing scores of overall success(e.g., number of categories completed), the WCST provides an assessment of specifictypes of errors, such as perseverative responses and set losses. Likewise, the CaliforniaVerbal Learning Test (CVLT; Delis, Kaplan, Kramer & Ober, 2000; Delis, Kramer,Kaplan, & Ober, 1987) assesses not only the number of words recalled, but also measuresqualitative aspects of memory, including error types such as perseverations and intrusions.The assessment of error types has also been a growing focus in the development of newerstandardized tests, particularly those that evaluate executive functions (Delis, Kaplan, &Kramer, 2001). Successful performance on executive function tasks requires a variety ofboth fundamental cognitive skills and higher-level executive functions. Thus, the analysisof error types is an integral part of executive function assessment.

One error type that has commonly been studied in cognitive assessment is persevera-tion. In general, a perseveration is the inappropriate and unintentional persistence of abehavior, and is believed to be an index of executive functioning (Lezak, 1995). SinceNeisser first introduced the term in 1895, perseveration has been associated with a varietyof neurological diseases and syndromes (for reviews see Hotz & Helm-Estabrooks, 1995a;Sandson & Albert, 1984) and considered to be a reliable sign of brain damage when com-mitted in multitude (Allison, 1966). In the past, researchers have attempted to operationalizethis error type by delineating categories of perseverative behavior (Hotz & Helm-Estabrooks, 1995a, 1995b). For example, Sandson and Albert proposed a taxonomy ofperseverations based on an extensive literature review encompassing a wide range oftasks, patient populations, and previous taxonomies. Three specific types of persevera-tions were proposed in their taxonomy. Stuck-in-set perseveration is an inappropriatemaintenance of a current category or framework. These authors suggest that this type ofperseveration results from a dissociation of actions from intent and is related neuroana-tomically to frontal lobe damage. Recurrent perseveration is the unintentional repetition,after cessation, of a previously emitted response. In contrast to a stuck-in-set persevera-tion, a recurrent perseveration falls within the appropriate task framework, and is only anerror because it is a repetition within that framework. Sandson and Albert postulate thatthe underlying process of recurrent perseveration involves a post-facilitation of memorytraces and find that it is related neuroanatomically to posterior left hemisphere damage.Continuous perseveration is the inappropriate repetition, without interruption, of a currentbehavior. They suggest that it is caused by a disturbance in motor output and that it isrelated neuroanatomically to basal ganglia damage.

Other error types that have been used to better characterize patients’ neuropsycholog-ical test performances are intrusion errors. These types of errors, however, have beeninconsistently defined in the literature, with descriptions of these error types often over-lapping with the definitions of perseverations. For example, Loewenstein and colleagues(Loewenstein, Wilkie, Eisdorfer, Guterman, & Berkowitz, 1989) defined five types ofintrusions: test intrusions are responses related to the category or content of a previouslyadministered distractor task; shift intrusions involve material from the immediately pre-ceding distractor task; conceptual intrusions are conceptually similar to an appropriateresponse; confabulatory intrusions consist of a single percept combining two appropriateresponses; and unrelated intrusions are responses unrelated to appropriate responses onany task given. According to Sandson and Albert’s (1984) taxonomy, test and shift

JESSICA MORALES HERNÁNDEZ
Page 3: perseverations

Perseverations and Intrusions 955

intrusions comprise stuck-in-set perseverations, whereas conceptual, confabulatory, andunrelated intrusions are not reflected in their taxonomy. Similarly, Delis and colleagues(1987; 2000) define intrusions on the CVLT-I and II as responses not on the current targetlist, and according to Sandson and Albert’s (1984) taxonomy, this definition also incorpo-rates stuck-in-set perseverations by including responses on a previous target list. Double-day and colleagues (Doubleday, Snowden, Varma, & Neary, 2002) described one type ofperseveration, closely corresponding to Sandson and Albert’s “continuous perseveration,”and three intrusion types that are (a) related to previously presented test material, (b)semantically associated with the test material, and (c) not related to preceding test mate-rial. This first intrusion type subsumes Sandson and Albert’s recurrent and stuck-in-setperseverations, while the latter two are not included in their taxonomy. Thus, as can beseen, there has been some confusion and inconsistencies in the literature as to how differ-ent types of perseverations and intrusions are defined.

Despite the inconsistent definitions in the literature, however, the use of both perse-veration errors and intrusion errors have lead to a better understanding of the neuropsy-chological deficits associated with various patient populations. For example, Sandson andAlbert (1987) applied their taxonomy to the behavior of participants with left hemispheredamage, right hemisphere damage, or Parkinson’s disease (PD). They found recurrent per-severation to be associated with left hemisphere damage, continuous perseveration withright hemisphere damage, and stuck-in-set perseveration with PD. Butters, Goldstein,Allen, and Shemansky (1998) found that participants with multiple sclerosis or Hunting-ton’s disease (HD) demonstrated higher frequencies of perseverations than participantswith Alzheimer’s disease (AD) on the Information and Vocabulary subtests of the WechslerAdult Intelligence Scale (Wechsler, 1955), with perseverations defined as a combinationof the stuck-in-set and recurrent types. They concluded that these qualitative differencesmay be important for distinguishing between subcortical and cortical dementias. Usingdiscriminant function analysis with error types and learning characteristics of the CVLTas predictors, Kramer, Levin, Brandt, and Delis (1989) correctly categorized 76% ofpatients with PD, HD, and probable AD. Intrusions, recurrent perseverations, and rate offorgetting were the most discriminating variables. Patients with AD and Korsakoff diseasehave been found to make comparable levels of intrusion and perseveration rates on theCVLT (Delis, Massman, Butters, & Salmon, 1991), whereas patients with HD have a rela-tively lower rate of intrusions on this test (Kramer et al., 1988). Other studies have alsofound that analysis of perseverations and intrusions helped to better clarify the nature ofcognitive impairment in a variety of patient groups, including individuals with schizophe-nia (Perry & Braff, 1998), aphasia secondary to stroke (Helm-Estabrooks, Ramage, Bayles,& Cruz, 1998), closed head injury (Hotz & Helm-Estabrooks, 1995b), and Lewy body orAlzheimer’s dementia (Doubleday et al., 2002).

Despite the clinical utility of examining these error types, there have been someinconsistencies and overlap in how these errors have been defined, as pointed out above.Perhaps because of these issues there has been little research examining how these errorsmight relate from a conceptual standpoint, or relatedly, whether the taxonomies used todefine these errors have any construct validity. The purpose of this present study was toexamine how various types of perseverations and intrusions are related in a group ofpatients with primarily subcortical pathology using the definitions provided by Sandsonand Albert (1984). This taxonomy was chosen because it has emerged in the literature asthe most common method for delineating categories of perseveration. Patients with sub-cortical pathology were examined in this study because they often commit perseverationand intrusion errors (Butters et al., 1998; Freedman, 1990; Fung, Morris, Leicester, Soo, &

Page 4: perseverations

956 K. L. Possin et al.

Davies, 1997; Lees & Smith, 1983; Levin, Llabre, & Weiner, 1989; Sandson & Albert,1987). We studied three categories of perseverations and one category of intrusions usingvarious indices from four commonly used neuropsychological tests: the Dementia RatingScale (DRS; Mattis, 1988), the California Verbal Learning Test (CVLT; Delis et al.,1987), the Wisconsin Card Sorting Test (WCST; Berg, 1948; Heaton et al., 1993), andtests of letter (FAS) and category fluency (animals, fruits, and vegetables; AFV). Thethree specific types of perseverations were stuck-in-set, recurrent, and continuous, and theone type of intrusion examined was defined as a response inappropriate for the presenttask and all previous tasks in the testing session. Construct and operational definitions ofthese error types can be seen in Table 1. Principal component analysis (PCA) was used todetermine the relationships among these various measures of perseverations and intru-sions. If Sandson and Albert’s taxonomy provides a good account of these errors, and thethree types of perseverations are distinct, then we would expect that individual compo-nents would emerge corresponding to each of the three types of perseverations. In con-trast, if the constructs measured by the three different types of perseverations overlap, wewould expect there to be a relationship among the various types of errors under study.

Method

Participants

A total of 77 patients with subcortical pathology participated in this study: 52 patients withPD, 19 with HD, and 6 with Progressive Supranuclear Palsy (PSP). The patients werereferred from a movement disorders clinic only if they did not have a history of neurologi-cal disease (other than PD, HD, or PSP), serious psychiatric illness, or substance abuse. Allpatients were diagnosed by a board-certified neurologist who specialized in movement dis-orders. PD patients were diagnosed based on the presence of at least two of the following

Table 1Construct and operational definitions for the various error types

Construct definitions of perseverations and intrusions

Operational definitions of perseverations and intrusions

Stuck-in Set Perseveration: the inappropriate maintenance of a current category or framework.

- WCST perseverative responses - CVLT wrong list responses

Recurrent Perseveration: the unintentiononal repetition, after cessation, of a previous emitted response.

- Fluency intra-trial repeated words - CVLT intra-trial repeated words

Continuous Perseveration: the inappropriate repetition, without interruption, of a current behavior.

- Drawing repetition without interruption on the DRS graphomotor subtest

Intrusion: the production of a response inappropriate for the present task and all previous tasks in the testing session.

- CVLT non-list words- Fluency non-target words

Continuous perseverations were not included in the PCA because they were scored as a dichoto-mous variable (presence vs. absence).

Page 5: perseverations

Perseverations and Intrusions 957

symptoms: (1) resting tremor, (2) rigidity, or (3) bradykinesia. All PD patients weretreated with dopaminergic agents at the time of testing. HD patients were diagnosed basedon a positive family history for the disease and the motor symptoms associated with HD.Patients with PSP were diagnosed based on the presence of supranuclear gaze palsy andbradykinesia, and at least three other common symptoms observed in this disease (e.g.,dysarthria, axial rigidity, falls, etc.). Demographic and mean DRS scores for the patientgroups are presented in Table 2.

Scoring of Perseverations and Intrusions

A scoring system was developed to operationalize Sandson and Albert’s (1984) defini-tions of perseverations, and the definition of intrusion proposed in this study.

Stuck-in-set Perseveration. This error type is the inappropriate maintenance of a currentcategory or framework. Two measures of stuck-in-set perseverations were included in thisstudy. On the WCST, this type of perseveration was scored when a participant inappropri-ately persisted in sorting to a category despite feedback from the experimenter that thesorts were no longer correct. This type of error is labeled as a “perseverative response” inthe traditional WCST scoring system, and has previously been used to operationalizestuck-in-set perseveration (Sandson & Albert, 1984). On the CVLT, a stuck-in-set perse-veration was scored when a participant provided a “List A” word when they were asked toname “List B” words, or vice-versa. This type of error is scored as an “across-list intru-sion” on the CVLT-II1.

Recurrent Perseveration. This error type is the unintentional repetition, after cessation, ofa previously emitted response after an intervening response or intervening stimulus. Incontrast to a stuck-in-set perseveration, a recurrent perseveration is appropriately withinthe framework of the task at hand. Hotz and Helm-Estabrooks (1995b) provided the recur-rent perseveration example of a patient who is asked to repeat a list of nine words thathave just been read to him, and responds with ‘sweater, jacket, grapes, sweater.’ Twomeasures of recurrent perseveration were included in this study. On the CVLT, a recurrentperseveration was scored when a participant repeated a correct response during a giventrial after at least one intervening response. This type of error closely corresponds to a“perseveration” in the CVLT scoring system, and a “repetition error” in the CVLT-II scor-ing system, with the exception that repeated responses without an intervening response are

1We also examined stuck-in-set perseverations on the Letter and Category Fluency tests andfound that only 13 participants committed these types of errors. Because of this low occurrence, stuck-in-set errors from the fluency tests were not included in the analyses described below.

Table 2Demographic characteristics and DRS total scores of the patient groups

Age Education DRS total

N Male M SD M SD M SD

PD 52 32 66.3 9.2 14.2 3.1 134.0 7.2HD 19 8 42.6 13.4 14.2 2.1 126.5 11.6PSP 6 3 69.5 6.9 13.8 2.9 131.8 11.2

Page 6: perseverations

958 K. L. Possin et al.

also included in the traditional scoring systems. On the Letter and Category Fluency Tests,a recurrent perseveration was scored when a participant repeated a correct response afterat least one intervening response.

Continuous Perseveration. This type of perseveration is the inappropriate repetition,without interruption, of a current behavior. A continuous perseveration was scored on thegraphomotor subtest of the DRS when a participant clearly repeated a component of adrawing or an entire drawing without interruption. For example, the participant may con-tinue to draw the triangles of the ramparts drawing rather than alternating, or the partici-pant may draw circles until the end of the page rather than just one as instructed. Becausecontinuous perseveration was scored as a dichotomous variable (presence versus absenceof a continuous perseveration), it was not included in the principal components analysis,but analyzed separately for its relationship with factor scores and other neuropsychologi-cal tests.2

Intrusion. This error type was defined as a response inappropriate for the present task andall previous tasks in the testing session. Intrusions on the CVLT were scored when words noton a list that had been read were produced as responses. This error type is equivalent to “totalintrusions” on the CVLT-II, after subtracting “across-list intrusions.” However, because thisindex was not included in the original CVLT, we computed it by hand for each participant.Intrusions on letter and category fluency were scored when words that did not begin with theletter or belong to the category of the present or previous fluency tasks were produced asresponses. Proper nouns and numbers on letter fluency were also scored as intrusions giventhat participants were explicitly told not to provide these types of responses.

Neuropsychological Assessment

In order to identify how the error indices examined in the present article relate to perfor-mance on traditional neuropsychological test indices, we administered additional neurop-sychological tests to the patients. Tests administered and indices studied included the DRS(total score; Mattis, 1988), Digit Span subtest from the Wechsler Adult Intelligence Scale-Revised (WAIS-R; longest span achieved; Wechsler, 1981), Trails A and B (time to com-pletion; Reitan & Wolfson, 1985), letter and category fluency (total words produced),Digit Symbol (WAIS-R; total score), WCST (total categories achieved; Heaton et al.,1993), Vocabulary (WAIS-R; total score), Boston Naming Test (BNT; total score;Kaplan, Goodglass, & Weintraub, 1983), Block Design (WAIS-R; total score), Judgmentof Line Orientation (JLO; total score; Benton, Hamsher, Varney, & Spreen, 1983), ReyComplex Figure Test (RCFT; total score on copy, immediate recall, and 20-minute delay;Osterrieth, 1944; Rey, 1941), CVLT (total free recall of List A trials 1-5 and long delayfree recall; Delis et al., 1987), and Finger Tapping (mean taps for dominant and nondomi-nant hands across 10, 10-second trials; Reitan & Wolfson, 1985).

Data Analysis and ResultsThe patient’s error types were scored by one of two authors (KP or VZ). In order to estab-lish consistency in scoring, they simultaneously scored a randomly selected sample of 20

2Continuous perseverations were also examined on the CVLT, Letter Fluency, and CategoryFluency tests and were found to occur in only 7 participants. This low number did not allow us toinclude these errors from these tests in the analyses described below.

Page 7: perseverations

Perseverations and Intrusions 959

patient charts during a training phase. Following this training, each rater independentlyscored a random sample of 15 charts for reliability analysis. Interrater reliability was ade-quate (r=.95). Given this high interrater reliabilty, the remaining 42 charts were eachscored by one rater. Prior to analysis, the scores on the two measures of stuck-in-set perse-verations (CVLT wrong list words and WCST perseverative responses), two measures ofrecurrent perseverations (CVLT intra-trial repeated words and Fluency intra-trial repeatedwords) and two measures of intrusions (CVLT non-list words and Fluency non-targetwords) were converted to ratio scores by dividing the total number of a given error type bythe total number of responses given on that specific measure. The conversion to ratioscores was carried out because it was possible that the absolute number of errors wouldnot adequately reflect the propensity of a participant to commit such an error given thetotal number of responses provided. For example, 3 perseverations reflects a higher pro-pensity to commit these types of errors relative to 10 total responses (ratio score = .3) thanrelative to 30 total responses (ratio score = .1). Therefore, ratio scores were used in theanalyses described below. The means, medians, minimums, maximums, and standarddeviations of the ratio scores, as well as the proportion of participants who attained scoresof 0 on each measure, are presented in Table 3.

The distributions of data collected on these six error ratio scores were examined todetermine whether they met the assumptions of multivariate analysis. Univariate outlierswere identified using a z-score cut-off of 3.29 (p<.001) and visual analysis of histogramsfor scores unattached to the rest of their distribution (as suggested by Tabachnick & Fidell,2001). Two CVLT intrusion univariate outliers were identified with z-scores of 3.4 and3.2. These scores were winsorized to one point higher than the next highest score, modify-ing their z-score values to 2.26. One CVLT Recurrent Perseveration univariate outlier wasidentified with a z-score of 3.4. This score was winsorized, modifying its z-score value to2.07. Three WCST Perseverative Response scores were identified as univariate outlierswith z-scores of 3.76, 3.00, and 2.97. Although the latter two scores did not exceed ourz-score cutoff of 3.29, they exceeded the next highest score by .85 standard deviation unitsand contributed to a highly significant positive skew. These scores were winsorized, mod-ifying their z-score values to 2.14.

Table 3Descriptive statistics for perseveration and intrusion ratio scores and the proportion of par-

ticipants who attained a score of zero on each measure

Mean Median SD Min. Max Score = 0

Stuck in set perseverationsWCST perseverative responses .19 .14 .12 .00 .51 .00CVLT wrong list words .02 .01 .03 .00 .13 .43

Recurrent perseverationsFluency intra-trial repeated words .05 .04 .04 .00 .21 .16CVLT intra-trial repeated words .06 .05 .05 .00 .19 .09

IntrusionsFluency non-target words .02 .01 .02 .00 .09 .43CVLT non-list words .05 .03 .06 .00 .25 .23

Page 8: perseverations

960 K. L. Possin et al.

Using a p value of .01 for skewness and kurtosis (Tabachnick & Fidell, 2001), all 6variables had significant positive skew, and were transformed using a square root transfor-mation. The transformation reduced positive skew in all variables; however, WCST Perse-verative Responses retained a significant positive skew with a standardized score of 3.33(p < .01). Considering that the population distribution underlying this error measure isexpected to be positively skewed, and there were no distinct outliers upon visual inspec-tion of the distribution, the variable was maintained with the square root transformation.All kurtosis values were not significant after the square root transformations (p > .01).Pairwise linearity was checked using scatterplots and found to be satisfactory. Using Mahal-anobis distance with p < .001 (Tabachnick & Fidell, 2001), no multivariate outliers wereidentified.

Principal components extraction with varimax rotation was performed through SPSSFACTOR on the 6 perseveration and intrusion measures for the sample of 77 patients3.Communality values ranged from .42 to .63. All measures were maintained. The analysisyielded a two-component solution, accounting for 54% of the variance in the observedvariables. The first component accounted for 32% of the variance; the second componentaccounted for 22%.

Component loadings for each of the variables can be seen in Table 4. Variables withloadings of .45 and above are interpreted (Comrey & Lee, 1992). The following measures,found to load on Component 1 “stuck in set perseverations and intrusions,” are presentedhere with their loadings: CVLT wrong list words (.76), CVLT non-list words (.71), Flu-ency non-target words (.65), WCST perseverative responses (.64). The following mea-sures were found to load on Component 2 “recurrent perseverations”: Fluency intra-trialrepeated words (.79), CVLT intra-trial repeated words (.74). CVLT non-list words had a sec-ondary loading on Component 2 of -.34. All other secondary loadings were less than .14.

To determine whether continuous perseverations were associated with either of thecomponents derived from the PCA, factor scores for each component were derived using theregression approach in SPSS FACTOR after the principal components extraction withvarimax rotation. These scores were then correlated with the occurrence of a continuous per-severation on the graphomotor subtests of the DRS (n=26 participants who made such errors

3Principal components extraction with direct oblimin rotation was also performed to determineif the solution would change if the components were allowed to correlate. The measures loading oneach component did not change from those determined by varimax rotation and the correlationbetween the components was negligible at -.05, so varimax rotation was chosen.

Table 4Factor loadings for all indices

Component 1 Component 2

Stuck in set perseverationsWCST perseverative responses .64 −.13CVLT wrong list responses .76 −.10

Recurrent perseverationsFluency intra-trial repeated words .10 .79CVLT intra-trial repeated words −.10 .74

IntrusionsFluency non-target words .65 .05CVLT non-list words .71 −.34

Page 9: perseverations

Perseverations and Intrusions 961

vs. n=51 who did not) using point-biserial correlations. The results revealed a significantassociation between the presence of a continuous perseveration with Component 1, (rpb=.39,p < .001), indicating that those patients who committed a continuous perseveration tended toalso commit more stuck-in-set perseverations and intrusions. In contrast, the presence of acontinuous perseveration was not associated with Component 2, (rpb =.11, p=.34), suggest-ing that recurrent perseverations were not associated with continuous perseverations.

To explore the relationship between perseverative or intrusive errors and performanceon the neuropsychological tests, Pearson product-moment correlations between factorscores and traditional indices on the neuropsychological tests were calculated. Also, point-biserial correlations were performed to examine the association between the presence of acontinuous perseveration and the neuropsychological test scores. Some participants didnot receive all of the neuropsychological tests, so the range of sample size varied by corre-lation from 68 to 77. The results of these correlations are presented in Table 5.

The stuck-in-set perseveration and intrusion component (Component 1) was signifi-cantly associated with poorer performance on the DRS, Trails A and B, FAS, AFV,WCST categories, Vocabulary, BNT, Block Design, JLO, Digit Symbol, RCFT (copy andimmediate and delayed recall), CVLT (trials 1-5 and long delay free recall). The component

Table 5Correlations of neuropsychological tests with factor scores and

continuous perseveration

Neuropsychological test

F1: Stuck-in-set / intrusion (r) F2: Recurrent(r) Continuous(rpb)

DRS −.51** −.10 −.47**Digit span forward .05 −.05 .11Digit span backward −.19 −.07 −.04Trails A .30* .03 .30*Trails B .34** .07 .26*Letter fluency −.31** −.13 −.22Category fluency −.48** −.15 −.27*Digit Symbol −.40** .07 −.30*WCST categories −.61** .03 −.24*WCST set losses .20 −.11 .12Vocabulary −.27* −.01 −.30*BNT −.23* −.05 −.18Block design −.39** −.11 −.17JLO −.45** −.05 −.19RCFT copy −.47** −.21 −.27*RCFT immediate −.29* −.19 −.04RCFT delay −.30* −.14 −.08CVLT 1-5 −.43** .12 −.20CVLT long delay

free recall−.49** .11 .02

Finger Tapping D .02 .05 .02Finger Tapping N .01 .06 −.07

*p<.05.**p<.01.

Page 10: perseverations

962 K. L. Possin et al.

was not significantly associated with Digit Span forward and backward, WCST set losses,or Finger Tapping. The recurrent perseveration component was not significantly associ-ated with any test of cognitive or motor functioning administered. Presence of continuousperseveration was significantly associated with poorer performance on the DRS, Trails Aand B, AFV, WCST categories, Vocabulary, RCFT copy, and Digit Symbol. Significantassociations were not found between continuous perseveration and Digit Span forwardand backward, letter fluency, WCST set losses, BNT, Block Design, JLO, RCFT (imme-diate and delayed recall), CVLT (trials 1–5 and long delay free recall), or motor function-ing (Finger Tapping).

DiscussionThe purpose of the present study was to investigate the constructs of perseveration andintrusion in patients with subcortical pathology. Sandson and Albert (1984) differentiatedthree categories of perseverations, which they argue are distinct at the levels of clinicalfeatures, process, and neuroanatomy. This taxonomy has emerged as the most commonmethod for delineating types of perseveration in the literature. However, the relationshipbetween or independence of these categories has not been formally tested. If these types ofperseveration are distinct at the level of process and neuroanatomy, as postulated by Sandsonand Albert, we would expect across-test measures of the same error type to load togetheron components derived from a PCA, and measures of different error types to loadseparately.

Two components emerged from the PCA. The indices that loaded on Component 1were the two measures of stuck-in-set perseverations (WCST perseverative responses andCVLT wrong list words) and the two measures of intrusions (Fluency non-target wordsand CVLT non-list words). The indices that loaded on Component 2 were the two mea-sures of recurrent perseverations (Fluency intra-trial repeated words and CVLT intra-trialrepeated words). The presence of a continuous perseveration on the graphomotor subtestof the DRS was significantly associated with higher scores on Component 1, but not Com-ponent 2. Importantly, the test indices that loaded on the different components did notbreak down along specific test lines. That is, all measures from the CVLT did not load onone component, and all measures from the Fluency tests did not load on another compo-nent. Rather, the test indices that were used to define the constructs of interest a prioriwere associated with one another. These findings lend some support to the manner inwhich we operationalized the constructs.

Overall, the present results provide some support for the taxonomy proposed bySandson and Albert (1984). Specifically, the loading of the recurrent perseveration mea-sures on Component 2, orthogonal to Component 1, provides evidence that recurrentperseverations are distinct from stuck-in-set perseverations, and the lack of a correlationbetween Component 2 and the measure of continuous perseveration suggests that recur-rent perseverations are not associated with continuous perseverations. In contrast, theresults from the PCA did not support a distinction between stuck-in-set perseverationsand continuous perseverations. Specifically, Component 1, which included measures ofstuck-in-set perseverations, was significantly associated with a measure of continuousperseverations (i.e., continuous drawings on the graphomotor subtest of the DRS). In addi-tion to examining the three types of perseverative errors proposed by Sandson and Albert,we also examined whether intrusion errors were related to these three types of errors.Interestingly, intrusion errors were significantly associated with Component 1, butnot Component 2. These findings provide further support for the separation of recurrent

JESSICA MORALES HERNÁNDEZ
JESSICA MORALES HERNÁNDEZ
Page 11: perseverations

Perseverations and Intrusions 963

perseverations from the other error types. Thus, taken together, the results of the PCA pro-vide support for certain aspects of the taxonomy proposed by Sandson and Albert — thatis, the distinction between recurrent perseverations and other types of perseverations.

The patterns of relationships among the two components from the PCA and variousneuropsychological tests were also revealing. Specifically, Component 1, which encom-passed the stuck-in-set perseverations and intrusion errors, was associated with clinicaltests tapping a wide range of cognitive areas, including executive functions, language,visuospatial processes, and memory. In fact, this component correlated with 16 out of the21 indices examined from the neuropsychological battery we administered (see Table 5).These findings suggest that stuck-in-set and intrusion errors may be a general indicator ofcognitive integrity in patients with subcortical pathology. Consistent with this possibility,stuck-in-set perseveration has been associated with the current severity of cognitive func-tioning in patients with HD (Lange, Sahakian, Quinn, Marsden, & Robbins, 1995;Lawrence et al., 1996) and has been shown to be a good predictor of future cognitivedecline in non-demented patients with PD (Woods & Troester, 2003).

Given the high rate of correlations between Component 1 and the various clinicalneuropsychological tests, it was not surprising that continuous perseverations werealso correlated with a large number of the clinical measures (see Table 5). However,in contrast to the relationship between the neuropsychological measures and Compo-nent 1, the relationship between the clinical tests and continuous perseverations wassomewhat more specific. That is, continuous perseverations appeared to be associatedwith tests of general cognitive functioning (DRS), traditional measures of executivefunctioning (Trails B, AFV, WCST categories), and other measures which likely havean executive function component (Digit Symbol, Trails A, RCFT copy). Importantly,unlike Component 1, this error type did not correlate with measures of memory. Thus,despite the fact that stuck-in-set perseverations, intrusion errors, and continuous per-severations are associated, and therefore likely share at least one common underlyingprocess, there appears to be some specificity between stuck-in-set perseverations andcontinuous perseverations.

Given the findings in the present study, one important issue that arises is what mightbe the underlying cognitive processes that lead to: (a) the significant associations amongstuck-in-set perseverations, continuous perseverations, and intrusions; and (b) the separa-tion of recurrent perseverations from the other error types. One possibility is that a pri-mary deficit in inhibition accounts for the shared variance of stuck-in-set perseverations,continuous perseverations, and intrusions. This inhibitory deficit could manifest, respec-tively, as difficulty inhibiting competing previous task frameworks, a current act beyondthe time it is appropriate, or responses that were not appropriate at any time. Impairmentsin inhibition have been observed in patients with subcortical pathology (Filoteo, Rilling, &Strayer, 2002; Kensinger, Shearer, Locascio, Growdon, & Corkin, 2003) suggesting thepossibility that such a process could underlie all three of these error types4.

Given the lack of associations between recurrent perseveration and the other errortypes or traditional neuropsychological test indices, it is difficult to speculate on what cog-nitive process may be underlying this error type. Delis and colleagues (2000) suggestedthat this type of error, which they have termed “repetitions,” could reflect a deficit in mem-ory. That is, a recurrent perseveration (defined by the intra-trial repetition of a recalled word)may occur because the patient forgot that they had stated the word previously during that

4Clearly, there are many mechanisms other than inhibition that could account for the pattern ofcorrelations observed in this present study. We are simply suggesting that a deficit in inhibition isone possible account of why these error types are related.

Page 12: perseverations

964 K. L. Possin et al.

trial. It seems unlikely that recurrent perseveration results from a memory deficit per se inthe patient groups studied because this component was not significantly associated withany of the general memory measures. However, it is possible that some sort of cognitivemonitoring that is not specifically evaluated by global measures of memory (e.g., remem-bering that you remembered), similar to what Delis and colleagues described, could beassociated with recurrent perseverations.

It is also of interest to consider the neuroanatomical underpinnings of these error types.Because the patients in this study all have diseases that affect frontal-subcortical circuitry, itfollows that this dysfunction may lead to these errors in this patient group. Sandson andAlbert (1984) speculated that stuck-in-set perseveration is related neuroanatomically to fron-tal lobe damage, continuous perseveration to basal ganglia damage, and recurrent persevera-tion to posterior left hemisphere damage. If stuck-in-set perseveration and continuousperseveration are indeed subserved by damage to different but highly connected brainregions, it follows that these errors should be related at the behavioral level, while at the sametime retaining some specificity as was found in the present study. It may be that recurrent per-severation is not subserved by dysfunction of the frontal-subcortical circuits in this patientgroup, which could explain the independence of this error type at the behavioral level.

A few words of caution are in order regarding the limitations of our study. First, it isimportant to point out that the errors we examined were removed from their original met-ric to correct for the association of error probability with number of responses (use of ratioscores) and to prepare the data to meet the assumptions of multivariate analysis (modifica-tions of univariate outliers and square root transformations). These alterations make it dif-ficult to discuss clinical implications in terms of the absolute number of errors a patientmakes. Further, it is unclear if the errors studied provide novel information beyond the tra-ditional indices also derived from the same tests. However, considering that the factorscores and the traditional indices correlated in only the low to moderate range, it appearsthat they are not redundant. Future work will be required in order to determine whether thevarious errors derived from the present study have any clinical utility (i.e., predictingfuture cognitive decline in patients with subcortical pathology).

A second potential limitation of the study is that the use of other operational defini-tions of the constructs in Sandson and Albert’s taxonomy could have led to differentresults. However, we were careful to select items that we felt best reflected the varioustypes of perseverations proposed by these investigators, and the results of the PCA supportour decision for how we operationalized the constructs provided by Sandson and Albert inthat those tests that were reported to measure specific types of perseverations loaded onthe same component. Nevertheless, it will be important for future studies to examine theseconstructs of perseverations using different operational definitions.

A final cautionary note regarding our findings is that although the PCA providedsome support for Sandson and Albert’s taxonomy in patients with subcortical pathology,this may not hold true for all patient groups. As a demonstration of this possibility, Delisand colleagues (Delis, Jacobson, Bondi, Hamilton, & Salmon, 2003) found that the factorstructure of CVLT variables differed markedly in patients with Alzheimer’s disease,patients with mixed neurological disease, and normal controls. In particular, these investi-gators found that indices of delayed recall loaded together on a separate factor from indi-ces of immediate recall in the Alzheimer’s patients, whereas the measures of immediateand delayed recall loaded on the same factor in the patients with mixed neurological dis-ease and normal controls. These findings highlight that different factor structures can beobserved in different patient populations or in normal controls. Thus, it will be importantfor future studies to examine how the various constructs examined in the present study

Page 13: perseverations

Perseverations and Intrusions 965

relate in other patient populations before stronger conclusions can be drawn from thepresent study.

In conclusion, the findings from the present study provide some support for the taxon-omy of perseverations proposed by Sandson and Albert (1984). The results of the PCAdemonstrated that recurrent perseverations are likely due to a different process than arestuck-in-set perseverations and continuous perseverations. Correlational analyses usingthe clinical neuropsychological measures demonstrated that, although stuck-in-set perse-verations and continuous perseverations are related, the two error types may not be due tothe exact same processes.

ReferencesAllison, R. S. (1966). Perseveration as a sign of diffuse and focal brain damage. I. British Medical

Journal, 2, 1027–1032.Benton, A. L., Hamsher, K., de, S., Varney, N. R., & Spreen, O. (1983). Judgment of line orienta-

tion. New York: Oxford University Press.Berg, E. A. (1948). A simple objective technique for measuring flexibility in thinking. Journal of the

International Neuropsychological Society, 2, 134–140.Butters, M. A., Goldstein, G., Allen, D. N., & Shemansky, W. J. (1998). Neuropsychological simi-

larities and differences among Huntington’s disease, multiple sclerosis, and cortical dementia.Archives of Clinical Neuropsychology, 13(8), 721–735.

Comrey, A. L., & Lee, H. B. (1992). A first course in factor analysis (2nd ed.). Hillsdale, NJ:Lawrence Erlbaum associates, Publishers.

Delis, D. C., Jacobson, M., Bondi, M. W., Hamilton, J. M., & Salmon, D. P. (2003). The myth oftesting construct validity using shared variance techniques with normal or mixed clinical popula-tions. Journal of the International Neuropsychological Society, 9(6), 936–946.

Delis, D. C., Kaplan, E., & Kramer, J. H. (2001). The Delis Kaplan Executive Function System. SanAntonio, TX: The Psychological Corporation.

Delis, D., Kaplan, E., Kramer, J., & Ober, B. (2000). California Verbal Learning Test-II. San Antonio,TX: The Psychological Corporation.

Delis, D. C., Kramer, J. H., Kaplan, E., & Ober, B. A. (1987). California Verbal Learning Test:Adult version manual. San Antonio, TX: The Psychological Corporation.

Delis, D. C., Massman, P. J., Butters, N., & Salmon, D. P. (1991). Profiles of demented and amnesicpatients on the California Verbal Learning Test: Implications for the assessment of memory dis-orders. Psychological Assessment, 3(1), 19–26.

Doubleday, E. K., Snowden, J. S., Varma, A. R., & Neary, D. (2002). Qualitative performance char-acteristics differentiate dementia with lewy bodies and Alzheimer’s disease. Journal of Neurol-ogy, Neurosurgery, and Psychiatry, 72, 602–607.

Filoteo, J. V., Rilling, L. M., & Strayer, D. L. (2002). Negative priming in patients with Parkinson’sdisease: Evidence for a role of the striatum in inhibitory attentional processes. Neuropsychology,16(2), 230–241.

Freedman, M. (1990). Parkinson’s disease. In J. L., Cummings. (Ed.), Subcortical dementia (pp.108–122). London: Oxford University Press.

Fung, V. S. C., Morris, J. G. L., Leicester, J., Soo, Y. S., & Davies, L. (1997). Clonic perseverationfollowing thalamofrontal disconnection: A distinctive movement disorder. Movement Disorders,12(3), 378–385.

Heaton, R. K., Chelune, G. J., Talley, J. L., Kay, G. G., & Curtiss, G. (1993). Wisconsin Card SortingTest (WCST) manual revised and expanded. Odessa, FL: Psychological Assessment Resources.

Helm-Estabrooks, N., Ramage, A., Bayles, K. A., & Cruz, R. (1998). Perseverative behaviour influent and non-fluent aphasic adults. Aphasiology, 12(7–8), 689–698.

Hotz, G., & Helm-Estabrooks, N. (1995a). Perseveration. Part I: A review. Brain injury, 9(2),151–159.

Page 14: perseverations

966 K. L. Possin et al.

Hotz, G., & Helm-Estabrooks, N. (1995b). Perseveration. Part II: A study of perseveration in closed-head injury. Brain Injury, 9(2), 161–172.

Kaplan, E. (1988). A process approach to neuropsychological assessment. In T., Boll, & B. K.,Bryant (Eds.), Clinical neuropsychology and brain function: Research, measurement, and prac-tice. Washington D.C.: American Psychological Association.

Kaplan, E. F., Goodglass, H., & Weintraub, S. (1983). The Boston Naming Test (2nd ed.). Philadel-phia: Lea & Febiger.

Kensinger, E. A., Shearer, D. K., Locascio, J. J., Growdon, J. H., & Corkin, S. (2003). Workingmemory in mild Alzheimer’s disease and early Parkinson’s disease. Neuropsychology, 17(2),230–239.

Kramer, J. H., Delis, D. C., Blusewicz, M. J., Brandt, J, Ober, B. A., & Strauss, M. (1988). Verbalmemory errors in Alzheimer’s and Huntington’s dementias. Developmental Neuropsychology,4(1), 1–15.

Kramer, J. H., Levin, B. E., Brandt, J., & Delis, D. (1989). Differentiation of Alzheimer’s, Huntington’s,and Parkinson’s disease patients on the basis of verbal learning characteristics. Neuropsychology, 3,111–120.

Lange, K. W., Sahakian, B. J., Quinn, N. P., Marsden, C. D., & Robbins, T. W. (1995). Comparisonof executive and visuospatial memory function in Huntington’s disease and dementia of Alzheimer’stype matched for degree of dementia. Journal of Neurology, Neurosurgery, and Psychiatry, 58,598–606.

Lawrence, A. D., Sahakian, B. J., Hodges, J. R., Rosser, A. E., Lange, K. W., & Robbins, T. W. (1996).Executive and mnemonic functions in early Huntington’s disease. Brain, 119, 1633–1645.

Lees, A. J., & Smith, E. (1983). Cognitive deficits in the early stages of Parkinson’s disease. Brain,106, 257–270.

Levin, B. E., Llabre, M. M., & Weiner, W. J. (1989). Cognitive impairments associated with earlyParkinson’s disease. Neurology, 39(4), 557–561.

Lezak, M. D. (1995). Neuropsychological assessment. New York, NY: Oxford University Press.Loewenstein, D. A., Wilkie, F., Eisdorfer, C., Guterman, A., & Berkowitz, N. (1989). An analysis of

intrusive error types in Alzheimer’s disease and related disorders. Developmental Neuropsychology,5(2&3), 115–126.

Luria, A. R. (1966). Higher cortical functions in man. New York: Basic Books.Mattis, S. (1988). Dementia Rating Scale (DRS). Odessa, FL: Psychological Assessment Resources.Neisser, A. (1895). Krankenvorstellung (Fall von ‘asymbolie’). Allgemeine Zeitschrifte fur Psychiatrie,

51, 1016–1021.Osterrieth, P. A. (1944). Le test de copie d’une figure complex: Contribution a l’etude de la percep-

tion et de la memoire. Archives de Psychologie, 30, 286–356.Perry, W., & Braff, D. L. (1998). A multimethod approach to assessing perseverations in schizo-

phrenia patients. Schizophrenia Research, 33(1–2), 69–78.Reitan, R. M., & Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery.

Tuscon, AZ: Neuropsychology Press.Reitan, R. M., & Wolfson, D. (1993). The Halstead-Reitan Neuropsychological Test Battery:

Theory and clinical interpretation. Tuscon, AZ: Neuropsychology Press.Rey, A. (1941). L’examen psychologique dans les cas d’encephalopathie traumatique. Archives de

Psychologie, 28, 286–340.Sandson, J., & Albert, M. L. (1984). Varieties of perseveration. Neuropsychologia, 22, 715–732.Sandson, J., & Albert, M. L. (1987). Perseveration in behavioral neurology. Neurology, 37, 1736–1741.Tabachnick, B. G., & Fidell, L. S. (2001). Using multivariate statistics (4th ed.). Needham Heights,

MA: Allyn & Bacon.Walsh, K. W. (1987). Neuropsychology (2nd ed.). Edinburgh: Churchill-Livingstone.Wechsler, D. (1955). WAIS manual. New York: the Psychological Corporation.Wechsler, D. (1981). WAIS-R. manual. New York: the Psychological Corporation.Woods, S. P., & Troester, A. I. (2003). Prodromal frontal / executive dysfunction predicts incident

dementia in Parkinson’s Disease. Journal of the International Neuropsychological Society,9, 1, 7–24.

JESSICA MORALES HERNÁNDEZ
Page 15: perseverations