tipos de perseveracion

Neurops.vchologia, Vol. 22, No. 6, pp. 715-732, 1984. 0028-3932/84 $3.00+0.00 Printed in Great Britain. 1984 Pergamon Press Ltd.

V A R I E T I E S O F P E R S E V E R A T I O N

JENNIFER SANDSON a n d MARTIN L. ALBERT

Department of Neurology, Boston University Medical School and Boston Veterans Administration Medical Center, 150 South Huntington Avenue, Boston, MA 02130, U.S.A., and Department of Psychology,

Cornell University, Ithaca, NY 14850, U.S.A.

(Accepted 10 March 1984)

Abstract--We propose a new taxonomy for perseveration consisting of three categories which are distinctive at the levels of clinical features, process, and neuroanatomy. Stuck-in-set perseveration, the inappropriate maintenance of a current category or framework, involves an underlying process deficit in executive functioning and is related neuroanatomically to frontal lobe damage. Recurrent perseveration, the unintentional repetition of a previous response to a subsequent stimulus, involves an abnormal post-facilitation of memory traces and is related neuroanatomically to posterior left hemisphere damage. Continuous perseveration is the inappropriate prolongation or repetition of a behavior without interruption. It involves a deficit in motor output and is most common in patients with damage to the basal ganglia.

INTRODUCTION THE TERM perseveration is generally used to describe any continuation or recurrence of experience or activity without the appropriate stimulus. N~SSER [29] noted perseveration in pathological conditions as diverse as psychosis and aphasia. He considered all forms of perseverative behavior to be reflections of one undetermined underlying deficit.

LIEPMANN [22] provided the first classification schema for perseverative behaviors, divid- ing them into tonic, clonic and intentional types. A patient with tonic perseveration, as defined by Liepmann, might have difficulty releasing the hand that he had been instructed to shake. Such a patient remains stuck, unable to relax, in the final stages of a completed action. With clonic perseveration a patient continues to repeat the action in which he is engaged. When asked to draw a series of three-looped figures, for example, a patient with clonic perseveration is unable to limit his drawing to just three loops. Intentional perseveration is the unintentional repetition of a previously emitted response when a new response is intended. Liepmann cited as an example the patient who correctly blows out a match and then repeats the blowing motion to subsequent stimuli. Liepmann believed both clonic and intentional perseveration to be "ideational" in origin, "there being an impasse in the area of sensory preparation of movement with the result that new stimuli can excite a previous idea and the movement caused thereby" p. 572.

Subsequent taxonomies of perseveration have dropped the clonic form, considering

In the spring of 1983, a few months before his death, Henry H6caen and I discussed the important role of perseveration in behavioral neurology and neuropsychology. We agreed that a systematic analysis of perseveration, its influence on observed neurobehaviorai deficits and its underlying mechanisms was warranted, and that the time was ripe for such a study. We discussed hypotheses which might serve as a framework for this new study. The following theoretical statement, developed subsequently in Boston with Jennifer Sandson, was inspired by those discussions--M LA.

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716 JENNIFER SANDSON and MARTIN U ALBERT

sus t a ined ac t iv i ty as s e p a r a t e f r o m b e h a v i o r s o f repe t i t ion , a n d m a n y have cons ide red p e r s e v e r a t i o n to r e p r e s e n t a u n i t a r y n e u r o p s y c h o l o g i c a l deficit . D i f f e r e n t t a x o n o m i e s p r o p o s e d fo r p e r s e v e r a t i o n a re p r e s e n t e d in T a b l e 1.

O u r c l in ica l expe r i ence , t o g e t h e r w i t h a de t a i l ed r ev iew o f the l i t e ra tu re , revea ls the need fo r a n e w sys t em fo r c lass i fy ing p e r s e v e r a t i v e b e h a v i o r . W e sugges t t ha t ca t egor i e s wi th in this p r o p o s e d n e w c lass i f ica t ion s c h e m e a re d i s t inc t at b o t h the p h e n o m e n o l o g i c a l and the

Table 1. Classification schemas of perseveration

Type of perseveration Definition Example

Tonic

Clonic

Intent ional

Efferent motor

Perseveration due to impairment in the program of action

Compulsive repetition

Impairment of switching

Ideational

Repetitious

Continuous

Stuck

LIEPMANN [22]

inability to motoricaUy relax after completing an action continuous repetition of an action

inappropriate repetition of a previously emitted response to a subsequent stimulus

LURI^ [23] pathological inertia of a previously emitted response defect in the program of action

FREEMAN and G^~eEI~COLE [9] inappropriate repetition of a behavior repetition of an immediately preceding response to the subsequent stimulus

spontaneous recurrence of a behavior after one or more intervening stimuli

HELMICK and BERG [17] recurrence of all or part of a current or previous response after a delay

continuation of a response beyond the point of completion with no intervening stimuli

YAMADORI [38] multiple inappropriate repetitions, either in whole or in part, of a previously emitted response

continuing to grasp a hand after shaking it drawing loops across an entire page after instructions to stop after three stimulus x - . response a stimulus y ~ response b stimulus z - . response a

overwriting when attempting to draw a single circle inability to switch from one task, such as drawing loops, to another, such as alternating letters

sticking the tongue out repeatedly instead of just once appropriate production of dots on Bender Gestalt card I followed by the inappropriate use of dots instead of circles on card 2 AbcdefgAhijkAIA on attempting the alphabet

stimulus x ~ response x stimulus b - . response x as well as AbcdAefA on attempting the alphabet : continuing to manipulate sticks after completing a given design

fu-to-ko-ro-ga-ta-ma (dagger)-- fu-to-ga-ra-mi (nonsense) on second try fu-t o-ko-ro-ga-ta-na - , fu-to-ga-ra-mi

VARIETIES OF PERSEVERATION

Table l - - -cont inued

717

Type of perseveration Definition Example

Immediate repetition to the immediately nu-ka-ni-ku-gi (a proverbt--, subsequent stimulus nu-ka-ni°ku-gi either in whole or in part, of the ma-ke-ru-ga-ka-chi response to the previous stimulus {an unrelated proverb~--,

Delayed

ma-ke-ru-ku-gioga (nonsense)

nu-ka-ni-ku-gi -~ nu-ka-ni-ku-gi

ma-ke-ru-ga-ka-chi --* ma-ke-ru-ga-ka-chi

mi-ka-ra-de-ta-sa-bi mi-ka-ra-de-ta-ku-gi

repetition of a previously emitted response after one or more intervening stimuli

FULD et al. [10]

Perseveration immediate recurrence of a no examples given previously emitted response to the subsequent stimulus

Intrusion delayed repetition of a previously emitted response after intervening stimuli

process levels, and quite possibly at the anatomical level as well. In support of this argument we shall first present evidence for the three independent categories within the taxonomy: (1) continuous and inappropriate repetition of a current behavior (continuous perseveration); (2) continuous and inappropriate maintenance of a current set or framework (stuck-in-set perseveration); and (3) unintentional repetition, after cessation, of a previously emitted response to a subsequent stimulus (recurrent perseveration). Recurrent perseveration, in turn, can be either immediate or delayed, depending on whether there have been intervening stimuli between the original and perseverated responses. We shall then present evidence in support of the three distinct neuropsychological process deficits which we believe underlie the different clinical forms. The process deficit in recurrent perseveration involves a failure of the usual inhibition of memory traces. In stuck-in-set perseveration it involves a breakdown in executive functioning such that actions become dissociated from intent. In continuous perseveration it involves a disturbance in motor output characterized by post-facilitation of motor impulses. Neuroanatomical distinctions between subject groups exhibiting the different syndromes will be noted throughout. Lastly, we shall present examples of each perseverative syndrome.

EVIDENCE FOR A NEW TAXONOMY OF PERSEVERATION Perseveration on tests requiring attention and cognitive flexibility has traditionally been

associated with frontal lobe lesions (see Table 2). This preservation, in both monkeys and humans, is almost always of the stuck-in-set type. Adult monkeys with orbitofrontal lesions, for example, are severely impaired on tests such as delayed alternation and object discrimination reversal which have a large alternation component. These monkeys are not impaired, however, on visual discrimination or delayed response tasks which require spatial abilities or memory alone 1-12, 13, 28]. Humans with unilateral left or right frontal lobe

718 JENNIFER SANDSON and MARTIN L. ALBERT

Table 2. Perseveration after frontal lesion in monkey and human

Subjects Relevant tasks used Major findings

Monkeys with orbital and dorsolateral frontal lesions

MlSHKIN [28]

delayed alteration; auditory and visual discrimination in a go/no go paradigm; object discrimination reversal; learning set trials; one-trial learning; bar pressing for reward

the orbital monkeys were significantly more impaired than the dorsolateral on all the tests except delayed alternation, on which both groups were impaired. They were particularly impaired on the reversal aspect of each task. They were unable to learn to inhibit either spontaneous or experimenter-induced preferences. Lesioned monkeys were slow to extinguish bar pressing.

Monkeys with total orbital, posteromedial orbital, lateral orbital, anterior orbital and dorsolateral lesions

BUTTER 17] extinction of food rewarded response; delayed spatial reversal; object discrimination reversal

posteromedial and total orbital monkeys make more perseverative responses prior to extinction than dorsolateral or control monkeys. Total orbital monkeys had significantly more perseverative errors and perseverative error runs than dorsolateral or anterior orbital monkeys on object discrimination reversal. Dorsolateral monkeys were worse than orbital on the spatial reversal task, but the orbital monkeys were also impaired.

Monkeys with orbital, dorsolateral and total frontal ablations

GOLDMAN [12, 13] delayed response; delayed alternation; visual discrimination; object discrimination reversal

adult orbitofront al-lesioned monkeys fail to reach criterion on tests of delayed alternation and object discrimination reversal, are moderately impaired on delayed response (although better than the dorsolateral monkeys) and very mildly impaired on visual discrimination. It is concluded that they have no difficulty with the spatial or memory aspects of the tasks but rather with the reversal aspects or with perseveration. Dorsolateral monkeys seem to have a spatial memory deficit, failing to obtain criterion on delayed alternation but not on object discrimination reversal.

VARIETIES OF PERSEVERAT1ON

Table 2---continued

719

Subjects Relevant tasks used Major findings

Humans with unilateral frontal and temporal lesions for control of intractable seizures

Case study of a woman with a bilateral frontal and temporal tumor involving the thalamus and hypothalamus

Extensive clinical observation of frontal lobe patients with varying etiologies

MILNER [26, 27, 31] Wisconsin Card Sort Test; visually guided stylus mazes; delayed comparison

HUDSON [18] motor and verbal tasks involving the auditory, visual and tactile modalities

Lulu^ [23] motor tasks with and without verbal instructions

patients with both right and left frontal lesions were impaired on the Wisconsin Card Sort Test. Many patients were aware of their deficits, stating that they knew it was the color, the shape or the form, while remaining unable to alter their response strategy. Patients with right frontal lesions were significantly worse than other groups at learning to follow a stylus maze with auditory feedback. They repeatedly broke the rules and made the same errors often even when corrected. Right frontal patients were also significantly worse on a test of delayed comparison (which one of these stimuli have you seen more recently?).

the patient perseverated on tests of proprioeeption and stereognosis. Perseverations were sometimes carried over from one modality to another, resulting in bizarre behavior. The patient's drawing of a cat was particularly notable for its incorporation of the features of a man from the previous assignment. Writing showed perseveration of words and consonants.

there are two distinct types of motor perseveration.

lesions are impaired on the Wisconsin Card Sort ing Test, a task requir ing conceptual shifting [27]. A str iking aspect of this stuck-in-set perseverat ion is the abil i ty of the pat ient with frontal lobe damage to verbalize that his response should be guided by color, shape or number while consistently sticking to only one dimension.

Hudson [18] described the stuck-in-set variety of perseverat ion on verbal and non-verba l tasks involving the audi tory, visual and tactile modali t ies in a w o m a n with massive frontal lesions with thalamic and hypotha lamic extension. The pat ient ' s drawing of a cat was part icularly notable for its incorpora t ion of the features of a man from the previous assignment. Perseverat ion cont inued even when modal i ty of response was changed. Lure^ [23] reported the case of a w o m a n with a large tumor of the posterior frontal lobes who was


unable to perform without perseveration any series of motor actions such as drawing alternating shapes or performing multiple movements to command. Tasks in which the required movement differed from the examiner's signal (e.g. raise your hand when I knock) were particularly difficult. Similar perseveration was noted in writing and in calculation and was not improved with visual example. The patient, however, showed no evidence of compulsive (continuous) movements and was able to stop an initiated action appropriately. Stuck-in-set perseveration has also been observed in patients with Parkinson's disease [20] and in dementia of undetermined etiology [9].

Perseveration is also common in aphasia, where it is seen on a variety of verbal and non- verbal tasks (see Table 3). Most perseveration in aphasia seems to be of the recurrent type. ALLISON and HURWITZ [2], for example, found that 16 of 24 aphasic subjects perseverated on at least one of a series of tasks, most of this perseveration consisting of repetition of a previously emitted response to a subsequent stimulus, such as on a visual naming task. Perseveration was also common in response to simple verbal commands, in reversing automatic series and in spontaneous speech.

HELMICK and BERG [17] administered a variety of tasks to both right- and left- hemisphere-damaged (aphasic and non-aphasic) patients. Significantly more perseveration was found in the language-disturbed left-hemisphere-damaged patients than in the other groups. Perseveration followed the presentation of a subsequent stimulus 66% of the time. MATEER [24] reported significantly more perseveration, largely delayed, in aphasics on a task involving imitation of multiple oral movements than in right hemisphere controls. YAMADORI [38] reported perseveration in 33 of 38 aphasic subjects on a verbal repetition task. Again, most of the perseverations occurred after presentation of the next stimulus. There was no correlation between perseveration and type or severity of the aphasic deficit. BUCKINGHAM el d . [6] analyzed both spontaneous and elicited speech samples from two patients with jargon aphasia due to posterior parietal lesions. Delayed perseverations were found to be quite frequent and to involve single words most often. The perseverate was sometimes a slightly altered version of the original utterance and sometimes a phonological, lexical or semantic blend. SHINDLER el al. [34] reported that 83 ~o of Wernicke's, 5030 of Broca's and 38 °/o ofanomic aphasics made at least one delayed perseverative error on a series of three verbal tests. While continuous perseverations did occur occasionally, they were significantly less frequent. There was no correlation between the two types of perseveration.

Recurrent perseveration is also common in patients with dementia, especially senile dementia of the Alzheimer's type. FULD et al. [10] reported that 88~ of patients with Alzheimer's disease and 57 9o of patients with multi-infarct dementia produced at least one delayed perseveration on a neuropsychological battery. SHINDLER et al. [34] reported recurrent perseveration in 55 ° 0 of patients with Alzheimer's disease, 40 ~ with multi-infarct dementia and 20 ~o with normal-pressure hydrocephalus.

Continuous perseveration is best exemplified by LUmA'S [23] case report of a woman with a massive tumor involving both frontal lobes and the basal ganglia. This patient had no difficulty switching from one activity to the next or carrying out conditioned responses to verbal instructions. When asked to draw a circle, however, she made multiple circular movements and was unable to stop. Similar continuations were observed with writing and with tapping. Continuous perseveration has been reported in schizophrenia [9] and in normal-pressure hydrocephalus [34]. It is also cited occasionally in aphasia (e.g. [17]), but only in cases where the possibility of subcortical damage has not been definitely ruled out.

Various combinations of the perseverative syndromes are observed in many neurological conditions. In addition, normal children under 5 yr show more perseverative behavior


Table 3. Perseveration in aphasia

721

Subjects Tasks used Major findings

33 dysphasic patients of mixed etiology; unknown lesions

24 aphasic patients of mixed etiology (16 vascular); lesion location unspecified

30 brain-damaged patients: 18 aphasic, 12 non-aphasic; 28 left hemisphere, 2 right hemisphere; mixed etiology: 10 controls

20 aphasic patients: 8 non- fluent, 12 fluent; 21 non- aphasic left hemisphere patients; 21 right hemisphere patients; 27 controls

HALVERN [15] 72 words presented in visual, auditory and auditory-verbal modality for verbalization

ALLISON and HtrawiTz [2] tests involving chiefly non- linguistic activities such as searching for objects, simple drawings and simple constructions; tests of gesture and pantomime; tests of simple spoken commands; repeating and reversing the order of series; naming sighted objects; naming from memory; writing; reading; spontaneous speech

HELMICK and BF~O ['17] naming and reversing series; writing sentences and a letter; drawing designs from memory; drawing designs from verbal memory; constructing designs; naming and describing the function of sighted objects; describing a picture; defining words; answering simple questions

MATEER [24] imitation of multiple oral movements

stimuli in visual condition were perseverated the most. Perseveration correlated positively with stimulus length in all modalities and with abstraction in the visual modality. There was no correlation between perseveration and either part of speech or frequency.

16/24 subjects perseverated on at least one task. Only 5/24 perseverated on tasks involving chiefly non-linguistic activities. Perseveration was "'common" in response to simple commands, in reversing automatic series, in naming sighted objects (when the perseverate was often a blend of current and previous stimuli) and in spontaneous conversation. Perseveration was "'uncommon" in naming from memory, reading and writing. Perseveration was more "common" in the patients with the least spontaneous speech.

the brain-damaged group as a whole perseverated on 10% of all trials. There was significantly more perseveration in language- disturbed than in non-language- disturbed subjects. 66% of all perseverates were of the repetitious variety. 3470 of all perseverates were continuous. Per~everation was seen most often on the least automatic tasks. Perseveration was more common on reversing series, writing sentences and drawing designs from memory and less common on answering questions, defining words and describing a picture.

Fluent aphasics and non-aphasic patients with left hemisphere damage made significantly more perseverative errors than either right hemisphere patients or controls. 78% of perseverative errors were of the delayed variety. Right hemisphere patients did not differ from controls in terms of perseveration.


Table 3 - - con t i nued


38 aphasic patients: 24 anterior, 14 posterior; mixed etiology

Jargon aphasics

2 aphasic patients with posterior parietal lesions

20 aphasic patients: 6 Wernicke's, 8 anomic, 6 Broca's

YAMADORI [38] repetition of meaningful and non- meaningful stimuli varying in length

BUCKINGHAM et al. [5] neologistic responses from collected corpora

BUCKINGHAM et al. [6] analysis of large samples of spontaneous and elicited speech with emphasis on delayed repetitions

SHINDLER et al. [34] visual confrontation naming; word associations; WAIS vocabulary subtest

perseveration was observed in 33/38 patients. Perseveration did not correlate with severity, duration or type of aphasia. Delayed-type perseveration was observed only in response to meaningful stimuli.

neologisms contain more alliteration and assonance than would be expected by chance.

words were the linguistic unit most often perseverated. The perseverated response was not always appropriate initially. The perseverate was sometimes a slightly altered version of a previous response, sometimes a phonological, lexical or semantic blend and sometimes a neologism. The perseverate frequently had a glottal sound as if it had been cut off.

83 ~o of Wernicke's, 50% of Broca's and 38 % of anomic aphasics made at least one perseverative error. Perseveration correlated positively with naming. Intrusions correlated positively with poor hygiene and Iogorrhea and negatively with WMS information, idiom comprehen- sion and WMS verbal memory. There was no correlation between perseverations and intrusions.

(of the stuck-in-set type) than older children [32]. Normal elderly persons on a task of word list generation perseverate, as do normal young adults in spontaneous speech. It is interesting, however, that perseveration is very rarely reported after focal right hemisphere damage. See Table 4 for an overview of perseveration in the neuropsychological literature.

EXPLANATORY THEORIES OF PERSEVERATION Many different accounts of perseveration have been proposed (see Table 5 for a

summary). None of these accounts, however, is adequate to explain all three perseverative syndromes. GOLDSTEIN [14] claimed that perseveration was attributable to a catastrophic

VARIETIES OF PERSEVERATION 723

Table 4. Perseveration in neurology and neuropsychology (excluding reports in aphasia and focal frontal lesions)


20 demented patients; 20 schizophrenics

Dementia

FREEMAN and GATHERCOLE [9]

free conservation; Bender cards; stick test designs; WMS designs; body part commands; drawing; writing, cancellation of letters; WA1S similarities; WAIS vocabulary; animal naming; recitation of series; Rorschach

there was no difference in the total number of perseverations between the two subject groups. The schizophrenic subjects produced more compulsive repetitions while the demented subjects had a more difficult time switching from one set to another. There was no correlation between the tests for any of the three types of perseveration. The greatest perseveration was elicited by the Rorschach.

38. demented patients: 21 with SDAT, 17 other

FULD et al. [10] 3½-hr neuropsychologicai battery 88 ~o of patients with SDAT and

57~o of patients with MID made at least one intrusion. Intrusions were associated with low levels of ChAT and large numbers of senile plaques.

17 healthy elderly; 20 focal brain lesion patients; 22 patients with dementia other than SDAT; 22 patients with SDAT

SHINDLER,et aL [34] visual confrontation; naming; popular word associations; WAIS vocabulary subtest

55% of patients with SDAT, 407, 0 of patients with MID and 20}o of patients with NPH made at least one intrusion. Patients with NPH produced significantly more perseverations than the other groups. Perseverations correlated positively with confabulations, easy frustration, poor hygiene, laconic speech and hostility. They correlated negatively with WMS information scores and Word Association performance. There was no correlation between intrusions and any other psychometric measure.

30 newly diagnosed (untreated) patients with Parkinson's disease

Parkinson's Disease

LEES and SMITH [20] Wisconsin Card Sorting Test; Word Fluency Test

Parkinsonian patients achieved fewer categories and made more perseverative errors on the WCST than controls. Parkinsonian patients evidenced more intrusions on the third letter of the word fluency test.


Table 4---continued


30 schizopherenic patients: 15 hospitalized, 15 out-patient

12 Korsakoff patients; 15 Huntington's disease patients; 11 aphasics; 13 alcoholic controls

2 patients with left hemisphere lesions; one of the two had a fight upper quadrananopsia

3 patients with fight occipitotemporal lesions

21 autistic children; 21 controls matched for non- verbal ability

Schizophrenia SIEGEL et al. [35]

14-min free conversation on two topics---one affectively charged and the other not

KorsakofJ's disease OSCAR-BERMAN et al. [30]

delayed alternation; delayed response; differential reinforcement of low rates of responding (different subjects)

Palinopsia and palinacousis KINSBOURNE and WARRING'ION [19]

MEADOWS and MUNRO [25]

Autistic children Boocnl~g [4]

a two-choice task to which a third choice was later introduced

the same basic idea was often reiterated with a lack of movement in the train of thought in both schizophrenic groups. The hospitalized group showed a greater degree of this form of perseveration than the non- hospitalized group.

Korsakoff's patients performed poorly on both DR and DA. unlike Huntington's patients, who were only impaired on DA. They seemed to have difficulty associating the relevant stimulus cues with reinforcement and to be especially sensitive to interference. On the DRL task the Korsakoff's never learned to slow their rate of responding. Their performance, however, was normal when the delay period was ended by an auditory cue.

the perseverated images were of greater intensity and remained longer than normal after-images. In general, they conformed to the laws that govern normal imagery.

the perseverated image usually appears in the defective (neglected) left visual field. Illusions of movement sometimes occur, as do illusions of spread. Perseverated images were both persistent and recurrent.

autistic children showed less spontaneous alternation than controls and were less likely to respond to a novel stimulus.


Table 4--continued

725


children under 4½ yr; older children

23 male stutterers; 25 control college students

Review of literature on effects of lesions

Normal children

ROSE [32] spontaneous alternation; mazes; probability learning

Stutterers

SAYLES [33] critical flicker fusion threshold

Rats with hippocampal lesions

ALTMAN et al. I-3] DRL; extinction of bar pressing; reversal tasks

Normal elderly

SHINDLER et al. 134] Animal naming

Normal adults

GARRETT [11]

children over 4~ yr are almost always above chance alternators. Children under 4~ yr rarely are (only 1 in 12 alternated at a level above chance). There is a sharp drop in the number of perseverative errors made on a maze task at age 5 yr. Younger children maximize more on probability learning. They don't seem to try new hypotheses in order to gain 100% reward.

mean flicker fusion threshold was significantly lower in stutterers.

Aroused rats with hippocampal lesions tend to emit more responses than unlesioned controls~

more normal elderly subjects made intrusions on this task than did demented subjects.

The speech errors of young adults contain perseverations of segments, words and phrases.

react ion to failure on difficult tasks. Whi le fatigue and f rus t ra t ion do seem to aggrava te perseverat ive tendencies [ l-l, persevera t ion is not a lways greater on more difficult i tems or on items by which subjects are most t roubled . M a n y pat ients , in fact, are comple te ly unaware of their persevera t ions , especial ly when they are recurrent . FREEMAN and GATHERCOLE [9] repor t tha t pa t ien ts often persevera te on i tems they successfully comple te on la ter a t tempts . Relatedly, SHINDLER et al. [34,l found no cor re la t ion between persevera t ion and severi ty of cognit ive deficits in demented subjects.

WEPMAN [37] suggested that verbal perseverat ions might comprise a significant po r t i on of an aphas ic ' s deficit. He p r o p o s e d that these verbal persevera t ions were expl icable in terms of an under ly ing d i so rde r o f selective a t ten t ion . W e p m a n ' s c la im is that lexical selection and


Table 5. Theories of perseveration

Theory [ref.] Proposed to explain

Catastrophic reaction [14] Increased sensitivity to interference [27] Pathological inertia of the stimulus [23] Inertia of the program of action 123] Selective inattention [37] Abnormal conditioning [21] Motivational abnormality [30]

Abnormal facilitation of memory traces [6, 18, 38] Impaired retrieval [34] Abnormal recall of visual traces from a visual storage buffer [36] Post-activation of visual memory traces [25] Disturbance in transfer of visual memory traces to storage buffer [36]

all forms of perseverative behavior perseveration in frontal lobe patients continuous repetitions an inability to switch activities verbal perseveration in aphasia some verbal perseveration in aphasia perseveration on tasks involving a variable reinforcement schedule in Korsakoff's patients delayed verbal perseverations

verbal perseveration in aphasia and dementia visual recurrence

palinopsia visual perseveration

verbal formulation take time and that subsequent stimuli are normally inhibited, a shutter is closed, until processing is complete. This processing, however, may be considerably slowed in aphasics, resulting in a longer inattentive period. When a response to an unattended stimulus is called for, the aphasic may produce the name of the last attended item.

There are several important problems with Wepman's account, even within the verbal modality to which it is restricted. First, it does not explain delayed perseverations. Second, it does not account for the fact that verbal perseverations are frequently neologistic, blends or contextually irrelevant. Third, aphasics perseverate in spontaneous speech when they can permit themselves sufficient processing time. Fourth, changing the modality of input or of response sometimes reduces perseveration. If the perseveration were caused by the closing of an attentional shutter, modality should have no effect, as the stimulus should never be encoded. Lastly, Wepman reports verbal perseveration on tasks where subsequent stimuli are not presented until previous stimuli have been responded to and the shutter theoretically opened. Aside from the occurrence of verbal perseveration, Wepman offers no evidence for a disorder of attention in aphasics who perseverate. Wepman's observation that perseveration may constitute a significant part of the aphasic patient's deficit is, however, extremely important.

LEICESTER et al. [21] make the observation that some, although certainly not all, perseverative behavior may be due to prior reinforcement and some to use of irrelevant stimulus parameters. These particular perseverations can be explained in terms of normal behavioral principles and do not require any abnormal physiology. They offer no explanation, though, of why their aphasic subjects were more sensitive to these factors than controls and why there is such variability in this sensitivity.

LURIA [23] proposed different underlying mechanisms for the two types of motor perseveration which he observed. These two types are roughly equivalent to our continuous and stuck-in-set categories respectively. In the first type, which he called efferent


perseveration, I~oth the actual program of action and the ability to switch from one program to another remain unimpaired while a "pathological inertia of the stimulus previously initiated" results in compulsive repetition. Although never reported by Luria, efferent perseveration also occurs in speech (e.g. as multiple repetitions of a final sound). Luria's term "pathological inertia" seems to refer to a disturbance in motor output caused by abnormal post-facilitation of motor impulses.

Luria's second type of perseveration, that manifest as an inability to switch from one action to another, was viewed as the result of inertia of the program of action itself. Luria noted that tasks on which verbal instructions conflict with kinesthetic or visual cues are particularly likely to result in perseveration and emphasized the role of verbal regulation in behavioral programming [16]. This type of perseveration seems to result from a dissociation between action and intent. It is important to point out, though, that stuck-in-set perseveration can occur on purely verbal tasks on which, for example, a subject might be unable to change semantic categories.

A currently popular theory in the literature on verbal perseveration is that verbal repetitions, of the type that we are calling recurrent perseverations, are a form of involuntary recall resulting from the uncontrolled facilitatory activity of memory traces. According to HUDSON [18], there is an extended period of augmentation of memory traces which must be actively inhibited. It is a failure of this inhibition which results in the involuntary recall of previous stimuli during attempts at subsequent recall. BUCKINGHAM et al. [6] also viewed intentional perseveration as resulting from the abnormal post-activation of memory traces. They claimed that new stimuli somehow become confused with still active older traces during subsequent attempts at recall. YAMADORI [38] asserted that stuck, immediate and delayed types of perseveration (see Table 1) reflect lessening degrees of post-activation. This interpretation is problematic, though, as delayed perseveration would require the greatest period of augmentation. Repetitions of the type that Yamadori calls immediate should be classified as recurrent perseverations, as they are recurrences rather than continuations and occur as often within one context as when switching tasks. It may be that the delayed subtype of recurrent perseveration results from abnormal recall of post-facilitated items from a short-term memory buffer while the immediate subtype reflects a failure, also due to post- facilitation, in the transfer of items to that buffer.

The post-facilitation of memory traces has also been proposed to explain palinopsia and palinacousis [19, 36] and can account for recurrent perseverations on purely motor tasks. Evidence cited in support of an underlying disturbance of memory includes the frequency with which recurrent perseveration is observed in demented patients who have impaired memory (e.g. [34]) and a negative correlation between delayed recurrent perseverations and choline acetyl transferase levels [10]. DRACHMAN and LEAVITT [8] noted intrusions in normal adults administered the anti-cholinergic agent scopolamine, which is known to impair memory.

CONCLUSION AND EXAMPLES OF THE PROPOSED VARIETIES OF PERSEVERATION

In summary, we have demonstrated the existence of three distinct types of perseveration and have suggested a possible neuropsychological mechanism to account for each. Recurrent perseveration is the unintentional repetition, after cessation, of a previously

728 JENNIFER S NDSON and MARTIN L. ALBERT

emitted response to a subsequent stimulus. The underlying process seems to involve a post- facilitation of memory traces. Recurrent perseveration is most common in aphasics with left hemisphere lesions and in cases of dementia of the Alzheimer's type. Stuck-in-set perseveration is the inappropriate maintenance of a current category or framework. Patients with stuck-in-set perseveration have a disturbance in executive functioning such that actions and goals became dissociated. It is most common in patients with frontal lobe pathology. Continuous perseveration is the inappropriate repetition, without interruption, of a current behavior. It seems to be caused by a disturbance in motor output and is most common in patients with subcortical involvement.

CASE REPORTS Stuck-in-set perseveration

J.K. is a 62-yr-old right-handed male admitted to the Aphasia/Neurobehavior Unit of the Boston Veterans Administration Hospital for evaluation of dementia. He had no significant medical history until approximately 1 yr prior to admission, when memory problems were first noted. Since that time he has become progressively more irritable and has developed trouble in walking. His voice has become slurred, hypophonic and raspy. ACT scan showed moderate diffuse cortical atrophy; EEG was unremarkable.

The patient was alert and cooperative throughout the neuropsychological evaluation. Language functions were significantly more impaired than visuospatial. In particular, significant difficulties were found in object naming, word list generation, oral reading and writing. Calculation ability was severely impaired due to both computational errors and a failure to carry. Writing numbers to dictation was also poor. Memory deficits were observed for both remote and new verbal information. Immediate recall of non-verbal figures was grossly accurate. Pull to the salient features of the stimulus hindered performance across tasks.

The most striking and pervasive aspect of the neuropsychological evaluation, however, was the degree of stuck-in-set perseveration shown. This is particularly well illustrated by the patient's persistence in bisecting lines on the Trailmaking Test (see Fig. 1). Line bisection had been the appropriate response for the Cancellation Test administered earlier. Stuck-in-set perseveration was also demonstrated on Digit Span Backwards, when the patient persisted in repeating the numbers in the presented order, as in the previous task. Other examples included: failure to alternate the production of cursive 'm's and 'n's; failure to switch from addition to subtraction: and failure to point to a series of objects in order, pointing instead to each object on every trial. There were very few instances of recurrent or continuous perseveration in this evaluation.

Continuous perset'eration W.S. is a 69-yr-oid right-handed male admitted for evaluation of dementia secondary to

Parkinson's disease. Tremor of right upper and lower extremeties first led to diagnosis 18 months prior to admission. Treatment course has been notable for sensitivity to anti- Parkinsonian medications, manifested by hallucinations and paranoia. Medical history is remarkable for Paget's disease and for an automobile accident at age 29 with possible 24-hr loss of consciousness.

Attention was variable throughout the neuropsychological evaluation. Performance on visuospatial tasks was extremely slow and segmented. Pull to small details occasionally


x/x,/ (A)

(B) End @

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® @®

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CO) FIG. I. Examples of stuck-in-set perseveration. (A) Performance on a task of line bisection; (B) carryover of line bisection to a task of connecting numbered dots; (C) line bisection observed on

subsequent task of alternately connecting numbered and circled dots.


resulted in loss of set on constructional tasks. Performance was also poor on verbal tasks requiring abstraction or manipulation of knowledge. Spontaneous generation of words to categories was limited. Recall of verbal passages, however, was adequate.

The most notable aspect of this evaluation was the presence of continuous perseveration. This is best exemplified in his production of multiple loops but is also observed in drawings to command (see Fig. 2) and the Rey-Osterrieth Complex Figure. Recurrent and stuck-in-set perseveration were only rarely evident.

A B FIG. 2. Examples of continuous pcrscvcration. (A) Patient's production of three-looped figures;

(B) patient's drawing of a daisy.

Verbal recurrent perseveration H.Z. is a 63-yr-old right-handed man who developed staphylococcal osteomyelitis of the

right clavicle 7 months prior to this evaluation. A C1-C 3 laminectomy was subsequently necessitated by bacteremia and abscesses. The patient was quadriparetic but had started to improve when meningitis recurred. Simultaneous with the meningitis, the patient suffered a left hemisphere infarct with associated speech disorder and right-sided weakness. These difficulties had just resolved when a second left hemisphere infarct resulted in their recurrence.

Neuropsychological evaluation revealed severe impairment on both verbal and non- verbal tasks. Verbal testing was limited by very sparse output. There was also frequent pull to irrelevant aspects of the stimulus. Impaired pencil grip and decreased graphomotor control limited performance on constructional tasks. Contour information, however, was well utilized. Map orientation was relatively well preserved.

In addition to his other deficits, this patient clearly exemplified recurrent perseveration in the verbal modality. This was particularly evident on the vocabulary subtest of the WAIS (see Table 6). Recurrent perseveration was also observed in finger naming, on the orientation subtest of the Wechsler Memory Scale and on the Famous Faces Test. There was evidence of echolalia throughout the evaluation.

Non-verbal recurrent persereration Recurrent perscveration in the non-verbal modality is well demonstrated by J.S., a 51-yr-

old left-handed former accountant. Five years prior to admission this patient first developed


Table 6. Recurrent perseveration on the vocabulary subtest of the WAIS-R in patient H.Z.

731

Word to be defined Definition

Bed lay on Ship lay on, no ship, bed Winter winter, summer, winter, no Breakfast breakfast, bed, bacon

signs of lethargy, right-sided weakness and mutism. Neurologic evaluat ion revealed a left fronto-parieta~ infarction. Past medical history is significant for spinal surgery to alleviate chronic neck, back and leg pain. The current admission was precipitated by pain in the right arm and leg.

Residual expressive difficulties made verbal testing difficult. Preserved abstract ion ability, however, was demonstra ted on the similarities subtest of the WAIS . Visuospatiai capacities were mildly to moderately impaired. There was poor at tention to detail on the picture completion and picture ar rangement subtests. Construct ions were generally simplified. Calculations were marked by computa t iona l errors. M e m o r y was poor on tasks involving constructions but shor t - t e rm recognit ion was within normal limits. There was little incidental learning.

Recurrent perseveration was exhibited on stick design const ruct ion (see Fig. 3A), drawings to command (see Fig. 3B) and the Benton Visual Retent ion Test. The pat tern of responses on the Raven Test of Progressive Matrices was also suggestive of recurrent perseveration, as was performance on the Wisconsin Card Sorting Test.

Model

T

Memory

B

A

FIG. 3. Examples of recurrent perseveration in the non-verbal modality. (A) Performance on a task of reproducing stick designs; (B) patient's drawing of a clock with recurrence of the number 7.

Acknowled#ement--We thank Drs Edith Kaplan, Hiram Brownell and Loraine Obler, and Ms Marjorie Nicholas for advice on the development of this paper. This project is supported by funds from the Veterans Administration Medical Research Service.


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tipos de perseveracion

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clonic perseveration

intentional perseveration

tonic perseveration

noted perseveration

continuous perseveration

recurrent perseveration

term perseveration

new response